Visual Adaptation and Retinal Gain Controls

C HAP T E R 9
Visual Adaptation and Retinal Gain Controls

R OB E R T S HAP L E Y AND C HR I S T I NA E NR OT H- C UGE L L
Laboratory o f Biophysics, Rockefeller University, New York, New York 10021, USA
and
Departments of Neurobiology & Physiology, and Engineering Sciences & Applied Mathematics,
Northwestern University, Evanston, lllinois 60201, USA
CONTENTS
1. I n t r o d u c t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264
1. 1. T e r mi n o l o g y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264
1. 2. Th e P u r p o s e o f Ad a p t a t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 267
2. P s y c h o p h y s i c a l La ws o f Li g h t Ad a p t a t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 276
2. 1. Th e Ro d Sy s t e m . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 277
2. 2. Th e Co n e Sy s t e m . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 290
3. Ga i n a n d Co n t r a s t Ga i n i n Re t i n a l Ga n g l i o n Cel l s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 294
3. 1. Ga i n Co n t r o l i n t he S c o t o p i c Ra n g e . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 296
3. 2. Ga i n Co n t r o l i n t he P h o t o p i c Ra n g e . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 302
3. 3. Co n t r a s t Ga i n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303
3. 4. Ef f e c t o f Ad a p t a t i o n o n t he Si ze o f t he Re c e p t i v e Fi e l d Ce n t e r . . . . . . . . . . . . . . . . . . . . . 304
3. 5. Ad a p t a t i o n a l P o o l i n g a n d Re c e p t i v e Fi e l d Si ze . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 306
3. 6. Ga i n Co n t r o l a n d Re c e p t i v e Fi e l d Si ze Ac r o s s t he P o p u l a t i o n o f Ga n g l i o n Cel l s . . . . . . 312
3. 7. Th e Ef f e c t o f t he Re c e p t i v e Fi e l d S u r r o u n d o n t he Ga i n o f t he Ce n t e r . . . . . . . . . . . . . . 314
3. 8. A Di f f e r e n t k i n d o f Ga i n Co n t r o l : Th e Co n t r a s t Ga i n Co n t r o l . . . . . . . . . . . . . . . . . . . . . 316
3. 9. Ti me Co u r s e o f Ga i n Ad j u s t me n t i n Re t i n a l Ga n g l i o n Cel l s . . . . . . . . . . . . . . . . . . . . . . . . 318
4. Ga i n as a F u n c t i o n o f I l l u mi n a t i o n i n Ama c r i n e Cel l s , Bi p o l a r Cel l s , a n d Ho r i z o n t a l Cel l s . 320
4. 1. Ama c r i n e Cel l s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 320
4. 2. Bi p o l a r Cel l s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 321
4. 3. Ho r i z o n t a l Cel l s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 323
5. Ga i n Co n t r o l i n P h o t o r e c e p t o r s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 324
5. 1. P h o t o r e c e p t o r s whi c h Ad a p t a l ot a n d S a t u r a t e . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 325
5. 2. P h o t o r e c e p t o r s whi c h S a t u r a t e b u t d o n o t Ad a p t . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 328
6. Th e o r i e s o f Re t i n a l Ga i n Co n t r o l a n d t h e De t e r mi n a n t s o f Vi s ua l Se ns i t i vi t y . . . . . . . . . . . . . . 329
6. 1. Th e o r i e s o f t he Re t i n a l Ga i n Co n t r o l . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330
6. 2. Re t i n a l Ga i n a n d Vi s ua l Se ns i t i vi t y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 335
7. Re t r o s p e c t i v e a n d Co n c l u s i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 337
Ap p e n d i x 1 - - Re t i n a l Ne u r o n s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 337
Ap p e n d i x 2 - - Re c e p t i v e Fi e l ds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 340
Ac k n o wl e d g e me n t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 342
Re f e r e n c e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 342
263
264 R. M. SHAPLEY AND C. ENROTH-CUGELL
1. I NTRODUCTI ON
Vision is our pr i mar y sensory channel f or
i nt eract i on with t he out si de worl d. It allows us t o
recognize familiar faces and creat ures, and objects;
it allows us t o ori ent ourselves in space and t o
navigate f r om place to place. It is a pat hway f or
e s t he t i c e n j o y me n t a nd f or i n f o r ma t i o n
t ransmi ssi on. The visual system is one of t he many
miracles of nat ure.
Intensive st udy of t he visual process has revealed
t hat t he ret i na must per f or m several oper at i ons on
t he image delivered by t he eye' s optics in or der t o
make manageabl e t he di f f i cul t j obs of t he
brain : pat t ern recogni t i on and spatial localization.
One of t he basic oper at i ons t he ret i na per f or ms is
the subj ect of this chapt er: ret i nal adapt at i on. The
retinal neur ons adapt t o vari at i ons in i l l umi nat i on
by changi ng t hei r gain and response t i me course.
The pur pose of adapt at i on is t o keep t he retinal
response t o visual obj ect s appr oxi mat el y t he same
when t he level of i l l umi nat i on changes. Thus,
cent ral visual processing may pr oceed wi t hout the
brai n having to at t end t o changes in t he average
light level caused by t he daily solar cycle, by
shading, by artificial i l l umi nat i on, or by ot her ,
perhaps unpredi ct abl e, events.
We will demonst rat e the visual significance of the
retinal regulation of cont rast sensitivity at di fferent
levels of illumination. This basic funct i on of retinal
adapt at i on is so i mpor t ant f or vision t hat t here is
a hi erarchy of retinal adapt at i on mechani sms at
several di fferent sites within t he retinal net wor k.
Ther e is clear evidence for adapt at i on in individual
phot or ecept or s, in some species. Ther e is evidence
f or adapt at i on at t he level of t he out er pl exi f or m
layer of t he retina, in bi pol ar cells. Ther e is also
evidence for anot her stage of adapt at i on at the inner
pl exi f or m layer, in amacri ne cells. Adapt at i on
per f or med by the ret i nal net wor k t hus appears to
involve at least t hree mechani sms in most retinas.
Such evidence leads to t he concept of a hi erarchy
of mechani sms which may be engaged at di fferent
backgr ound levels and with di f f er ent t i me courses.
In individual cells or in the retinal net wor k, t he
neural signals sent on t o t he next stage in neural
processing usually are fed back t o regul at e the
response to new or persistent inputs. The t heori es
for adapt at i on which we shall discuss requi re
feedback in or der t o explain t he phenomena
associated with visual adapt at i on. One can t herefore
state as an overview t hat visual adapt at i on is
achieved by a hi er ar chy of feedbacks designed t o
regul at e cont rast sensitivity.
It is impossible within t he space of a review
chapt er t o deal with visual adapt at i on t o changes
in i l l umi nat i on and also t o do j ust i ce to t he subj ect
of recovery of sensitivity in t he dar k af t er all light
has been t urned off. The latter phenomenon usually
goes by t he name dark adaptation. Dark adapt at i on
is in some ways similar t o light adapt at i on but is
di f f er ent in such significant ot her ways t hat it
deserves a chapt er all its own. It is not covered in
t he fol l owi ng pages.
1.1. Terminology
Because t he fact s and t heor i es of visual
adapt at i on are compl i cat ed enough, one ought t o
be clear about t he meani ngs of words which are
used t o describe the facts, and so we will defi ne
several words which are critical f or t he ensuing
discussion. It is most i mpor t ant t o defi ne what
adaptation means, but some prel i mi nary t erms
requi re defi ni t i on first.
1.1.1. SENSITIVITY AND GAIN
Unf or t una t e l y, " s e ns i t i vi t y" has di f f er ent
meani ngs in di f f er ent fields. In psychophysi cs it
means l / t hr eshol d or, in ot her words, the reciprocal
of t he stimulus st rengt h requi red f or t he stimulus
t o be perceived reliably. Accordi ng to this meaning,
"sensi t i vi t y" is rel at ed t o t he si gnal / noi se rat i o
inside the psychophysical observer (cf. f or example,
Barlow and Levick, 1969; or Rose, 1948, 1973). The
" noi s e" in this case is caused by all the physiological
fl uct uat i ons in t he ret i na and brai n, fl uct uat i ons
which make it difficult f or an observer t o be certain
t hat a stimulus has been present ed. This " noi s e "
is caused, in t he dar k, by t her mal br eakdown of
phot opi gment in phot or ecept or s, spont aneous
r a n d o m r el ease o f n e u r o t r a n s mi t t e r s , and
fl uct uat i ons in t he physi ol ogi cal state of the ret i na
and brai n. When t he r et i na is i l l umi nat ed,
addi t i onal noise is caused by t he retinal response
t o the r andoml y arriving st ream of light quant a.
Psychophysi cal "sensi t i vi t y" can be i nfl uenced by
VISUAL ADAPTATION AND RETINAL GAIN CONTROLS
processes which change t he magni t ude of t he noise
f r om which t he signal must be pi cked out as well
as by t hose which af f ect t he size of t he signal.
I n phys i ol ogi c a l e x p e r i me n t s , t he wor d
"sensi t i vi t y" is usual l y used t o mean t he reci procal
of t he stimulus requi red t o pr oduce a neural
response of a cri t eri on size. In this meani ng of t he
wor d, noise is i gnor ed because neural responses are
usual l y averaged over a number of identical
stimulus cycles t o el i mi nat e noise as much as
possible. Ther e has been conf usi on in t he l i t erat ure
when a result on psychophysi cal sensitivity has been
t a k e n t o i mpl y s o me t h i n g de f i ni t e a b o u t
physiological sensitivity or vice versa, because in one
case noise has an ef f ect and in t he ot her it does not .
We will t r y t o avoi d conf usi on by calling
psychophysi cal sensi t i vi t y, "'sensitivity", and
physiological sensitivity, "'gain". Gai n we define as
t he r at i o of t he magni t ude of t he physi ol ogi cal
response t o t he stimulus magni t ude, in t he small-
signal range in which response is pr opor t i onal t o
t he stimulus. Gai n t hus has units like mV/ qua nt um
in phot or ecept or s, or i mpul s e/ quant um in ret i nal
g a n g l i o n cel l s. Al t h o u g h we di s t i ngui s h
physiological gain f r om psychophysi cal sensitivity,
t he t wo are rel at ed. I f t he i nt ernal noise were mor e
or less unaf f ect ed by backgr ound light, a reduct i on
in ret i nal gai n as a consequence of an increase in
backgr ound woul d pr oduce a cor r es pondi ng
r educt i on in visual sensitivity.
1.1.2. ADAPTATION
Consi der ed in t erms of sensitivity and gain, t he
one unambi guous t r adi t i onal t er m which describes
t he adapt at i on st at e is total dark adaptation, t he
st at e of highest sensitivity reached by an observer
and highest ret i nal gai n r eached by a living ret i na
t hat has been left in t ot al darkness f or a few hours.
We defi ne light adaptation as t hose vari at i ons in
t he pr oper t i es of t he visual system f r om t he t ot al l y
dar k adapt ed state which are pr oduced by vari at i on
in t he level of light. For i nst ance, light may change
the gain of the retina, or its time course of response,
or its spectral sensitivity, or its spatial summat i on
propert i es. However , an i ncrease of ret i nal noise
due t o t he r a ndom times of arrivals of light quant a
is not strictly speaki ng a pr oper t y of t he ret i na
whi ch is changed by light. But it is a f act or whi ch
coul d lead t o an increase of t he psychophysi cal
265
t hreshol d. Ther ef or e, in or der t o under st and how
light adapt at i on cont r i but es t o vision, specifically
t o t he vari at i on of visual sensitivity with mean level
of i l l umi nat i on, one must distinguish bet ween
adapt at i on and the effects of increased noise caused
by light. Similarly, as we will show, gain can be
reduced by sat ur at i on, e.g. t he l i mi t at i on on t he
ampl i t ude of response i mposed by a response
ceiling. We wish t o distinguish this ki nd of gain
reduct i on due to sat urat i on, or as it has been called
"r es pons e compr es s i on" , and t he gain cont r ol of
adapt at i on which involves a change in the properties
of t he ret i na with t i me duri ng i l l umi nat i on.
1.1.3. BRIGHTNESS, LUMINANCE, AND RETINAL
ILLUMINATION
Thr oughout our discussion, brightness means
apparent brightness, the subjective sensation of how
light or dar k an obj ect is. The obj ect i ve measure
of t he amount of light emanat i ng f r om a l umi nous
source or refl ect i ng obj ect , weighted by t he
obser ver ' s spectral sensitivity f unct i on, is called
luminance (Wyszecki and Stiles, 1967, p. 372). The
illumination falling ont o a surface f r om a di st ant
l umi nous source is pr opor t i onal t o t he l umi nance
of t he source mul t i pl i ed by t he square of t he
numeri cal aper t ur e of t he opt i cal system bet ween
source and surface. The numeri cal aper t ur e of an
opt i cal system is t he reci procal of its f - number . For
t he eye, t he numeri cal aper t ur e is pr opor t i onal t o
t he pupi l di amet er, and t he ret i nal i l l umi nat i on is
t her ef or e pr opor t i onal t o t he area of t he pupil.
Lumi nance can be expressed in t erms of effect i ve
quant a of light per unit solid angle per unit t i me
per uni t area of t he source. Il l umi nat i on can be
expressed in t erms of effect i ve quant a of light per
uni t t i me per uni t ar ea of t he surface on which t he
light is falling. We will write L f or stimulus
l umi nance and I f or retinal i l l umi nat i on, with t he
under st andi ng t hat in most experi ment s t he pupil
area is fixed and t her ef or e t he t wo quant i t i es are
si mpl y pr opor t i onal . Evi dence will be present ed
bel ow about t he i mpor t ance of t he l umi nous f l ux
of light falling on a recept i ve field. Fl ux is
illumination multiplied by area and can be expressed
in units of effect i ve quant a per unit time.
266 R. M. SHAPLEY AND C. ENROTH- CUGELL
1. 1. 4. CONTRAST, CONTRAST SENSITIVITY, AND CONTRAST
GAIN
Cont rast is a physi cal pr oper t y of t he visual
stimulus; it is the magni t ude of l umi nance vari at i on
in t he st i mul us rel at i ve t o t he aver age l umi nance.
We will show t hat t he per cept i on of cont r ast
depends upon retinal adapt at i on. There is a pr obl em
with defi ni ng cont r ast preci sel y because t here are
t wo obvi ous defi ni t i ons which di ffer appr oxi mat el y
by a f act or of t wo. In st udyi ng t he visibility of
aperi odi c obj ect s like uni f or m disks or bar s or
rect angl es on a backgr ound, t he nat ur al defi ni t i on
of cont r ast is
C = ( L o - L B ) / ( L B ) ( l a)
where Lo is the l umi nance of the obj ect and LB the
l umi nance of t he backgr ound, as i ndi cat ed in Fig.
l(a). Lo - - LB is usually called M_~ and so equat i on
(1) is usual l y wri t t en as:
C = AL/ LB. ( l b)
It is well known t hat f or t est st i mul i of l arge ar ea
the psychophysi cal sensitivity fol l ows Weber ' s Law
cont rast , which are each appr opr i at e for a part i cul ar
ki nd of st i mul us, t he t wo di f f er ent defi ni t i ons are
related because t hey refer to a single physical reality,
namel y t he rel at i ve var i at i on of a modul at ed
c ompone nt r ef er r ed t o a st eady st at e, or average,
component .
Cont rast sensitivity we defi ne as one di vi ded by
the psychophysi cal t hreshol d cont rast , either Weber
or Rayl ei gh cont r ast as t he case may be. Contrast
gain is neural response divided by st i mul us cont r ast
(Weber or Rayleigh) and will have units mV per unit
cont r ast , or ( i mpul ses/ s) per uni t cont r ast .
At low cont r ast , t he Rayl ei gh cont r ast of a
grat i ng is appr oxi mat el y one hal f t he Weber
cont r ast , as can be seen by compar i ng equat i on (1)
with equat i on (3) as appl i ed to Fig. 1. The Rayleigh
( a )
APERIODIC STIMULUS
I Background
[L, I Lo
A L T / L B = k (2a)
CT = k (2b)
where AL T is t he t hr eshol d l umi nance i ncr ement ,
and k is a const ant , t he t hr eshol d cont r ast . C is
r ef er r ed t o in t he psychophysi cal l i t erat ure as the
Weber f r act i on, but we pr ef er t o call it t he Weber
contrast, Cw.
Ther e is a second def i ni t i on of cont r ast whi ch is
used f or peri odi c spat i al pat t erns like sine grat i ngs.
Thi s is t he defi ni t i on used i mpl i ci t l y by Rayl ei gh
(1889) and mor e explicitly by Mi chel son (1927) t o
express t he visibility of i nt erference fringes:
(b)
PERIODIC STIMULUS
LMEAN
C R = ( t ma x - L mi n ) / ( L ma x +L mi n ) ( 3 )
= ( Zma x - Lmi n ) / ( 2 L . . . . )-
As seen in Fi g. l ( b) , Lma x is t he ma x i mu m
l umi nance and Lmi n the mi ni mum l umi nance in t he
spat i al l y peri odi c pat t er n. We call CR the Rayleigh
contrast. Bot h defi ni t i ons of cont r ast have been
used in t he l i t erat ure of adapt at i on, so we make
t hem explicit here. It is i mpor t ant t o realize t hat
t hough t here are t hese t wo di f f er ent defi ni t i ons of
FIG. 1. The t wo ki nds of cont r as t .
(a). We be r cont r as t is i l l ust r at ed by a one - di me ns i ona l pl ot
o f t he l umi na nc e profi l e o f a br i ght obj ect on a ba c kgr ound.
The We be r c ont r a s t is def i ned as ( Lo- LB) / LB.
(b). Rayl ei gh c ont r a s t is i l l ust r at ed wi t h t wo di f f er ent
l umi na nc e pr of i l es o f gr at i ng pat t er ns : t he upper pr of i l e is
o f a s qua r e wave gr at i ng, t he l ower is t he pr of i l e of a si ne
gr at i ng. For each gr at i ng, t he Rayl ei gh c ont r a s t is def i ned
as (Lmax-Lmin)/(Lmax+Lrnin). Thi s is equi val ent t o t he
a mpl i t ude o f t he gr at i ng di vi ded by t he me a n level, i . e.
( Lmax-Lmean) / Lmean .
VISUAL ADAPTATION AND RETINAL GAIN CONTROLS 267
cont r ast is t he mean- t o- peak ampl i t ude of t he
grat i ng di vi ded by t he mean; t he Weber cont r ast is
t he pe a k- t o- pe a k ampl i t ude di vi ded by t he
l umi nance at t he t r ough of t he l umi nance profi l e,
whi ch f or low cont rast s is appr oxi mat el y t he same
as t he mean luminance. One may t herefore compar e
measur ement s of Rayl ei gh and Weber cont r ast
sensitivities when t he stimuli are at low cont r ast ,
as in most psychophysi cal experi ment s. One shoul d
expect t he Rayl ei gh cont r ast sensitivity t o be about
twice t hat of the Weber cont rast sensitivity, because
of t he appr oxi mat e f act or of t wo di f f er ence in t he
def i ni t i on of t he t wo kinds of cont r ast . Ther ef or e,
when we write about (Weber) cont r ast sensitivity
or (Rayleigh) cont r ast sensitivity, we distinguish
t hem because of t he way t he measur ement s were
made, but we concei ve of t hem as t wo di f f er ent
measures of one underl yi ng pr oper t y of t he visual
syst em, its sensitivity f or cont r ast .
1.2. The Purpose of Adaptation
1.2.1. To MAKE THE MAGNITUDE OF THE RETINAL
RESPONSE DEPENDENT ON CONTRAST
In science as in ot her activities it is a good strategy
t o ask " Wh y ? " Thi s quest i on put s pr obl ems in
perspect i ve, and t he at t empt s t o answer " Wh y ? "
are nearl y always frui t ful . So one ought t o ask,
" Wh y is t here light a da pt a t i on? " We believe t he
answer is t hat adapt at i on keeps t he retinal response
t o cont r ast i nvar i ant with changes of i l l umi nat i on,
and t her eby achieves one maj or goal of vision:
const ancy of t he visual per cept i on of refl ect i ng
obj ect s.
Ani mal s i ncl udi ng man have evol ved in a worl d
of reflecting surfaces: water, eart h, leaves, flowers,
and ot her ani mal s. What charact eri zes a refl ect i ng
obj ect opt i cal l y is its r ef l ect ance, since t he
r e f l e c t a nc e is d e t e r mi n e d by t he phys i cal
charact eri st i cs of t he surface of t he obj ect . The
reflectance is i nvari ant with respect t o illumination,
within r easonabl e limits. The l umi nance of an
obj ect , L o, is pr opor t i onal t o t he pr oduct of t he
obj ect ' s refl ect ance, Ro, and i l l umi nat i on, I.
L o = K' Ro ' I (4)
We know f r om experi ence and experi ment (e.g.
Land and McCann, 1971) t hat over a wide range
of i l l umi nat i on t he brightness of a reflecting obj ect
does not change and t hat t he brightnesses of an
ar r ay of refl ect i ng surfaces are percei ved in t he
order of their reflectances. This leads t o the (correct)
i nference t hat the visual system must have a met hod
f or est i mat i ng somet hi ng about t he refl ect ance of
refl ect i ng obj ect s (cf. Land and McCann, 1971;
Mar r , 1982). We believe this " s ome t hi ng" is t he
cont rast (either Weber or Rayleigh contrast), which
depends onl y on t he refl ect ance, as shown below.
Fur t her mor e, one may i nfer t hat t he const ancy of
per cept i on of an obj ect as its l umi nance varies
i ndi cat es an under l yi ng const ancy of ret i nal
response t o the cont rast of t he obj ect in spite of t he
l umi nance vari at i on. For i nst ance, t he brightness
of this pri nt does not appear t o var y as t he page
is br ought closer t o or f ur t her away f r om a light
source, even t hough t he l umi nance of the pri nt may
var y by fact ors of ten. We believe t he r eason t he
pri nt appears t he same brightness is t hat t he
magni t ude of our retinal responses is the same when
our eyes sweep across t he pr i nt at each of t he
di f f er ent levels of i l l umi nat i on, because t he ret i nal
response magni t ude depends on t he cont r ast of t he
pri nt .
We will now present t he ar gument t hat t he
const ancy of ret i nal response is achi eved by means
of t he mechani sms of ret i nal adapt at i on which
pr oduce a dependence of t hat response on cont r ast
( Robson, 1975). Thi s concept arises nat ur al l y out
of a cri t i que of a st at ement of t he pr obl em by Er nst
Mach, t he great philosopher-physicist (Mach, 1865,
t r ansl at ed in Rat l i ff, 1965).
At t he end of his first paper on t he visual illusion
now called " Ma c h Bands , " Mach pr oposed a new
pri nci pl e f or psychol ogy: uni que psychol ogi cal
events must correspond to uni que physical processes
inside t he brai n. As an i l l ust rat i on of this new
principle, he of f er ed t he fol l owi ng exampl e:
"Let us examine another phenomenon with the help
of our principle, which to my knowledge no one has yet
discussed. White of a lesser intensity appears gray next
to a brighter white. On the other hand, we are never in
doubt whether we have before us a white or gray paper
even under quite different conditions of illumination: in
bright sunshine, overcast sky, in twilight, or by candle
light, we have always almost the same sensation. What
might be the cause of this? If the light intensity is 2-,3-,
2 6 8 R . M. SHAPLEY
or n- f ol d bri ght er, so t hen is t he ret i nal i mage of t he white
paper 2-, 3-, or n- f ol d br i ght er , but so al so is t he rest of
t he vi sual field a nd t he ent i re r et i na recei ves t he 2-, 3-, or
n- f ol d i l l umi nat i on. The r at i o o f t he qua nt i t y of light on
t he ent i re r et i na a nd t he i mage of t he paper r emai ns
c ons t a nt under ot her wi se equal condi t i ons , l t hi nk,
t her ef or e, t hat a pr ocess is i ni t i at ed whos e i nt ensi t y
depends on t hi s r at i o, and whi ch caus es t he s ens at i on of
whi t e for t he ret i nal i mage. The br i ght nes s of t he ret i nal
i mage is, so to speak, bei ng eval uat ed in t er ms of t he t ot al
exci t at i on. Thi s is a j udge me nt , t he psychol ogi cal side of
t he mat t er . The physi cal si de is t he pr oces s me nt i one d.
It has not yet been di s c ove r e d. "
Mach' s exampl e shows a deep insight i nt o t he
per cept i on of bri ght ness and t he pur pose of visual
adapt at i on. However , t here are some details of his
br i ef anal ysi s which are not quite right. In
appr eci at i ng what is still val i d and what needs
cor r ect i on, one may begi n t o see t he poi nt of light
adapt at i on.
We will discuss t wo related but distinct comment s
in t he quot ed par agr aph. The first is, " Whi t e of a
lesser i nt ensi t y appear s gr ay next t o a bri ght er
whi t e" . Thi s obser vat i on can be expl ai ned by
mode r n psychophysi cs which has est abl i shed t hat
the bri ght ness of an obj ect is det er mi ned, to a great
ext ent , by t he Weber cont r ast bet ween t he obj ect
and its sur r oundi ngs ( Hei nemann, 1955, 1972;
Whi t t l e and Chal l ands, 1969). However , it is al so
known t hat bri ght ness is mai nl y det er mi ned by the
contrast near the border bet ween an obj ect and its
sur r oundi ngs. Thi s surpri si ng concl usi on is forced
by t wo experi ment s. First, the brightness di fference
bet ween the t wo regi ons of unequal l umi nance
vari es di rect l y with t he shar pness of the bor der
bet ween t hem, bei ng maxi mal f or t he st eepest
bor der ( Thomas and Kovar , 1965; Shapl ey and
Tol hur st , 1973). Second, t wo regions of equal
l umi nance appear of unequal bri ght ness when a
local l umi nance di fference is i nt roduced as a bor der
bet ween t he m ( Rat l i f f , 1965; Cr a i k, 1966;
Cornsweet , 1970; Land and McCann, 1971; Shapley
and Tol hur st , 1973). See Fig. 2 f or an i l l ust rat i on
of this effect . Thus, the dependence of bri ght ness
on cont r ast , which Mach referred t o in his 1865
paper , is now known t o be mai nl y a dependence on
bor der cont r ast .
The rel at i on bet ween bri ght ness, cont r ast , and
light adapt at i on emerges f r om a critical exami nat i on
of a second r emar k made by Mach, which concerns
bri ght ness const ancy, " . . . we are never in doubt
AND C. ENROTH- CUGELL
whet her we have bef or e us a whi t e or gr ay paper
even u n d e r qui t e d i f f e r e n t c o n d i t i o n s o f
i l l u mi n a t i o n . . . " . Thi s obs e r va t i on can be
expl ai ned by the fact t hat the cont r ast of an obj ect
on a backgr ound is not changed by var i at i on in the
level of i l l umi nat i on. Thus, if the visual syst em has
the ability to derive brightness f r om cont rast , it will
t hereby achieve brightness constancy. We will at this
poi nt demons t r at e t hat cont r ast is i nvar i ant wi t h
i l l umi nat i on, and t hen show how the cal cul at i on of
cont r ast by the visual syst em can be expl ai ned in
t er ms of retinal adapt at i on.
The i nvari ance of cont r ast wi t h changes in t he
level of i l l umi nat i on can be demons t r at ed by an
exampl e. Consi der as the si mpl est case a uni f or ml y
i l l umi nat ed scene wi t h an obj ect on a backgr ound.
The si t uat i on is i l l ust rat ed in Fig. 3. The light
comi ng f r om t he obj ect side of t he bor der is
pr opor t i onal to I . Ro where I is the light falling on
the scene f r om the source of illumination, and Ro is
the reflectance of the object. The light reflected f r om
the backgr ound side of the bor der is I . R B. The
Weber cont rast is (IRo-IRB)/IR B. Dividing numer -
at or and denomi nat or by I yields (Ro-RB)/RB as the
cont r ast of an obj ect of refl ect ance Ro upon a
backgr ound of refl ect ance Ra. Thus, t he cont r ast
is independent of the level of illumination I and
depends onl y on the reflectances of obj ect and back-
gr ound.
Now we must show t hat retinal adapt at i on
provi des the mechani sm by which the visual syst em
responds to cont rast . Consi der what happens when
the recept i ve field of a retinal cell (see Appendi x 2)
crosses the bor der bet ween an obj ect and a
backgr ound, as in t he exampl e of Fig. 3. Suppose
t hat the recept i ve field is " l o o k i n g " at the
backgr ound j ust bef or e an eye movement occurs
[Fig. 3(a)], and t hat the eye movement causes t he
recept i ve field to cross t he bor der [Fig. 3(b)]. The
change in the amount of light falling on the
recept i ve field of t he neural uni t is the st i mul us
which elicits a neural signal whi ch identifies t he
bor der . The st i mul us is t hus IRo-IR w Now we
must consi der the rol e of adapt at i on. A neur on
crossing t he bor der onl y has been " l ooki ng" at the
backgr ound side of t he bor der . So t he neur on is
adapt ed to IR~. As a r easonabl e hypot hesi s about
what adapt at i on does, to be j ust i fi ed by dat a l at er,
we pr opos e it adj ust s t he gai n of the neur on t o be
VI SUAL ADAPTATI ON AND RETI NAL GAI N CONTROLS 269
FIG. 2. Br i ght ness depends on bor der cont r as t . Thi s is a n i l l ust rat i on o f t he Cr ai k - O' Br i e n - Cor ns weet i l l usi on (cf. Rat l i f f ,
1965; Cor ns we e t , 1970). The ent i r e r i ght ha l f o f t he fi el d is a ppa r e nt l y br i ght er t h a n t he l eft hal f , yet t he l umi na nc e s o f
t he t wo ha l f fi el ds ar e equal a wa y f r o m t he bor de r bet ween t h e m, as can be seen by cover i ng t he bor der wi t h a n opa que
st r i p. Near t he bor der , t he l umi na nc e is st eepl y decreasing t owa r ds t he bor der on t he da r k si de, a n d it is st eepl y increasing
t owa r ds t he bor de r on t he br i ght si de, as can be seen in t he l u mi n a n c e pr of i l e dr a wn u n d e r n e a t h t he p h o t o g r a p h .
(a)
/ I - R o = L o
R e c e p tiv e ~
Field ~) , i ~ /I'RB=LB
Bockground
(b) Receptive
F i e l d , )
B a c k g ro u n d
FIG. 3. The invariance of contrast with changes in level of
illumination, and how this is sensed by a visual cell's receptive
field. This picture shows the luminance profile of an object
(with reflectance R o) on a background (with reflectance RB)
when both are illuminated uniformly, with illumination L
The position of the receptive field of an individual retinal
cell is indicated by the shaded rectangle. In (a), the visual
cell is "looking" at the background. In Co), an eye movement
has carried the receptive field of the cell onto the object.
Equation (5) in the text demonstrates that this cell will respond
to the Weber contrast of the object on the background, i.e.
(Ro-RB)/RB, which is independent of illumination L As
explained in the text, in order for this calculation to work
the cell must be influenced by a gain control which adjusts
the cell's gain to be reciprocal with background illumination.
pr opor t i onal t o t he reci procal of t he val ue of t he
i l l umi nat i on at which t he cell' s recept i ve field has
been " l o o k i n g " up t o t he moment it crosses t he
border. This inference is suggested by Weber' s Law,
equat i on (2). Thus t he signal in our hypot het i cal
ne ur on will equal t he st i mul us I' Ro-I' RB
multiplied by t he gain, K/(I. RB), where K is a pro-
por t i onal i t y const ant . The concl usi on is t hat what
t he visual system uses t o charact eri ze an obj ect is
a signal
S =K" (I 'Ro-I " RB)/I " RB (5)
which is pr opor t i onal t o the Weber cont rast . In this
case t he neural response t o t he obj ect is i nvari ant
with respect t o changes in t he i l l umi nat i on, I. Thi s
chai n of reasoni ng onl y hol ds i f t he gain of t he
ret i na is reci procal with backgr ound i l l umi nat i on,
in anal ogy with Weber ' s Law. When ret i nal gain
is not reci procal with backgr ound, one shoul d
expect devi at i ons f r om brightness const ancy.
This line of reasoni ng leads t o t he concl usi on t hat
t he det ect i on of cont r as t depends on light
adapt at i on. A di f f er ent view is t hat t he dependence
of ret i nal responses on cont r ast is a consequence
of t he spatially ant agoni st i c c e n t e r - s u r r o u n d
organi zat i on of receptive fields (discussed bel ow in
Appendi x 2), but we believe this view t o be
i ncorrect . I f t her e are eye movement s, spatial
cont r ast will be " s e e n " by t he highly localized
recept i ve fields of ret i nal neur ons as successive
cont rast , or in ot her words as t empor al modul at i on
of t he amount of light falling on t hose recept i ve
fields ( Hel mhol t z, 1909). As shown above, in this
si t uat i on, t he mechani sms of adapt at i on t oget her
with t he compact nat ur e of t he recept i ve fields
pr oduce a response dependent on cont r ast wi t hout
any r equi r ement f or a spat i al l y ant agoni st i c
sur r ound. The pur pose of havi ng recept i ve field
surrounds pr obabl y is t o make retinal neurons mor e
sensitive t o pat t erns with nar r ow spatial gradi ent s,
or high spatial frequenci es, t han t o coarse pat t erns
or di ffuse light. Put anot her way, with light
adapt at i on but wi t hout recept i ve field sur r ounds,
r et i nal neur ons woul d r es pond t o cont r ast .
However, with receptive field surrounds but wi t hout
adapt at i on, t he ret i na woul d be unabl e t o r espond
t o cont rast ; it woul d sat urat e qui ckl y (see Sect i on
1.2.2.). This poi nt of view is similar t o t hat put
f or war d by Whi t t l e and Chal l ands (1969).
Consi derat i on of Mach' s st at ement t oget her with
mor e recent wor k on brightness const ancy under
condi t i ons of non- uni f or m i l l umi nat i on leads t o an
i nt erest i ng concl usi on about t he spatial spread of
adapt at i on. Mach, and ot hers af t er hi m (Heri ng,
1920; Hel son, 1964), have supposed t hat t he eye
compared, "t he quant i t y of light on the entire retina
and t he i mage of t he pa pe r " , in or der t o cal cul at e
the brightness of t he paper. This is not correct . The
first correct i on is t hat brightness depends on a local
phenomenon, t he cont r ast near t he bor der of an
obj ect , not on t he quant i t y of light in t he i mage of
t he obj ect (see Fig. 2). Second, t he ret i na does not
compar e t he quant i t y of light " o n the entire r et i na"
with t he amount of light in t he obj ect , as Mach
suggested. As Davi dson and Fr eeman (1965) and
Land and McCann (1971) have shown, brightness
is const ant under condi t i ons of spatially non-
uni f or m i l l umi nat i on. We have argued t hat ret i nal
272
adapt at i on is t he basis of bri ght ness const ancy. I f
ret i nal adapt at i on aver aged light " o n t he ent i re
r et i na" as Mach supposed, it coul d not pr oduce
bri ght ness const ancy when t he i l l umi nat i on was
spat i al l y non- uni f or m. Ret i nal gai n woul d be the
same at all poi nt s on t he ret i na. Neur al signals at
one poi nt on t he ret i na woul d be at t enuat ed t o t he
same ext ent as neural signals f r om anot her regi on
of unequal l ocal i l l umi nat i on. The cor r ect
cal cul at i on of the bor der cont r ast by t he ret i na
would br eak down. This implies t hat the retinal gain
cont r ol mechani sm must be somewhat localized, as
i ndeed phys i ol ogi c a l evi dence d e mo n s t r a t e s
(Cl el and and Enr ot h- Cugel l , 1968 among ot hers).
Mach and ma ny ot hers later, including Land and
McCann (1971), pr opos ed t hat t he vi sual syst em
cal cul at ed t he r at i o I Ro/ I RB = Ro/ RB directly,
but this is i ncorrect , pr obabl y f or the fol l owi ng
reason. The rat i o Ro / Rs is nearl y al ways close t o 1
in nat ur e because t he ( achr omat i c) refl ect ances of
most nat ur al obj ect s are so nearl y the same. I f
Ro/ RB were the quant i t y bei ng measur ed, correct
i dent i fi cat i on of whet her an obj ect is bri ght er or
dar ker t han t he backgr ound woul d become a
pr obl em of accurat e measur ement and compar i s on
of t he rat i o wi t h 1. The Weber cont r ast as defi ned
earlier is the difference between the reflectance ratio
and 1. That is, (Ro-RB)/RB = ( Ro/ Ra) - l . The
Weber cont r ast , ( Ro- RB) / R B, changes sign f or
obj ect s bri ght er t han the backgr ound (posi t i ve
cont r ast ) compar ed t o obj ect s dar ker t han t he
backgr ound (negative cont rast ). The change of sign
l eads t o a mu c h eas i er , l ess e r r o r - p r o n e
di scr i mi nat i on of dar k f r om bri ght obj ect s t han
would comput at i on of the refl ect ance rat i o Ro/ RB.
Fur t her mor e, t he vi sual syst ems of ver t ebr at es put
the basic meas ur ement of t he sign of t he cont r ast
i nt o t he f unct i onal archi t ect ure of t he ret i na (cf.
Her i ng, 1920). Cells whi ch are excited by posi t i ve
cont r ast (the " o n " cells of Har t l i ne, 1938; and t he
" on- c e nt e r " cells of Kuf f l er , 1953) are segregat ed
f r om the cells which are excited by negative cont rast
( " o f f " cells of Har t l i ne and " o f f - c e n t e r " cells of
Kuf f l er ) . As di scussed in Appe ndi x 1, t he
el abor at i on of these " o n " and " o f f " pat hways
involves separ at i on of ret i nal synapt i c connect i ons
in t he inner pl exi f or m l ayer of t he ret i na, as
suggested by Fami gl i et t i and Kol b (1976), and t hen
pr oven by Fami gl i et t i et al. (1977) and Nel son et
R. M. SHAPLEY AND C. ENROTH-CUGELL
al. (1978). These physi ol ogi cal and anat omi cal
obs er vat i ons r ei nf or ce t he pur el y f unct i onal
hypot hesi s t hat the ret i na is designed t o measure the
cont r ast of obj ect s in or der to pr ovi de t o t he br ai n
an i l l umi nat i on- i nvar i ant descri pt i on of the worl d
of obj ect s. Spat i al l y localized light adapt at i on is a
cruci al f act or in this retinal f unct i on.
1.2.2. TO HANDLE THE LARGE RANGE OF
ILLUMINATION LEVELS
A rel at ed r eason f or the necessity of light
adapt at i on is t he very extensive r ange of aver age
light levels pr esent ed t o t he eye by nat ure. A white
paper (refl ect ance = 1) in moonl i ght has a
l umi nance of about 3 x 10 -2 cd m-L A white paper
in sunlight is six orders of magni t ude bri ght er,
about 3 x 104 cd m- L Backgr ounds whi ch af f ect
vi si on ext end t hree log units bel ow refl ect ed
moonl i ght and one log unit above reflected sunlight,
a t ot al r ange of about 10'% Par t of this enor mous
r ange is t aken care of by paral l el processi ng in
separ at e r od and cone pat hways. In humans f or
exampl e, the highly sensitive rod syst em handles the
t hree l owest decades of backgr ounds . The less
sensitive cone system handles the upper six log units,
and the decade of order 0.1 cd m -2 is shared (Riggs,
1965). However , in ot her ani mal s the overl ap of the
ranges of backgr ound handl ed by r od and cone
systems may di ffer because of a di fferent rod - cone
weighting. For i nst ance, in t he cat in which the
r od - cone rat i o is about one hundr ed times great er
t han in man (St ei nberg et al., 1973), t he r od syst em
handl es five log units r at her t han t hree and the
cones onl y domi nat e visual r esponses above
10 cd m -2 in backgr ound. A t abl e which expresses
the l umi nances in st andar d units and in t er ms of
quant a of light per second per degree squar ed in
area, is of f er ed as Tabl e 1.
A human is so sensitive when dar k adapt ed t hat
he can detect (wi t hout any false posi t i ve responses)
t hat a light fl ash has been pr esent ed when onl y
about one hundr ed quant a of light are i nci dent on
his cor nea (Nagel, 1909; Hecht et al., 1942; cf.
Cor nsweet , 1970). When one t akes i nt o account
l osses in t he eye and t he i nef f i ci ency of
t r ansduct i on, this implies t hat about t went y retinal
responses t o quant a of light are requi red f or such
ul t ra-rel i abl e visual per f or mance (this is a hi gher
numbe r t han est i mat ed by Hecht et al., 1942, and
TABLE I. Quantal Equivalents of Photometric Units and some Other Useful
Equivalences
P h o t o me t r i c Un i t E q u i v a l e n t i n Qu a n t a
1 c d m -2
t h r o u g h 1 mm ~
p u p i l , s c o t o p i c
(1 s c o t o p i c t d, h u ma n )
1 c d m -2
t h r o u g h 1 mm ~
p u p i l , p h o t o p i c
(1 p h o t o p i c t d , h u ma n )
1 l u me n ( s c o t o p i c )
1 l u me n ( p h o t o p i c )
Ot h e r Us e f u l Eq u i v a l e n c e s
4. 46. l 0 s q u a n t a ( 5 0 7 n m) ( de g 2 s) -t
1. 26. 106 q u a n t a ( 5 6 0 n m) ( deg 2 s) -1
1. 4. 1015 q u a n t a ( 5 0 7 n m) s -1
4 . 2 . 1 0 is q u a n t a ( 5 6 0 n m) s -1
Un i t Us e f u l E q u i v a l e n t
1 q u a n t u m( 5 0 7 n m) s - ' 4 . 1 0 -' 9 wa t t s
1 q u a n t u m( 5 6 0 n m) s -I 3. 5" 10 -' 9 wa t t s
1 d e g 2 o n h u ma n r e t i n a 8. 5" 10 -4 c m 2
1 d e g 2 c a t r e t i n a 4 . 8 - 1 0 -4 c m 2
273
is based on mor e recent estimates of quant um
efficiency by Barlow, 1977). However, Sakitt (1972)
has shown t hat i f one relaxes t he st ri ngent
requi rement of no false positives, human observers
can do bet t er t han chance when on t he average onl y
a single quant um of light excites t he ret i na. Thi s
must mean t hat a single quant um response is
compar abl e in magni t ude t o t he i nt ra-ret i nal dar k
noise. Compar abl e sensitivity is possessed by ot her
ani mal s.
The high sensitivity of a dar k adapt ed eye poses
a pr obl em when t he obser ver moves i nt o bri ght er
surroundi ngs. Al most all neur ons have a limited
response range, f r om small signals t o the peak levels
set by bi ol ogi cal cons t r ai nt s such as i oni c
equilibrium potentials. The range of responses is no
great er t han a f act or of one hundr ed f r om noise t o
ceiling. The pr obl em is obvi ous. How can t he r od
pat hway in t he ret i na encode t hr ee t o five log units
of stimulus level when it onl y has a f act or of one
hundr ed in response t o wor k with? The answer is
it cannot , and it does not . The ret i na adapt s
(reduces its gain) in t he presence of large average
inputs in or der t o represent onl y modul at i ons
ar ound t he average level when the average becomes
t oo large t o handle with t he high dar k adapt ed gain.
This pr obl em of sat ur at i on of neural responses
is rel at ed t o t he need f or stable cont r ast sensitivity,
which we have argued is t he mai n pur pose of
adapt at i on. I f t he ret i na did not adapt , t he cont rast
gain and cont rast sensitivity woul d pl ummet at high
light levels. Thus we woul d become blind t o
reflecting objects in bright daylight. This woul d not
be a stable survival st rat egy, and t her ef or e t here is
a biological need f or adapt at i on. In fact , as our
review of t he psychophysi cal and physi ol ogi cal
results will show, t he cont r ast sensitivity and
cont r ast gai n of humans and ani mal s general l y
increase as t he i l l umi nat i on increases, fi nal l y
levelling of f t o asympt ot i c values in bri ght light. At
this poi nt we will demonst r at e how t he sat ur at i on
of neural response woul d lead t o a decline in
cont r ast gain. Then we will present a suggestion f or
an adapt at i on mechani sm whi ch of f er s an escape
f r om t he " s at ur at i on cat as t r ophe" .
Fi rst let us consi der how t he Na k a - Ru s h t o n
equat i on, whi ch appr oxi mat el y describes t he
i nt e ns i t y- r e s pons e f unct i on of distal ret i nal
n e u r o n s , woul d l ead t o a " s a t u r a t i o n -
cat as t r ophe" if t he ret i na did not adapt . This is t he
Na k a - Rusht on equat i on:
R = ( I / ( I + Is)) Rmu (6)
where R is t he response of t he neur on measur ed as
t he change in membr ane pot ent i al f r om its t ot al l y
dar k adapt ed level, I is t he i l l umi nat i on of t he
stimulus. Is is t he semi -sat urat i on const ant also
equal t o the illumination at which R reaches its half-
maxi mal value. This equat i on ( Naka and Rusht on,
1966) is called t he Mi c ha e l i s - Ment en equat i on by
Bayl or and colleagues (Bayl or and Hodgki n, 1973;
274
Ba y l o r e t al . , 1974; Ba y l o r e t al . , 1979) a f t e r a
s i mi l a r e q u a t i o n whi c h ar i s es i n t he t h e o r y o f
e n z y me ki net i cs . Th e e q u a t i o n de s c r i be s a s ys t e m
whi ch s a t ur a t e s . Fi gur e 4 s hows a g r a p h o f R/ Rma x
vs / p l o t t e d on l i n e a r - l i near c oor di na t e s , a n d it can
be seen t h a t R is a s a t u r a t i n g f u n c t i o n o f I : a b o v e
t he va l ue I s , t he l i ght c a n i nc r e a s e by s ever al
o r d e r s o f ma g n i t u d e b u t t he r e s p o n s e , R, c a n
i nc r e a s e at mo s t b y a f a c t o r o f t wo.
t he a mo u n t o f r e s p o n s e pe r a mo u n t o f c o n t r a s t ,
t hus :
Gco n = dR/(dI /I a) = dR/ dl og/
= ~/ ( ~r / &)
( 8 )
a n d t o c a l c ul a t e t he c o n t r a s t ga i n f or a n e u r o n
whi c h obe ys t he Na k a - R u s h t o n r e l a t i o n we
s ubs t i t ut e e q u a t i o n (7) i nt o e q u a t i o n (8) t o o b t a i n :
g
E
or-
1 . 0 -
0.8 - ~
0.6
0.4
0.2
0 I I
0 200 400
I I
600 800
ILLUMINATION
FIG. 4. The Naka-Rusht on relation. This is a plot of
( R/ Rmax) =I / ( I +I s) , the Na k a - Rushton relation, on
l i near-l i near coordinates. As can be seen, the relation
produces a compressive nonlinear curve; the response
saturates when I > I s. In this example, the semi-saturation
illumination, I s, was chosen to be 100 in arbitrary units.
As a r g u e d by Wi l l i a ms a n d Ga l e (1977), Na k a e t
al. (1979), No r ma n n a n d P e r l ma n (1979c), a n d
Va l e t o n a n d v a n No r r e n ( 1 9 8 3 ) , t h e
Na k a - R u s h t o n e q u a t i o n c a n be us ed t o de s c r i be
ga i n a n d c o n t r a s t ga i n i n e x p e r i me n t s i n whi c h t he
s t i mul us is a n i n c r e me n t o n a b a c k g r o u n d , b y
e xa mi ni ng how an i nc r e me nt a l r e s pons e h R de pe nds
on a n i n c r e me n t a l s t i mul us h / s u p e r i mp o s e d on a
b a c k g r o u n d I B. I n t h i s c a s e t h e I i n t h e
Na k a - R u s h t o n e q u a t i o n is IB + h i , t he r e s pons e
is R B + AR, a n d t he ga i n is d R / d I ~- A R / A I , when
h i is s mal l . The ga i n c a n be c a l c u l a t e d by
d i f f e r e n t i a t i n g e q u a t i o n (6) ( Wi l l i a ms a n d Ga l e ,
1977; Na k a e t al . , 1979):
d R / d I = [ l / ( / a + / s ) ] 2 / s R m a x
~ { 1/ (&2)}. (/sRmax) f o r / a > > / s (7)
Th e We b e r c o n t r a s t ga i n Gcon c a n be d e f i n e d as
Gcon = / s R ma x " I a / ( / B + / s ) 2
"-~ ( / s R ma x ) " 1 / ( [ a ) a s / B > > I s .
(9)
Wh a t t hi s me a n s is t h a t on a c c o u n t o f s a t u r a t i o n
t he We b e r c o n t r a s t ga i n wo u l d de c l i ne as t he
a mo u n t o f s t e a d y b a c k g r o u n d l i ght i nc r e a s e d, i n
i nve r s e p r o p o r t i o n t o t he a v e r a g e l i ght l evel . Th u s
t he " s a t u r a t i o n - c a t a s t r o p h e " is i mp l i c i t i n
e q u a t i o n (9). Fi g u r e 5 i l l us t r a t e s t he ga i n a n d t he
1.0 ~ / - - ~ , N \ x - - Goin
--- Cont r osf Get n
D 0.8 x x \
a . 0 . 6 "-.~
~ 0 . 4 ~
~ 0 . 2
o " 7 - - - ~ 1 1 -..
o 200 4 0 0 6 0 0 8 0 0
ILLUMINATION
FIG. 5. The gain and (Weber) contrast gain of the
Na ka - Rushton relation. Gain is drawn as the continuous
curve and contrast gain as the dashed curve. The saturating
nature of the Naka - Rushton relation causes the gain to be
a monotonically decreasing function of illumination [cf.
equation (7)], while the contrast gain has a peak at I = I s
(which was chosen to be 100 as in Fig. 4).
c ont r a s t gai n ( equat i ons 7 a nd 9) f or a n e u r o n whi ch
obe ys t he Na k a - R u s h t o n r e l a t i o n . I f t he r e t i n a
wo u l d not a d a p t , t he ( We b e r ) c o n t r a s t ga i n wo u l d
d r o p as t he l i ght l evel i nc r e a s e d.
Th e r e t i n a a d a p t s t o a v o i d s a t u r a t i o n by h a v i n g
an " a u t o ma t i c ga i n c o n t r o l " ( Ros e, 1948); t he gai n
o f t he r et i na is r e duc e d af t er t he r e c e pt i on o f e nough
l i ght , so t ha t t he n e u r a l r e s p o n s e u s u a l l y d o e s n ' t
s a t u r a t e i n t he p h y s i o l o g i c a l r a n g e o f i l l u mi n a t i o n .
We wi l l ha ve a l ot t o s a y a b o u t t he me c h a n i s m o f
t hi s a u t o ma t i c ga i n c o n t r o l , wh e n we di s c us s t he
experi ment al psychophysi cal and physiological ~00
dat a. It is wort h observing how an aut omat i c gai n "~
t~
cont rol solves the probl em of the " s at ur at i on x
300.
cat ast r ophe" formal l y. One requires t hat R is not
t;x
simply a funct i on of the i l l umi nat i on I but depends
200
on I times a gai n fact or, g, which depends on the
value of I at present and in the recent past. Thus "
g i s a " f u n c t i o n a l " o f I ( t ) , g = g { t , I ( t ) } , b u t w e w i l l ~ loo
write it simply as g{IB} t o si mpl i fy the algebra.
This si mpl i fi cat i on is reasonabl e since we are onl y
0
anal yzi ng the case of an i ncrement on a st eady
backgr ound, in which case g woul d be fixed at a
st eady state level set by the backgr ound. The
Na k a - Ru s h t o n equat i on modi fi ed to include
adapt at i on becomes:
R/Rmm, = g{ I B} ' I / ( g{ I B} ' I + Is) (lOa)
which can be expressed anot her way by dividing
numer at or and denomi nat or by g{Is}, as follows:
(10b)
R/Rm~,= I /[I + (I s/g{I B})]
= I / ( I + I s ' )
in which I s' = Is/g{Ia}.
The effect of adapt at i on can therefore be t hought
of, t o a first appr oxi mat i on, as changi ng the value
o f t he s e mi - s a t u r a t i o n c o n s t a n t i n t he
Na k a - Ru s h t o n equat i on, Is (Dawis and Purpl e,
1982). This change in t he semi -sat urat i on const ant
has been observed in retinal neurons; of t en it is
referred t o as "cur ve- shi f t i ng" because when
e qua t i on (10b) is gr a phe d on l i n e a r - l o g
coordi nat es, the curve translates t o the right as I s'
increases ( Nor mann and Werbl i n, 1974; Werbl i n,
1977; Nor mann and Perl man, 1979c among others).
Fi gure 6 illustrates the phenomenon of "cur ve-
shi ft i ng" in cat retinal ganglion cells, from the work
of Sakmann and Creut zfel dt (1969). Sat urat i on is
post poned by this strategy. Wi t h the appropri at e
choice of t he g funct i onal , one can obt ai n Weber' s
Law wi t h such a modi fi ed Naka - Rusht on model
(Dawis and Purpl e, 1982; Valeton and van Norren,
1983).
It can also be shown t hat such a model can avoid
the probl em of cont rast gain falling at high light
levels, as follows. In anal ogy with equat i on (9) we
can derive the cont rast gain of the modi fi ed
275
I I
9.10 -s
I l I I
9.10 ~ 9 10 -3 9 10 "z 9.10 -I 9
t est spot t umi nonce ( c d / r n 2)
Fr o. 6. " Cu r v e - s h i f t i n g " i n cat r et i nal ga ngl i on cell
r es pons es . Pe a k r e s pons e o f a cat r et i nal ga ngl i on cell (in
spi kes s -1) t o a t est s pot f l as hed on a b a c k g r o u n d , as a
f unc t i on o f t est s pot l umi na nc e , at six di f f er ent b a c k g r o u n d
l umi nances . The ba c kgr ound l umi na nc e s ar e i ndi cat ed in t he
f i gur e above a n d t o t he l eft o f each cur ve, i n uni t s o f l og
cd m -2 (di l at ed pupi l ) . The t est s pot was 0. 5 dog i n di amet er
a nd was directed t o t he receptive field cent er. The backgr ound
was 30 dog i n di amet er , a n d was o n c ont i nuous l y. The
s t i mul us s pot was on f or 500 ms , a n d was pr es ent ed
repet i t i vel y at 0. 2 Hz. The r es pons e me a s ur e was t he n u mb e r
o f i mpul s e s i n t he 50 ms af t er s t i mul us ons e t mi n u s t he
n u mb e r o f i mpul s es i n a c ompa r a bl e cont r ol per i od. Twe nt y
r es pons es were aver aged f or each poi nt . Fr o m S a k ma n n a n d
Cr eut zf el dt (1969).
Na k a - Rusht on model:
Gco.' = I s " Rm,~,'IB/(IB + I s ' ) 2
and since adapt at i on keeps In<< I s ' , the cont rast
gai n is approxi mat el y:
Gcon' ~Rmax Is/Is'= R m a , , ' g { I a } I a / I s ( l l )
whi ch can be kept al ways i ncr easi ng and
approxi mat el y const ant at high backgrounds by the
correct choice of the dependence of the g functional,
and t herefore I s ' , on t he backgr ound. As will be
seen, the ret i na usually makes this correct choice.
Summi ng up, we may say t hat adapt at i on is
necessary t o prevent sat urat i on which woul d
otherwise depress the cont rast sensitivity (cf.
Adel son, 1982). In discussing psychophysical and
electrophysiological results on sensitivity and gain,
we will show how the processes of light adapt at i on
count eract the t endency of visual neurons to
sat urat e.
It may be instructive t o consider Fechner' s
integration of Weber' s Law (equation 2) as anot her
proposed answer t o the probl em of providing
276 R. M. SHAPLEY AND C. ENROTH- CUGELL
const ant cont rast sensitivity (Boring, 1950). Fechner
pr opos ed t hat a cert ai n fixed a mount of change in
i nt ernal sensat i on was requi red f or t hreshol d. We
can call this val ue ArT. He t hen pr opos ed t hat Ar T
was pr opor t i onal t o M/IB which is also fixed at
t hr eshol d in t he Weber ' s Law range. The crucial
as s umpt i on was t hat r, the i nt ernal a mount of
sensat i on, was si mpl y a f unct i on of t he a mount of
light I; t hus r = r(/). Wi t h this assumpt i on, Fechner
coul d t hen t reat Weber ' s Law as an appr oxi mat i on
to a di fferent i al equat i on f or r. Thus, A/ / I coul d
be appr oxi mat ed by a di fferent i al dI/I, while the
i ncr ement in sensat i on Ar coul d be appr oxi mat ed
by the di fferent i al dr. Thi s led to Fechner ' s
di fferent i al equat i on:
dr = a. dI / I (12a)
obj ect i ons, one may say t hat Fechner arri ved at t oo
shal l ow an i n t e n s i t y - r e s p o n s e curve because his
t heor y was t oo si mpl e (see Sperl i ng and Sondhi ,
1968 f or a si mi l ar poi nt of view).
Havi ng discussed the funct i onal role of the retinal
gai n cont r ol in st avi ng o f f s at ur at i on and
mai nt ai ni ng hi gh cont r ast sensitivity, we will now
consi der psychophysi cal results on t he dependence
of visual sensitivity on the backgr ound or mean level
of i l l umi nat i on. A critical issue is, t o what ext ent
is sensitivity det ermi ned by noise and to what extent
by retinal adapt at i on? Then we will consi der the
pr oper t i es and mechani sms of retinal adapt at i on.
2. P S YCHOP HYS I CAL LAWS OF L I GHT
ADAP T AT I ON
where a is a pr opor t i onal i t y const ant . I nt egr at i ng
this equat i on, he obt ai ned,
r = a. l og(/ ) + rl (12b)
where r, is the response at I = 1. Fechner ' s Law
(12b) is not ri ght , as can be seen bot h t heoret i cal l y
and empi ri cal l y. First, the t heoret i cal obj ect i on is
t hat r may not be vi ewed, wi t hout adequat e
j ust i f i cat i on, as a si mpl e f unct i on of the val ue of
/, t he light, i ndependent of t he past hi st ory of
i l l umi nat i on. Because it is now well known t hat t he
ret i na and br ai n have a finite t i me course of
response, and r esponse ampl i t ude and t i me course
ar e mo d i f i e d by t he p r e v i o u s h i s t o r y o f
i l l umi nat i on, we now must consi der r to be a
t r ans f or mat i on of /, or, t o be t echni cal , a
functional. Ther ef or e, t he mat hemat i cal f or ms of
equat i ons (12a, b) are not j ust i fi ed. Fur t her mor e,
t her e are empi r i cal consequences of Fechner ' s
t heor y. Fechner ' s r easoni ng leads us t o believe t hat
We be r ' s Law implies t hat r must be pr opor t i onal
t o log L Thi s is a ver y shal l ow sat ur at i ng f unct i on
of L The much st eeper Na k a - Rus ht on equat i on
is act ual l y obs er ved. I n essence, Fe c hne r ' s
expl anat i on of Weber ' s Law is in t er ms of response
c o mp r e s s i o n on a v e r y ge nt l y s a t u r a t i n g
i n t e n s i t y - r e s p o n s e f unct i on, r at her t han t he
cor r ect expl anat i on in t er ms of aut omat i c cont r ol
of gai n on a much st eeper i n t e n s i t y - r e s p o n s e
cur ve. Combi ni ng t heor et i cal and empi r i cal
As pr opos ed in t he Introduction, we believe light
adapt at i on t o be an essential retinal mechani sm f or
a l l owi ng e f f o r t l e s s , i l l u mi n a t i o n - i n v a r i a n t
eval uat i on of the optical characteristics of reflecting
objects. One har dl y ever is awar e of adapt at i on
when it is per f or mi ng this f unct i on. However , the
effect s of adapt at i on become not i ceabl e when one
observes self-luminous sources of light: st ars,
l amps, candles, and televisions. These visual objects
change in bri ght ness when t he ambi ent level of
i l l umi nat i on changes. When the light level is high
enough, t hey di sappear f r om view compl et el y; t hey
fall bel ow t he per cept ual t hr eshol d f or i ncrement s.
Thus t he act i on of light adapt at i on is exposed by
t he dai l y cycle of t he fadi ng and r eappear ance of
t he stars, t hough adapt at i on is wor ki ng unobt r u-
sively all t he t i me t o keep t he per cept i on of
refl ect i ng obj ect s unaf f ect ed by t hat same cycle.
The i nfl uence of ambi ent i l l umi nat i on on t he
sensitivity f or l umi nous sources like st ars and
candl es has been not i ced since ant i qui t y. A poet i c
descr i pt i on and psychol ogi cal expl anat i on was
of f er ed by Shakespeare in The Merchant of Venice.
As Por t i a and Neri ssa ret urn t o Por t i a' s villa
Bel mont at night af t er t he t r i umph over Shyl ock in
Venice, t hey speak about sensat i on and percept i on:
P ORT I A
Th a t l i ght we see is bur ni ng in my hal l .
How f ar t hat little candl e t hr ows hi s be a ms ,
So shi nes a good deed in a n a u g h t y wor l d.
VI SUAL ADAPTATI ON AND RETI NAL GAI N CONTROLS 2 7 7
NERISSA
When the moon shone we did not see the candle.
PORTIA
So doth the greater glory dim the less.
A substitute shines brightly as a king
Until a king be by, and then his state
Empties itself, as doth an inland brook
Into the main of waters . . . .
(Act V, Scene 1, II. 89-97).
Th e ba s i c p h e n o me n o n is a c c u r a t e l y d e s c r i b e d
he r e , t he f a d i n g t o d i s a p p e a r a n c e o f a we a k
i n c r e me n t o n a b a c k g r o u n d . Si nce t he b a c k g r o u n d
was mo o n l i g h t i n S h a k e s p e a r e ' s " e x p e r i me n t " ,
Ne r i s s a mu s t ha ve b e e n o b s e r v i n g l i ght a d a p t a t i o n
o f t he r o d s ys t e m. Thi s we n o w c o n s i d e r mo r e
q u a n t i t a t i v e l y .
2.1. The Rod System
2.1.1. SENSITIVITY AS A FUNCTION OF BACKGROUND
2.1.1.1. Aguilar and Stiles' experiment. A ba s i c
f act o f vi s ua l e xpe r i e nc e is t h a t t he s e ns i t i vi t y f or
i nc r e me nt s o f l i ght is r e duc e d b y s t e a dy b a c k g r o u n d
i l l u mi n a t i o n . We wi l l r evi ew t he p s y c h o p h y s i c a l
i n v e s t i g a t i o n s o f t hi s p h e n o me n o n i n o r d e r t o
a n s we r t he q u e s t i o n , " t o wh a t e xt e nt is t he l os s o f
vi s ual s ens i t i vi t y d u r i n g i l l u mi n a t i o n c a us e d by t r ue
l i ght a d a p t a t i o n o f t he vi s ual s ys t e m, a n d t o wh a t
e xt e nt is i t c a u s e d b y i n c r e a s e d " n o i s e " i n t he
s t i mu l u s i t s e l f ? "
The c a n o n i c a l d a t a c o n c e r n i n g t he d e p e n d e n c e o f
t he p s y c h o p h y s i c a l t h r e s h o l d o n t he l evel o f
b a c k g r o u n d i l l u mi n a t i o n a r e t h o s e o f Ag u i l a r a n d
St i l es (1954; Fi g. 7). Th e s t i mul i wer e c h o s e n t o
s t i mu l a t e t he r o d s ys t e m mo s t e f f e c t i ve l y. Th e
s t i mul us was l a r ge (9 d i a me t e r di s k) , p r e s e n t e d i n
t he p e r i p h e r y o f t he vi s ua l f i el d, a n d wa s o f a
b l u e - g r e e n c o l o r o n a r e d b a c k g r o u n d . Th e r e d
b a c k g r o u n d de s e ns i t i z e d t he c one s ys t e m r e l a t i ve l y
mo r e t h a n wo u l d a whi t e b a c k g r o u n d , a n d t he
b l u e - g r e e n t es t d i s k s t i mu l a t e d t he r o d s mo r e
e f f e c t i ve l y c o mp a r e d t o c one s t h a n wo u l d a whi t e
s t i mul us . Th e s t i mu l u s was p r e s e n t e d f or 0. 2 s
whi c h a l l o we d t he r o d s t o s u mma t e t he i r s i gnal s
t e mp o r a l l y . I n t hi s way, Ag u i l a r a n d St i l es wer e abl e
_ _ g
0 -- 4
g
4-' t~
~ .g g
0 lxl ,I-
ra 0 / ,' 2 ~
4-"
E - I -
I1)
b B
~ - 2 - - - - I
Scare 06
- 3 1
- - - - 0. 4
~ ~ - - 0 . 2
- 4
- 4 - 2 0 2 4
L o g ( f i e L d r a d i a n c e , s c o t o p i c r o L a n d s )
FIG. 7. Human " r o d " threshold as a function of
background illumination. The stimulus was a 9 deg disk on
a 20 deg background presented 9 deg from the fovea. The
disk was blue - green and the background was red in color,
in order to enhance rod responses compared to cone
responses. The stimulus was presented for 200 ms. The
background was continuous. Curve A is the threshold
illumination vs background. Curve B is what we would call
the Weber contrast at threshold, and is labeled the "Fechner
fraction" in this graph. From Wyszecki and Stiles (1967);
original data replotted from Aguilar and Stiles (1954).
t o i s ol a t e t he r o d s ys t e m a n d s t u d y i t s p r o p e r t i e s
ove r a wi de r r a nge o f b a c k g r o u n d s t h a n ha s us ua l l y
be e n pos s i bl e . On e uni t mu s t be d e f i n e d i n o r d e r
t o u n d e r s t a n d t he i r r e s ul t s , t he uni t o f r e t i na l
i l l u mi n a t i o n , t he t r o l a n d ( a b b r e v i a t e d t d) . I n
h u ma n s , a l u mi n a n c e o f 1 cd m -2 vi e we d t h r o u g h
a p u p i l wi t h a n a r e a o f 1 mm 2 i s s ai d t o g e n e r a t e
a r et i nal i l l umi na t i on o f 1 t d. The val ues o f t r o l a n d s
i n mo r e p h y s i c a l uni t s is gi ve n i n g r e a t de t a i l b y
Wy s z e c k i a n d St i l es (1967).
As Ag u i l a r a n d St i l es d e s c r i b e d t he i r d a t a , t he
f i r s t ma j o r f e a t u r e s h a r e d b y s e ve r a l o b s e r v e r s was
t h a t wh e t h e r t h e r e was z e r o b a c k g r o u n d o r a
b a c k g r o u n d b e l o w 2 . 1 0 -3 t d , t h e t h r e s h o l d
278
r emai ned const ant and equal t o t he absol ut e
t hr eshol d [Fig. 7 (curve A)]. In t he human,
2. 10 -a td of ret i nal i l l umi nat i on is equi val ent t o
about 1000 quant a(507 nm) (deg 2 s) -1 i nci dent on
t he cor nea (Wyszecki and Stiles, 1967). Thi s is t he
range of backgr ounds in whi ch t he sensitivity is
l i mi t ed by i nt ernal noise in t he obser ver , t he so-
called " d a r k - l i g h t " (Barl ow, 1957, 1965). Then
Agui l ar and Stiles observed t hat the t hreshol d began
t o rise and t he sensitivity began t o fall when t he
backgr ound exceeded 2. 10 -3 td. At backgr ounds
above 10 -2 td (equi val ent t o r oughl y t he or der of
10 -3 cd m -2 wi t h a 3 mm pupi l ), t he t hr eshol d was
equal t o a const ant t i mes t he backgr ound: Weber ' s
Law.
MT = kwlB
t han 10-' td, consi st ent wi t h t he val ue r epor t ed by
Fuor t es et al. (1961) and slightly hi gher but close
t o Bl ackwel l ' s (1946) val ue. The r o d - cone br eak
depends on retinal locus since, f or exampl e, t here
can be no r o d - c o n e br eak in t he al l -cone f ovea.
The number s cited above have been t aken f r om
psychophysi cal i nvest i gat i on of t he near peri phery,
5 - 1 0 f r om fovea.
2. 1. 1. 2. The square root law and "' noise". As
was first made clear by Rose (1948), the r od- dr i ven
visual syst em is of t en st arved f or light quant a and
works right up against the limit i mposed by quant al
noise in t he st i mul us and the backgr ound. Under
such condi t i ons, t he ul t i mat e l i mi t at i on on visual
per f or mance will be neural noise caused ei t her by
f l uct uat i ons in the light, or by f l uct uat i ons in the
(13) sensor y pr oper t i es of the obser ver , or bot h. Thi s
has defi ni t e i mpl i cat i ons about dependence of
sensitivity on backgr ound l umi nance. The f or m of
t he human sensitivity versus backgr ound curve
depends on exper i ment al condi t i ons (e.g. st i mul us
size, dur at i on, wavel engt h) and does not al ways
(14) l ook like the curve obt ai ned by Agui l ar and Stiles
(1954; Fig. 7, curve A). It is likely t hat over much
of the visual range in t he real worl d of white stimuli
on a white backgr ound, the rod-dri ven visual syst em
does not at t ai n t he ideal condi t i on of adapt at i on,
We be r ' s Law.
The effect s of quant al noise and i nt ernal noise
on the dependence of sensitivity on backgr ound are
i l l ust rat ed especi al l y dr amat i cal l y in Fig. 9 f r om
Bar l ow (1965). He ar r anged a r od- i s ol at i on
i ncrement t hreshol d experi ment to illustrate the four
di f f er ent regi mes whi ch can be seen in the human
sensi t i vi t y' s dependence on backgr ound. The
st i mul us was a bl ue green spot 0.75 in di amet er ,
of 8 ms dur at i on, pr esent ed 10 f r om t he f ovea on
a 10 or ange backgr ound. I f t he st i mul us had been
smal l er in area, the sensitivity woul d have been
f l uct uat i on- l i mi t ed f r om the regi on l abel ed " d a r k
l i ght " to " r o d s at ur at i on" . I f it had been of l onger
dur at i on and l arger in area, t he curve woul d have
l ooked like t he results of Agui l ar and Stiles (1954).
The l i mi t at i on on sensitivity at the low end of t he
backgr ound scale is usual l y at t r i but ed to " d a r k
l i ght " r at her t han t o the quant al f l uct uat i ons f r om
the backgr ound (Barl ow, 1957, 1964, 1977). I n this
regi on of backgr ounds it is supposed t hat quant al
f l uct uat i ons f r om t he backgr ound light are smal l
Thus t he sensi t i vi t y S = 1/(AIT) is i nver sel y
pr opor t i onal t o backgr ound in t he We be r ' s Law
range:
S = l / ( kw' I B) = k ' w' l / ( I n) .
Above 102 td (equi val ent t o 5.107 q(507 nm)
(deg 2 s) -1 i nci dent on t he cornea), the i ncr ement
t hreshol d rose mor e steeply t han Weber ' s Law. This
is what woul d be expect ed f or a syst em whi ch
sat urat es. For exampl e, a syst em whi ch obeyed t he
Naka - Rusht on equat i on (6), whi ch is one ki nd of
sat ur at i on, ul t i mat el y has a t hr eshol d which
depends on t he squar e of t he backgr ound level, as
shown in our equat i on (7) above. Ther ef or e, t he
sensitivity above 102 td in backgr ound i l l umi nat i on
can be expl ai ned by sat ur at i on in one of t he neural
el ement s in t he vi sual pat hway l eadi ng f r om rods
t o t he cent ral ner vous syst em. Thi s phe nome non is
of t en called " r o d s a t ur a t i on" , but t hat is a
shor t hand descri pt i on. The psychophysi cal dat a do
not e s t a bl i s h t h a t t he r e s p o n s e s o f r od
phot or ecept or s t hemsel ves are sat ur at i ng duri ng
" r o d s at ur at i on" .
In humans, the rods nor mal l y yield the i ncrement
t hr eshol d t o the cones at a backgr ound ar ound
10-' t d, as shown in Fig. 8 (Wyszecki and Stiles,
1967). Her e backgr ounds are gi ven in log erg
(deg 2 s)-' , and the r od - cone br eak occurs at - 6.7
log erg (deg 2 s) -1. Thi s cor r esponds to appr oxi mat e-
ly 6.104 quant a(deg 2 s) -1 which is j ust a little great er
VISUAL ADAPTATI ON AND RETI NAL GAI N CONTROLS 279
- 5
- 4
- 5
- 6
I I I I
: 5 P a r a ' [ - o v e o
;% = 5 8 0 n m
# =500 nm
I I I I /
, ~. .
o/
I
I
I
1 I I I I
- - 8
( Z e r o ) - 9 - - 8 - - 7 - - 6 - - ~ - - 4 - - 3 - - 2
Log M,~
- I
FIG. 8. The r od - cone t r a ns i t i on i n h u ma n vi si on. Th e l og o f t he ener gy per uni t t i me per uni t ar ea o f a t est s pot is pl ot t ed
on t he or di nat e. The abs ci s s a is t he l og ener gy per uni t t i me per uni t a r e a o f a concent r i c b a c k g r o u n d di sk. Th e uni t s f or
b o t h ar e er gs (deg 2 s) -t me a s u r e d at t he c or ne a ( bef or e l osses i n t he eye a n d r et i na) . The s e can be expr es s ed equi val ent l y
as qua nt a ( 507 n m) ( deg 2 s) -I a n d t he r e f or e c o mp a r e d t o r et i nal i l l umi na t i ons i n t r ol a nds , t d (cf. Ta bl e 1). Th e r o d - c one
br e a k t a ke s pl ace at a b o u t - 6. 7 l og er gs (deg 2 s) -1 whi c h is equal t o 6. 10" quant a( 507 n m) (deg 2 s) -1, a n d a ppr oxi ma t e l y
equi val ent t o 0.1 t d. I n t hi s e xpe r i me nt t he t est s t i mul us was a 1 deg s pot pr es ent ed f or 60 ms . Th e t est wavel engt h was
580 n m. Th e ba c kgr ound wavel engt h was 500 n m, pr es ent ed cont i nuous l y. Ba c kgr ound size was not gi ven but was pr oba bl y
a b o u t 10 deg i n di a me t e r , concent r i c wi t h t he t est s pot . Te s t a n d b a c k g r o u n d s pot s were pl aced 5 deg f r o m t he f ovea. F r o m
Wys zecki a n d Stiles (1967).
compar ed t o t he vari ance whi ch is i nt ernal t o t he
r et i na caused by t he r ma l i s omer i zat i on of
phot opi gment , spont aneous openi ng and closing of
phot or ecept or membr ane channels, or spont aneous
neur ot r ansmi t t er release. These sources of noise
have been shown t o act in a way compar abl e t o
i l l umi nat i on, summi ng over distance and t i me, and
t her ef or e are concei ved of as an equi val ent " d a r k
l i ght " (Barl ow, 1957).
The val ue of " d a r k l i ght " was est i mat ed by
Barl ow (1957) as t he ret i nal i l l umi nat i on at t he
i nt ersect i on of a line dr awn t hr ough t he initial fl at
por t i on of t he i n c r e me n t - t h r e s h o l d curve wi t h a
line ext r apol at ed down f r om t he st rai ght sl opi ng
por t i on ( on l o g - l o g coor di nat es) . Let us make
explicit why this i nt ersect i on gives an est i mat e of
t he " d a r k l i ght ". The i n c r e me n t - t h r e s h o l d cur ve
may be expressed in an equat i on: MT = (ID + IB) p.
P is t he slope of t he rising por t i on of t he curve on
l o g - log coordinates, and varies f r om 1 for Weber' s
Law t o 0.5 f or t he square r oot law. The initial flat
por t i on of t he curve is where Io is much l arger
t han IB and t her ef or e in this range AI x = ( I o ) P. The
st rai ght sl opi ng por t i on is where IB is much l arger
t han Its, and t here M x = (IB) P. At t he i nt ersect i on
of t he t wo lines ( on log - log coor di nat es) , t he t wo
expressions for t he threshold illumination are equal,
and t hus at this poi nt t he backgr ound i l l umi nat i on
Ia equal s t he " d a r k l i ght " Io.
It appears t hat t he " d a r k l i ght " limits visual
sensitivity by being the domi nant t er m in t he retinal
noi se r at her t han by setting t he val ue of t he ret i nal
gain cont r ol . Barl ow (1957) surveyed t he l i t erat ure
on measur ement s of " d a r k l i ght " and f ound t hat
P R R 3 - H
280
most investigators agreed that the "dark light" was
represented by an equivalent retinal illumination of
2- 10 -3 td. This is equivalent to 1000 quanta(507 nm)
(deg 2 s)-' incident on the cornea. As a source of
noise, such a value of "dar k light" is enough to
explain the magnitude of the absolute threshold of
about one hundred quanta at the cornea (Hecht et
al . , 1942), with reasonable assumptions about
integration time, area of summation, and quantum
efficiency of the eye, as the following calculation
demonstrates (cf. Barlow, 1957). If the integration
time is about 0.1 s, and the integration area is about
1 deg 2, and the eye' s quant um efficiency is about
0.25, then one can calculate that the "dar k light"
has a mean and variance of 25 events per integration
time per integration area, and therefore a standard
deviation of 5 events per integration time per
integration area. If one assumes a threshold signal
to noise ratio of 4 (Rose, 1973), the absolute
threshold predicted from the "dar k noise" caused
by "dar k light" would be about 20 quanta
effectively absorbed by the rods, which is close to
the observed 25 (the measured 100 at the cornea
multiplied by the quantum efficiency of 0.25). Thus,
"dar k light" appears to limit absolute sensitivity
by causing "dar k noise".
>.
n
5
8 o
._J
Ascending the scale of backgrounds in Fig. 9, we
next encounter the region in which the increment
threshold increases like the square root of the
background. This is the range in which Rose (1948)
proposed that the visual threshold would be limited
by quantal fluctuations. In this range one observes
the square root law;
A~T ~--- ~Q ~B 1/2 ( 1 5 a )
S = kQ' 1 B - 1 / 2 (15b)
The square root law follows from Rose' s
explanation because the standard deviation of a
neural shot-noise (Dodge e t al . , 1968), resulting
from the temporal summation of the neural
responses to randomly arriving quanta, would grow
like the square root of the background light level.
The response to the increment on this background
would have to be picked out in the presence of the
neural shot noise induced by the background, and
the stimulus strength would have to be increased
in proportion with the standard deviation of that
noise. This argument is valid with the assumption
that the signal/noise ratio at threshold is kept
i / " FIXATION POINT
x ~ RO0 SATURATION
- i ' "
AOAPTINGBACKGROUNO / W ~ /
QUANTUM FLUCTUATIONS / /
DURATION 8 MSEC
I 1 I I 1 l I I
2 3 4 5 6 7 8 9
LOG ( QU A N T A 5 0 7 mp DEG. "= SEC " t ) BACKGROUND
FIG. 9. Sensitivity vs background: dark light, quantal fluctuations, Weber's Law, and rod saturation. The full repertoire
of psychophysical laws is illustrated in this experimental curve which is the graph of sensitivity for a blue -green test spot,
0.75 deg in diameter, 8 ms in duration, presented 10 deg from the fovea on an orange colored background which was 10 deg
in diameter. The different regimes are labeled in the figure. From Barlow(1965).
VISUAL ADAPTATI ON AND RETI NAL GAI N CONTROLS
const ant (Rose, 1948). Ther e are good reasons t o
believe in this assumpt i on, because human subjects
can keep t hei r reliability (e.g. percent age of false
positive responses) pr et t y const ant at t hr eshol d
across backgr ounds, and this is consi st ent with a
const ant si gnal / noi se r at i o across backgr ounds
(Rose, 1973). The expl anat i on of t he square r oot
law as a result of quant al fl uct uat i ons and t he
resul t i ng neur al shot noi se seems i nt ui t i vel y
implausible t o some people because we do n o t " see"
t he q u a n t a l f l u c t u a t i o n s whi ch l i mi t our
per f or mance as we can see supr at hr eshol d visual
noise, e.g. the " s n o w" on a poor television picture.
However , i f one comput es t he number of quant a
avai l abl e in cont r ast det ect i on tasks, as Rose did
ori gi nal l y, one is f or ced t o t he concl usi on t hat
quant al noise is t he limiting f act or in such
per f or mance. We will do this cal cul at i on bel ow in
t he cont ext of t he dependence of cont rast sensitivity
on mean level of i l l umi nat i on.
Not e t hat t he decrease in sensitivity caused by
quant al noi se is not st ri ct l y speaki ng l i ght
adapt at i on. Rat her , it is a loss in sensitivity caused
by t he propert i es of t he stimulus. The visual system
woul d not have t o adapt in or der t o fol l ow t he
square r oot law.
Next in Fig. 9 are t he t ransi t i on t o Weber ' s Law,
and fi nal l y r od sat ur at i on, bot h of whi ch we
consi dered when we discussed t he results of Agui l ar
and Stiles.
2. 1. 1. 3. Square root to Weber transition. The
t ransi t i on f r om t he square r oot law t o Weber ' s Law
deserves special consi der at i on. Thi s occurs at t he
backgr ound illumination at which the visual system
switches f r om being quant um-l i mi t ed t o being gain-
c o n t r o l l i mi t e d. As s uch, i t is t he f i r s t
psychophysi cal i ndi cat i on of real light adapt at i on.
Cr awf or d' s (1947) results were t he first t o i ndi cat e
t ha t t he t r a n s i t i o n o c c u r r e d at d i f f e r e n t
backgr ounds f or test t arget s of di f f er ent size.
Barl ow (1957) expl or ed t he condi t i ons whi ch
i nfl uenced t he t ransi t i on. The concl usi ons he
r eached were t hat bri ef, small test spots pr oduced
increment thresholds which rose like the square r oot
of t he backgr ound over t he ent i re scot opi c range.
The i ncr ement t hr eshol d curves f or spots of large
area, present ed f or l onger times, had slopes close
t o 1, i.e. Weber ' s Law, over t he whol e r od range
as in Agui l ar and Stiles' wor k. Fi gure 9 illustrates
281
t hat i ncrement t hr eshol d curves f or spots of
i nt er medi at e area, pr esent ed bri efl y, have a
transition f r om square r oot t o Weber laws. It would
be i nt erest i ng t o know exact l y how this t ransi t i on
depends on t he spatial and t empor al fact ors, but
Barl ow' s dat a f or t he r od system are i ncompl et e on
this poi nt .
2.1.2. CONTRAST SENSITIVITY AS A FUNCTION OF
ILLUMINATION LEVEL
Under t he condi t i ons t hat Weber ' s Law hol ds,
the threshold increment of illumination is a constant
t i mes t he backgr ound, i.e. (MT)=kw lB. Thi s
implies t hat t he t hr eshol d cont r ast and its inverse,
t he cont rast sensitivity, are const ant in t he Weber ' s
Law regi me, as can be seen in t he fol l owi ng
equat i on
Scon = 1 / ( AI T / / B )
Sco n = 1/kw = k' w. (16)
In Fig. 7 this is t he range f r om 10 -2 t o 102 t d.
Remember t hat const ant cont r ast sensitivity is t he
ideal whi ch light adapt at i on must strive f or i f it is
t o achi eve its mai n goal: percept ual i nvari ance of
refl ect i ng surfaces with changes in backgr ound.
The r e f or e , t o t he ext ent t he ps ychophys i cs
appr oaches Weber ' s Law, this maj or goal is met .
The threshold Weber contrast shows a clear break
bet ween r od and cone f unct i on as can be seen in
Fig. 10, f r om Bl ackwel l ' s (1946) dat a (see also
St ei nhardt , 1936; Crai k, 1938). The mi ni mal
(Weber) cont r ast t hr eshol d f or t he rods is about
0.08 cor r espondi ng appr oxi mat el y t o a cont r ast
sensitivity, as we have def i ned it above, of 12.
However , smal l er t arget s requi re hi gher cont rast ;
an 18' spot has as its least r od cont r ast t hreshol d
a (Weber) cont r ast of 0.67 wi t h a cor r espondi ng
(Weber) cont r ast sensitivity of onl y 1.5. Ther e is a
clear j ump in per f or mance when the cones come in,
wi t h We b e r c o n t r a s t t h r e s h o l d s decl i ni ng
asympt ot i cal l y t o 0.008 and cont r ast sensitivities
cl i mbi ng t o 125 or mor e.
At t he t ransi t i on f r om square r oot t o Weber ' s
Law, t he cont r ast t hr eshol d undergoes a t ransi t i on
f r om declining like t he inverse square r oot of
backgr ound t o becomi ng a const ant i ndependent of
backgr ound. Thi s can be seen f r om t he expressions
3
~ 5 . 6
2
-7 6 -5 q -3 2 ] 0 1 5
Log o d a p t o t i o n b r , g h t n e s s { f oo~ t o mb e r ~ s, - I f o o t L a mb e r ~ = 5 4 5 cd m )
FIG. 10. The dependence of the Weber contrast threshold on background illumination. The test targets were circular disks
on a large concentric background, viewed continuously. The test and background were neutral in color, and thresholds
were determined by the method of forced choice. The points are the average thresholds of ten subjects. Different sized
test targets generated the different curves, and the size of the target, in minutes of visual angle, is indicated for each curve.
The straight line drawn in at the lower left corner of the graph has a slope of - 1/2, which is the predicted slope of the
contrast threshold against background for the square root law. Modified from Blackwell (1946).
f or the square r oot law equat i on (15) and Weber ' s
Law equat i on (14). The cont rast threshold, MT/ I B,
becomes
Square r oot law
(MT/Ia) = kQ I n- l/2 (17a)
Weber ' s Law
(AIT/Ia) = kw. (17b)
Behavior of this sort can be seen in Blackwell' s dat a
Fig. 10. The contrast threshold falls roughl y like the
inverse square r oot over most of t he scotopic range,
t hough it is begi nni ng t o level of f t owar ds Weber ' s
Law [equat i on (17b)] f or t he largest targets. Under
t he condi t i ons of Blackwell' s experi ment s, t he r od
system does not ent er i nt o t he Weber Law regime
bef or e t he cones take over. However , the results of
Koender i nk et al. (1978) on cont r ast sensitivity as
a f unct i on of retinal eccent ri ci t y and mean level
suggest t hat , in t he far per i pher y of t he ret i na,
Weber ' s Law is achieved in the scot opi c range even
wi t hout t he t wo- col or pr ocedur e of Agui l ar and
Stiles (1954).
Mor e recent studies of t hreshol d cont r ast have
used a stimulus with a sinusoidal l umi nance profi l e
[Fig. 1 (B)]. Ther e are t hree extensive studies on t he
(Rayleigh) cont rast sensitivity of t he r od system, by
van Nes and Bouman (1967), by Dai t ch and Gr een
(1969), and by Smi t h (1973). These are consi st ent
in finding a maxi mal (Rayleigh) cont rast sensitivity
of bet ween 20 and 30 (which is equi val ent t o a
Weber cont r ast sensitivity of 1 0 - 15, in agreement
with Blackwell). Fi gure 11 is a pl ot of some of
Dai t ch and Gr een' s dat a showi ng t he dependence
of scot opi c cont r ast sensitivity on mean level.
The dependence on mean level of t he (Rayleigh)
cont r ast sensitivity f or gratings conf i r ms the
concl usi on t hat t he square r oot law r at her t han
Weber ' s Law domi nat es r od vision in humans
(Dai t ch and Green, 1969; Smi t h, 1973). The
cont r ast sensitivities f or very low spatial f r equency
gratings (less t han 0.5 c/ deg) level of f t o a Weber
Law limit, but cont r ast sensitivities f or higher
spatial frequenci es increase with t he average level
of i l l umi nat i on, fol l owi ng t he predi ct i on of t he
square r oot law, equat i on (17a). Ther ef or e, the
shape of t he " cont r as t sensitivity vs spatial
f r equency" curves f or st eady viewing change with
the average level. At low levels t hey are "l ow- pass"
funct i ons which have t hei r peak sensitivity at low
spatial f r equency. At higher levels of i l l umi nat i on,
t here is a defi ni t e peak at an i nt ermedi at e spatial
frequency, and a low spatial f r equency " c u t o f f "
(Dai t ch and Green, 1969; Smith, 1973). An
anal ogous effect is seen in phot opi c human vision
(van Nes and Bouman, 1967).
I f one calculates how many quant a are available
t o detect t hreshol d cont rast , one is forced t o admi t
t hat quant al fl uct uat i ons must pl ay a significant
> . .
t - , -
1 / 1
z ~
t . )
10.0
8.0
6,0
4.0
2 . 0
0 . 0
I
2 C/DEG
o
o
o o
0.5 ClDEG
1 L I l I I I
-2.50 -2.00 -I.50 -I.00 -0.50 0.00 0.50
MEAN I LLUMI NATI ON (LOG TROLANDS)
FIG. 11. The dependence of the Rayleigh contrast sensitivity
on mean level. Results for two spatial frequencies of test
target are shown: 0.5 c deg-' as empty circles, and 2 c deg -1
as filled circles. An artificial pupil of 1 mm di ameter was
used. The test targets were sinusoidal grating patterns
generated on the face of a c at hode ray t ube ( CRT) di s pl ay
which subtended 8 deg by 3 deg, centered 12 deg from the
fovea. The phosphor of the CRT was P31(yellow-green)
but a Wratten 65 filter was interposed between subject and
screen to shift the dominant wavelength of the phos phor
t owards the peak of the rod spectral sensitivity function. The
target was presented for 200 ms every second. Control
experiments established that the rods were the photoreceptors
which determined threshold up to 0 log t d. Pl ot t e d from
Daitch and Green (1969).
par t in limiting cont r ast sensitivity in t he scot opi c
r ange. Suppos e we ma ke t he c ons e r va t i ve
assumpt i on t hat no less t han one quar t er of t he
quant a i nci dent on t he cor nea may be used f or
cont r ast det ect i on. Fur t her we assume t hat t he
i nt egrat i on t i me over which quant a may be count ed
is about 0.1 s. Fi nal l y, and most crucially, we
assume t hat t he i nt egr at i on area f or t he neur ons
which are i nvol ved in t he det ect i on task is at most
1 deg 2. Thi s last assumpt i on is based on t he
measur ement s of recept i ve field cent er sizes of
ret i nal gangl i on cells in cats and monkeys at
compar abl e ret i nal loci t o t he ones used in t he
human psychophysi cal experi ment s ( Hubel and
Wiesel, 1960; de Monast er i o, 1978; Cl el and et al.,
1979), and on t he not i ons of t he Channel
Hypot hesi s expanded in Sect i on 2. 1. 3. Gi ven these
assumpt i ons, one may cal cul at e what t he highest
cont r ast sensitivity mi ght be in t he scot opi c range,
at t he highest backgr ound in this range whi ch is
about 10-' td. This backgr ound retinal illumination
cor r esponds t o 5" 104 quant a( deg ~ s) -' i nci dent on
t he cor nea. I f one quar t er of t hese quant a may be
used by t he ret i na, in an area of 1 deg 2, over a t i me
of 0.1 s, t hen t he t ot al avai l abl e quant a f r om such
a backgr ound are 1250. I f quant al fl uct uat i ons are
t he limiting f act or , t hen t he st andar d devi at i on of
t he quant al count with this mean number of 1250
must be t he limiting source of noise. The st andar d
devi at i on of t he quant al noise must be t he square
r oot of 1250, whi ch is about 35. In most det ect i on
experi ment s t he s i gna l - noise rat i o is t aken t o be
about 4, so t hat t he t hr eshol d amount of quant a
woul d have t o be about 4-35 = 140. This is 140
neural l y triggered quant al events; we must mul t i pl y
by 40 (the reci procal of 1/ 40 whi ch is t he pr oduct
of the quant al efficiency of 1/ 4 times the integration
t i me of 0.1 s) t o obt ai n t he stimulus i l l umi nat i on,
measur ed at t he cor nea, t o pr oduce this many
neural events. Thus we get t hat t he stimulus
i l l umi nat i on must be equi val ent t o 5. 6. 103
quant a(deg 2 s)-' . The best quant um-l i mi t ed (Weber)
cont r ast sensi t i vi t y one coul d expect woul d
t her ef or e be (Ia/MT) = (5" 104)/(5.6 103) or about
9, whi ch is about as high as t he human (Weber)
cont r ast sensitivity reaches in t he scot opi c range.
It is i nt erest i ng t hat Agui l ar and Stiles (1954) went
t hr ough an anal ogous cal cul at i on in t he Discussion
of t hei r famous paper, and concl uded t hat t hey had
discredited the idea t hat quant al fluctuations limited
det ect i on of cont rast . However , in t hei r cal cul at i on
t hey made t he assumpt i on t hat , because t hey used
a disk 9 deg in diameter as a stimulus, all the quant a
in t he 64 deg 2 ar ea of t he disk were available f or
t he det ect i on t ask. We now know this assumpt i on
is unr easonabl e. Pr esent l y avai l abl e knowl edge
about t he di st ri but i on of recept i ve field sizes
suppor t s Rose' s (1948) hypot hesi s about t he
i mpor t ance of quant um fl uct uat i ons in scot opi c
vision.
The great i mpr ovement in cont r ast sensitivity
associated with the shift f r om r od t o cone pat hways
is compl i cat ed by t he effect s of ret i nal i nhomo-
genei t y studied by Koender i nk et al. (1978). They
measur ed cont r ast sensitivity funct i ons with sine
gratings which subt ended a fixed area of 4 deg by
4 deg, at several l ocat i ons in t he visual field.
Fi gure 12 shows t hei r fi ndi ng t hat in t he far
per i pher y t here is no increase of cont r ast sensitivity
bet ween scot opi c and phot opi c backgr ound levels,
and in t he near per i pher y t here is onl y an increase
of about a f act or of t wo in t he phot opi c cont r ast
284
R. M. SHAPLEY AND C. ENROTH- CUGELL
10
I I I 1 I I
- / ecc
l I I I L I
0 o 10 5 0
FIG. 12. Lowes t t hr e s hol d mo d u l a t i o n dept h as a f unc t i on
of r et i nal eccent ri ci t y a n d me a n level o f i l l umi nat i on. Thes e
da t a ar e all f r o m c ont r a s t t hr e s hol d me a s u r e me n t s f or si ne
gr at i ng pat t er ns whi ch s ubt e nde d 4 deg by 4 deg a nd were
dr i f t i ng at a t e mpor a l f r equency of 4 Hz. The st i mul i were
pr es ent ed on a Hewl et t - Pa c ka r d 1310A di s pl ay wi t h a P 15
phos phor ( domi nant wavel engt h at 510 nm) , and were viewed
by t he s ubj ect t h r o u g h a 2 mm di amet er art i fi ci al pupi l .
Cont r as t sensi t i vi t y cur ves were me a s ur e d at each eccentricity
a nd i l l umi nat i on, a n d t he mi n i mu m t hr e s hol d mo d u l a t i o n
dept h (t he r eci pr ocal o f t he peak c ont r a s t sensi t i vi t y acr os s
spat i al f r equency) for each condi t i on was denot ed m*, whi ch
is t he qua nt i t y pl ot t ed i n t he f i gur e. The di f f er ent s ymbol s
ar e f or di f f er ent me a n i l l umi nat i ons . Emp t y circles are for
10 t d; filled circles ar e f or 1 t d; circles wi t h dot s in t he cent er
ar e f or 0.1 t d. Fr o m Koender i nk et al . (1978).
sensitivity over the scot opi c. It seems t hat t he foveal
phot opi c cont rast sensitivity is especially high when
compar ed with t he phot opi c (and scotopic) cont rast
sensitivity of t he peri pheral retina. They also f ound
t hat , f or a st i mul us of a gi ven size and spat i al
frequency, t he t r ansi t i on f r om squar e r oot law to
Weber ' s law depended on the ret i nal eccentricity;
t he t r ansi t i on occur r ed at l ower l umi nances t he
mor e per i pher al was t he st i mul us.
2.1.3. THE CHANNEL HYPOTHESIS
Ther e exists a wor ki ng hypot hesi s one can use t o
i nt er pr et Ba r l ow' s , Bl ackwel l ' s , Dai t ch and
Gr een' s, and Koenderi nk e t a l . ' s , findings about the
i nfl uence of size or spat i al f r equency or retinal
eccent ri ci t y on t he t r ansi t i on f r om squar e r oot law
t o Weber ' s Law. Thi s hypot hesi s is t hat t he vi sual
syst em is compos ed of a set of size or spat i al
f r equency channel s ( Campbel l and Robs on, 1968;
Enr ot h- Cugel l and Robson, 1966; Robs on, 1975;
Gr a ha m, 1980). It is supposed t hat a t est st i mul us
sifts t hr ough t he channel s and excites onl y t hose
channel s which are " t u n e d " t o t he st i mul us. Such
an hypot hesi s can be used in conj unct i on wi t h
research fi ndi ngs on t he adapt at i on pr oper t i es of
ret i nal gangl i on cells wi t h di fferent -si zed recept i ve
fields to make sense out of t he t r ansi t i on f r om
square r oot law t o Weber ' s law (Enrot h-Cugel l and
Shapl ey, 1973b). In essence, t he expl anat i on is t hat
t he channel s whi ch r es pond t o l ow spat i al
frequenci es suf f er mor e loss of sensitivity wi t h
increase in backgr ound t han do the channel s which
r espond t o high spat i al frequenci es because ret i nal
gai n cont rol s depend on areal s ummat i on of
backgr ound i l l umi nat i on. The channel s which are
most sensitive t o low spat i al frequenci es, accor di ng
to this view, sum adapt i ve signals over a l arger area
t han do t he channel s mos t sensitive t o high spat i al
frequenci es. A mor e det ai l ed expl anat i on of this
poi nt is of f er ed in t he Theor y section.
2 . 1 . 4 . HUMAN AND FELINE CONTRAST SENSITIVITIES
COMPARED
Since mos t of t he el ect rophysi ol ogi cal results on
retinal adapt at i on and gai n cont r ol come f r om
exper i ment s on ani mal s, it is rel evant t o compar e
h u ma n p s y c h o p h y s i c a l and cat b e h a v i o r a l
meas ur ement s of cont r ast sensitivity at di f f er ent
mean levels of i l l umi nat i on. Recent l y, this has
become possible because of the results of Past er nak
and Mer i gan (1981). Thei r results show t hat t here
are not i ceabl e di fferences bet ween t he cont r ast
sensitivities of cat and man. As can be seen in
Fig. 13, the cat ' s cont r ast sensitivity i mpr oves with
mean level in a way anal ogous t o man, but at all
mean levels t he cat ' s peak cont r ast sensitivity is
l ower. Thi s may be because t he hi gh mean
l umi nances were phot opi c f or t he human, but all
mean l umi nances were pr obabl y scot opi c f or t he
cat. The r o d - c o n e t r ansi t i on in cat s is at a much
hi gher mean l umi nance t han in man, pr es umabl y
because of t he much hi gher r od - cone rat i o in t he
cat (Lennie e t a l . , 1976). Cont r ast sensitivity grows
much mor e steeply for high spatial frequencies t han
f or low, in cat as in man. However , t he acui t y of
t he cat is much worse t han t hat of man, as can be
seen in Fig. 13 by the separ at i on bet ween t he high
spat i al f r equency cut of f s of t he cont r ast sensitivity
curves at all mean levels except t he lowest.
However , t he basi c si mi l ari t i es bet ween t he
dependences of fel i ne and h u ma n c ont r a s t
sensitivities on mean level of illumination encourage
us t o at t empt a synt hesi s of huma n psychophysi cal
studies of light adapt at i on wi t h t he body of
ioo
io
LU
t.~ ~0
0 2
io
VI S UAL ADAP T AT I ON AND RE T I NAL GAI N CONT ROL S
~
0 0 CO/m2
1 0 - 2 cclln~-
~
16 10 acdlm2
16 x 1 0 _ 6 c d / r n 2
S P A T I A L F R E Q U E N C Y ( c / d e g )
FIG. 13. The de pe nde nc e o f c ont r a s t sensi t i vi t y on me a n
l umi na nc e in ma n a nd cat . The cat r esul t s were obt ai ned wi t h
a t wo- al t er nat i ve f or ced choi ce p a r a d i g m a n d t hr e s hol d was
t a ke n as 75% cor r ect . The h u ma n r esul t s were obt a i ne d in
a si mi l ar ma n n e r . For bot h h u ma n a n d cat , t he nat ur al pupi l
openi ng det er mi ned ret i nal i l l umi nat i on. The gr at i ng pat t er ns
were di s pl ayed on t wo CRTs wi t h P3 1 ( y e l l o w- g r e e n )
phos phor s . The me a n l umi na nc e was cont r ol l ed wi t h neut r al
dens i t y fi l t ers pl aced i n f r ont o f t he CRT scr een. Fr o m
Pa s t e r n a k a n d Me r i ga n (1981).
knowl edge a bout ret i nal adapt at i on in t he cat .
2.1.5. THE TIME COURSE OF ADAPTATION
The change in sensi t i vi t y af t er a ba c kgr ound has
been t ur ned on is not i mmedi at e. The t i me cour se
of this change has been st udi ed using t he t echni que
of " Cr a wf o r d ma s k i n g " , in whi ch a backgr ound
is fl ashed on f or a fi ni t e t i me, and a br i ef t est fl ash
is super i mposed on t he backgr ound at vari ous times
af t er t he onset of t he backgr ound. The mos t useful
285
resul t s obt ai ned wi t h this met hod on t he r od vi sual
pat hways are t hose of Adel son (1982). Fi gure 14
summar i zes his mai n fi ndi ngs. I t can be seen t hat
when t he t est fl ash is super i mposed on a st eady
backgr ound, t he t hr eshol d f or t he t est fol l ows a
curve like t hat obt ai ned by Agui l ar and Stiles (1954;
Fi g. 7A). However , when t he t est is appl i ed j ust at
t he onset of t he backgr ound, t he dat a show evidence
f or sat ur at i on, a st eep upt ur n in t he t hr eshol d vs
backgr ound curve, at a backgr ound i l l umi nat i on
mor e t han t wo log units l ower t han t he st eady-st at e
curve. One can t her ef or e i nfer t hat t he process of
adapt at i on t akes t i me t o rescue t he r esponse f r om
t hi s sat ur at i on. Ho w much t i me can be i nf er r ed
f r o m t he ot her curves in Fi g. 14. At t est -
backgr ound offset s of 2 0 0 - 1000 ms the sat ur at i on
occurs at about one log uni t hi gher t han at zero
of f set . Thi s means t hat a first st age of adapt at i on
is basi cal l y compl et e wi t hi n 200 ms. Then bet ween
1 s and st eady st at e a second sl ower process moves
t he sat ur at i on out anot her log uni t .
Adel son (1982) i nt er pr et s these results in t er ms
of a cascade of processi ng, in which an initial linear
st age is f ol l owed by a sat ur at i ng t r ansducer . I f
adapt at i on act s at or bef or e t he sat ur at i on,
sat ur at i on of t he r esponse of t he cascade can be
avoi ded. Thi s is a si mi l ar scheme t o t he one we
out l i ned in Sect i on 1.2.2. However , Adel son (1982)
consi ders t wo di f f er ent t ypes of adapt at i on whi ch
he calls " s ubt r a c t i ve " and " mul t i pl i c a t i ve " . I n
experi ment s in which he used pr e- adapt at i on bef or e
t he " Cr a wf o r d ma s ki ng" , he was abl e t o show t hat
t he r api d adapt at i on, whi ch has a t i me const ant of
about 100 ms, is multiplicative, i.e. it acts like a gai n
cont r ol . However , t he sl ow adapt at i on, whi ch has
a t i me const ant of a bout 30 s under t he condi t i ons
of Ad e l s o n ' s e xpe r i me nt s , a p p e a r e d t o be
subt r act i ve. The nat ur e of t he slow subt r act i ve
adapt at i on di scovered in these experi ment s remai ns
t o be det er mi ned. The r api d gai n cont r ol has been
obs er ved in physi ol ogi cal exper i ment s t o be
described bel ow. It is of t heoret i cal i mpor t ance t hat
t he gai n cont r ol mechani s m, while fast , is not
t ur ned on i nst ant aneousl y when t he backgr ound
goes on.
2.1.6. WHAT PSYCHOPHYSI CS I MPLI ES ABOUT RETI NAL
MECHANI SMS
2.1.6.1. Psychophysical sensitivity loss: gain
3
2
S
o
o
a~ - - I
k -
2
--5
( a)
Del / / / ! ~ 1
200 9J I L
5 o o . , | L
,ooo d / / "
cgr--~: g ~; o 0 5 i 5 2
2 ~ t DeLay sec
,
g,
" 1 , " , - : i - : ,
0 20 40 60 80 ] O0
-3 -2 - I 0 l 2 3
DeLay sec
Background, Log scot t d
FIG. 14. Transient saturation and adaptation in the human rod system. A square test spot, 4.5 deg on a side and of 480 nm
wavelength, was superimposed on an 11 deg red background centered 12 deg from the fovea in the nasal direction of the
visual field (temporal retina).
In panel (a) are shown increment threshold curves taken at different times after the onset of the background flash. The
test was 30 ms in duration, and the background was either continuous (empty squares) or was flashed on at various times
before the test and was left on for 400 ms after the test. The delay between background onset and test onset is shown in
(a) as an inset. Also graphed there (lower right) are the Weber contrasts at threshold for the different conditions, though
they are labeled Weber fractions here. In panels (b) and (c) the time course of adaptation is shown by plotting the value
of the threshold for the test spot presented with different delays after the onset of the background (3 scotopic td) which
remains on. Panels (b) and (c) are the same data plotted on two different time scales, to illustrate the rapid and slow phases
of adaptation. From Adelson (1982).
reduction or noise increase? Wh a t d o t he
p s y c h o p h y s i c a l r es ul t s t el l us a b o u t t he u n d e r l y i n g
me c h a n i s ms o f t he c o n t r o l o f s e ns i t i vi t y i n h u ma n
r o d vi s i on? I n e x p e r i me n t s whi c h s i mu l a t e d o u r
e v e r y d a y vi s ual p e r c e p t i o n o f o b j e c t s ( Bl ackwel l ,
1946), t he r o d - d r i v e n h u ma n vi s ual s ys t e m d i d not
qui t e r e a c h t he goa l o f We b e r ' s La w. Up t o t he
t r a ns i t i on f r o m t he s quar e r o o t l aw t o We b e r ' s Law,
t he t he or e t i c a l e x p l a n a t i o n r e qui r e d is onl y i n t e r ms
o f c ha nge s i n t he n e u r a l noi s e l evel c a us e d b y
q u a n t u m f l u c t u a t i o n s i n t he b a c k g r o u n d l i ght . At
hi gher b a c k g r o u n d s t h a n t he l evel s r e qui r e d f or t he
r od - cone t r a ns i t i on i n t he whi t e - on- whi t e s t i mul us
s i t u a t i o n , t he r o d s ys t e m mu s t a d a p t , f or i t s
s e ns i t i vi t y d r o p s mo r e t h a n c a n be a c c o u n t e d f or
s i mp l y i n t e r ms o f a n i nc r e a s e o f noi s e due t o
q u a n t u m f l uc t ua t i ons . Al s o , t he n e u r o n s whi c h a r e
t he me d i u m f or pe r c e i vi ng gr a t i ngs o f ve r y l ow
s pa t i a l f r e q u e n c y mu s t ha ve t he i r s ens i t i vi t i es
c o n t r o l l e d b y mo r e t h a n q u a n t a l noi s e, be c a us e t he
s e ns i t i vi t y d r o p s mo r e s t e e pl y t h a n t he s q u a r e r o o t
l aw. Thus noi s e a n d ga i n c o n t r o l mu s t be i nvol ve d
i n t he v a r i a t i o n o f vi s ual s e ns i t i vi t y wi t h c ha nge s
i n b a c k g r o u n d o r a ve r a ge l evel o f i l l u mi n a t i o n .
2. 1. 6. 2. The site of adaptation: the retina. On e
q u e s t i o n we ha ve not a s k e d or a n s we r e d i s, wh a t
d o t he p s y c h o p h y s i c a l r es ul t s i mp l y a b o u t t he si t e
o f a d a p t a t i o n ? I t c o u l d be i n t he r e t i n a or i n t he
b r a i n o r b o t h . Se ve r a l p s y c h o p h y s i c a l e x p e r i me n t s
i mp l y t ha t i t is r e t i na l . F o r e x a mp l e , Ba t t e r s b y a n d
Wa g ma n (1962) d e mo n s t r a t e d t h a t t he r e is l i t t l e
i n t e r o c u l a r t r a n s f e r o f s t e a d y l i ght a d a p t a t i o n . I f
t he r e wer e a l ar ge c e nt r a l c o mp o n e n t o f l i ght
a d a p t a t i o n , one mi ght e xpe c t a l a r ge a mo u n t o f
i n t e r o c u l a r t r a n s f e r . Ot h e r s i mi l a r e x p e r i me n t s a r e
t hos e o f He i n e ma n n (1955) a n d Wh i t t l e a n d
Cha l l a nds (1969) b o t h o f whi ch i nvol ved i nt e r oc ul a r
br i ght ne s s ma t c h i n g . I n b o t h set s o f e x p e r i me n t s ,
a di m ma t c h i n g l i ght on an even d a r k e r b a c k g r o u n d
was ma t c h e d t o mu c h b r i g h t e r l i ght s on b r i g h t
b a c k g r o u n d s . Th e t wo l i ght s wer e pr e s e nt e d t o
d i f f e r e n t eyes a n d t he r e was e v i d e n t l y l i t t l e or no
i n t e r o c u l a r t r a n s f e r o f t he a d a p t i n g ef f ect o f t he
b r i g h t b a c k g r o u n d .
Th e ga i n o f t he h u ma n e l e c t r o r e t i n o g r a m ( ERG)
i n r e s p o n s e t o a l a r ge t est t a r g e t c ha nge s wi t h
b a c k g r o u n d i l l u mi n a t i o n i n a wa y ve r y s i mi l a r t o
t he ps yc hophys i c a l sensi t i vi t y f or t ar get s o f t he s a me
size (Biersdorf et al., 1965). This experiment
indicates that the gain of the retina is affected at
the same light levels as the visual threshold for large
targets. A further question one might raise is, where
in the retina is the site of this gain change? Much
of the physiological work we present below was
motivated by this question. Prior to the
physiological investigation, this question of the site
in the retina of gain control was investigated
psychophysically and this work led to the two
concepts of gain control by pigment depletion,
which has been shown to be only a minor factor
in the control of retinal gain, and the adaptation
pool, which still motivates research.
2.1.6.3. Pi gment depletion. Vertebrate visual
pigments are bleached by light into non-receptive
intermediates which must be regenerated to a
receptive state enzymatically. It was thought for
some time that visual pigment depletion, resulting
from bleaching by the background light, was the
main cause of light adaptation (Hecht, 1924). This
would put the site of adaptation right at the initial
transduction stage in vision. However, it is now
known that the pigment regenerates so quickly that
there is a rather small amount of pigment bleached
1.0
0.8
r,
o
"~ 0.6
o
L-
~ 0.4
0.2
287
for either rods or cones over much of the visual
range of backgrounds (Rushton, 1962). This can be
seen in Figs. 15 and 16. Figure 15 is from Alpern
and Pugh (1974) and shows the fraction of human
rhodopsin, the rod pigment, bleached as a function
of a steady background. Even up to rod saturation
(5" 108 quanta(507 nm) (deg 2 s) -~) the rod pigment
has been bleached away less than 270, but the visual
threshold would have risen by a factor of more than
107, a discrepancy in prediction. Figure 16 shows
a similar result for human cones, from Alpern et
ai. (1971). The cone pigment has been only bleached
by half at about 104s trolands which is near the top
of the photopic range. So we can rule out pigment
depletion as playing a major role in human light
adaptation, though it has some effect on photopic
(cone-driven) sensitivity (Boynton and Whitten,
1970; Valeton and van Norren, 1983). It is
interesting that photopigment depletion began to be
doubted as an explanation of light adaptation quite
a long time ago, from experiments on increment
threshold and photopigment concentration in the
frog retina conducted by Granit et al. (1939). In
those experiments ERG thresholds were increased
by log units by backgrounds which had no
. - . \ .
: , \ !
\ . ' \ ;
5 7 5 n m
" ! \ .
5 0 0 n m
. ~ .
0 , I I I I I I
1 2 1 3 1 4
L o g q u a n t a s e c - I c m - ~ o f r e t i n a a t t h e c o r n e a
~
1 0 s e c W h i t e
I
1 5
FIG. 15. Pigment depletion in rods caused by steady illumination. The amount of the rhodopsin in a 5 deg field located
18 deg peripheral to the fovea in the temporal retina was measured with a retinal densitometer (described in Alpern et a l . ,
1971 and in Alpern and Pugh, 1974) Plotted vertically i s t h e fractional amount of rhodopsin left in the steady state at
the background illumination plotted on the horizontal scale. The three curves are for steady lights of 500 nm, 575 nm,
and white light The 500 and 575 nm lights were obtained with the white source and interference filters The results to
concentrate on are the 500 nm results, since 500 nm is near the peak wavelength of absorption of rhodopsin and so will
give the greatest pigment depletion at the lowest retinal illumination. The half bleaching point for the 500 nm curve is at
about 13.2 log quanta(cm 2 s)-' which is equivalent to about 10.2 log quanta(deg 2 s) -1, the more familiar unit of retinal
illumination [also equivalent to about 4.3 log (scotopic) td]. These values of quanta are referred to the cornea and do not
take into account losses in the eye. From Alpern and Pugh 0974).
PRR3-H*
I I ~ " ( i _ p ) 0 0 ) 4 . . ~ = p I 2
06- -
0"4 i ' ~ ~
0"2
O'O
I 1 l 1
4 45 50 5~
log I 2 photopic trofands
FIG. 16. Pigment depletion in cones caused by steady illumination. Plotted in the graph are retinal densitometry
measurements of the human fovea at different levels of steady illumination of a yellow - green bleaching light. P is the
fraction of cone pigment remaining in the steady state. The half-bleaching illumination is about 4.5 log photopic td, which
is equivalent to approximately 10.6 log quanta(deg ~ s)-' of quanta at 560 nm, the peak wavelength for the long-wavelength
cones. Note that the half-bleaching point for the cones is within half a log unit of the half bleaching point for rods, when
expressed in units of quanta of the optimal wavelength for the pigment. From Alpern et al. (1971).
measurable effect on the extractable rhodopsin
concentration. Furthermore, Rose (1948, 1973) has
presented an elegant argument which disposed of
pigment depletion as the sole explanation of light
adaptation. If pigment depletion were significant
in the scotopic range, the quantal-noise limited
contrast sensitivity would be held down to a very
low level. This would be the consequence of
depleted pigment; light would be absorbed less
efficiently. Since the contrast sensitivity does rise
in the quantal-noise limited range, and it rises to
a degree consistent with a relatively constant
quantum-efficiency, there cannot be a significant
amount of pigment depletion in the scotopic range
of vision. Figure 15 proves the correctness of this
argument.
2.1.6.4. Adapt at i on pools. Since one of the
critical issues in this field is the actual site in the
retina of the process of light adaptation, a natural
question to ask is, how far does adaptation spread
in space? We have already argued in the
Introduction that light adaptation has to be
localized to some extent, for functional reasons. But
how localized? Perhaps the photoreceptor is the site
of adaptation, or perhaps the retinal ganglion cell,
or perhaps one of the retinal interneurons.
William Rushton, in his well known Ferrier lecture,
summarized his years of work on this problem
(Rushton, 1965). He concluded that there must be
adaptation pools more proximal in the retina than
the photoreceptors, and that within these pools light
evoked signals were added up to set the gain of the
retina by negative feedback. Rushton used two
pieces of psychophysical evidence to support his
contention that there were adaptation pools. His
arguments from these two bits of evidence are
vulnerable to criticism, and yet the idea of
adaptation pools has been extremely fruitful and
provocative.
Rushton' s first bit of evidence for the concept of
adaptation pools was the extremely low level of light
required to raise the psychophysical threshold by
0.5 log units above the absolute threshold.
According to Rushton, the number of light quanta
which adapted the retina was only one tenth of the
number of rods upon which the background fell,
i.e. about 5-10' quanta s -1 over a circular back-
ground 10 deg in diameter. Thus, he concluded rod
VISUAL ADAPTATION AND
signals were reduced in magnitude, even those from
rods which had never seen the adapting light. How-
ever, as we have stated repeatedly, a decline in
psychophysical sensitivity does not necessarily mean
a decline in retinal gain but may simply be a rise
in the noise level against which the signal must be
discriminated. There would be no change in retinal
gain in this latter case, even though the psycho-
physical sensitivity had declined. When we repeated
this experiment of Rushton' s on retinal ganglion
cells, and found a significant effect on retinal gain
at such low backgrounds that only a fraction of the
rods received a photon each second, Rushton' s
argument was made much tighter (Enroth-Cugell
and Shapley, 1973a).
Rushton' s second argument was based on an
experiment with gratings. The idea was to present
a background grating and then a test grating in
phase, and another test grating 180 deg out of
phase, with the background grating. All gratings
were square waves of 2 c deg -1 spatial frequency.
Rushton reported no difference in threshold for the
in-phase and out-of-phase condition, and then
argued this meant that the background signals were
pooled in an adaptation pool which he supposed
was larger in diameter than the period of the
background grating, 0.5 deg. There is something
wrong with the reasoning behind this experiment,
and with the actual result, which was not replicated
by Barlow and Andrews (1967). The weakness of
the argument is interesting because it relates to the
degree of localization of adaptive effects, to the
concept of spatial channels, and to results on
adaptation pools in retinal neurons.
Adaptation pools ought to be roughly the same
size as the receptive fields of the retinal neurons they
adapt. This is consistent with our argument in the
Introduction (Section 1) about the function of
adaptation in providing brightness constancy when
there are gradients of illumination, as was observed
by Davidson and Freeman (1965) and Land and
McCann (1971). Electrophysiology indicates that
the size of an adaptation pool is equal to (Cleland
and Enroth-Cugell, 1968; Enroth-Cugell and
Shapley, 1973b) or less than (Green e t al . , 1977;
Harding, 1977) the size of the receptive field of a
retinal ganglion cell it regulates. Therefore,
functional reasoning and electrophysiological
evidence support the inference that if a retinal cell
RETINAL GAIN CONTROLS 289
can resolve a grating pattern, the adaptation pool
which controls that cell's adaptation state should
also be able to resolve the grating. Now the channel
hypothesis implies that the 2 c deg -1 grating that
Rushton (1965) used stimulated just those cells
whose receptive fields could resolve 2 c deg -1.
Daitch and Green' s (1969) data indicate that these
cells are towards the high end of the spatial
frequency range for rod-driven visual cells in the
peripheral retina. We must conclude that if these
cells resolved the 2 c deg -1 test pattern their
adaptation pools must also have been able to resolve
the pattern. Therefore, one ought to have observed
that the threshold for a superimposed test pattern
should have depended on its position relative to the
adapting grating. In-phase with the adapting grating
should have been the position of highest threshold.
This is just what Barlow and Andrews (1967) found,
and the failure of Rushton (1965) to obtain this
result probably was a consequence of image blur
or light scatter. Barlow and Andrews concluded that
their results cast doubt on the existence of
adaptation pools. However, by the argument above,
their result does not disprove the existence of
adaptation pools at all. It just confirms what is now
known from other experiments, that the adaptation
pools "see", i.e. resolve patterns, as well as the
receptive fields they serve.
A different kind of experiment on adaptive
summation was performed by Westheimer (1965).
The test spot was small (0.1 deg) and the adapting
field was a circular disk concentric with the
stimulus. The adapting disk was constant in
luminance but varied in diameter. Under these
conditions, threshold increased as a function of
adapting disk diameter up to a diameter of about
0.75 deg. In this range, threshold was approxi-
mately proportional to the area of the adapting
disk. Surprisingly, for disk diameters larger than
0.75 deg the threshold dropped, suggesting that light
falling beyond 0.375 deg from the test spot acted
to "sensitize" the response to the test.
At first the "sensitization" discovered by
Westheimer was thought to be due to adaptation
produced by a neural element which had a
spatially- opponent cent er - surround receptive
field. Such a neuron might have a steady state
response to the large adapting disk which was much
smaller than its steady response to the small disk.
290
I f the gain of the cell were related to this steady state
response, t he gai n r educt i on woul d be less f or t he
large disk. However , physi ol ogi cal results on
s c o t o p i c a d a p t a t i o n do not s u p p o r t t hi s
i nt erpret at i on of the psychophysi cal result (Enrot h-
Cugell e t al . , 1975; Barl ow and Levi ck, 1976). That
is, the gai n of the receptive field center in cat retinal
gangl i on cells in t he scot opi c r ange decreases and
t hen levels of f as backgr ound di amet er is increased,
and is not a decreasing and t hen increasing funct i on
as woul d be supposed f r om t he convent i onal
i nt er pr et at i on of sensi t i zat i on. Fur t he r mor e ,
psychophysi cal sensi t i zat i on in t he scot opi c r ange
has not been convi nci ngl y demons t r at ed under
stabilized i mage condi t i ons ( MacLeod, 1978). Thi s
suggests t hat ret i nal or cent ral st i mul at i on by t he
movi ng bor der of t he backgr ound disk may be
needed f or sensi t i zat i on t o be obser ved ( MacLeod,
1978). Mor eover , t he rel at i on of sensi t i zat i on t o
retinal adapt at i on has been quest i oned by Lenni e
and MacLeod (1973) who showed t hat the key to
sensitization was the u n i f o r mi t y in l umi nance of the
0.75 deg di amet er desensitizing disk and t he out er
annul us. I f t he out er annul us were ei t her l ower o r
h i g h e r in l umi nance t han t he cent ral disk it woul d
reduce sensi t i zat i on.
2.2. The Cone System
2.2.1. SENSITIVITY AS A FUNCTION OF BACKGROUND
The cone syst em ( Phot opi c syst em) is like t he r od
syst em in yielding We be r ' s Law under some
circumstances and t he square r oot law under others.
As is evi dent f r om Fig. 8 f r om Wyszecki and Stiles
(1967), in huma n vi si on t he cones t ake over at
t hr eshol d f r om t he r ods above 0.1 t o 1 td in
backgr ound ret i nal i l l umi nat i on. The i ncr ement
t hr eshol d curves in t he l i t erat ure t end t o all show
a cone pl at eau (cone " d a r k l i ght "; Barl ow, 1958)
f r om 0.1 up t o about 10 t d. The phot opi c Weber ' s
Law f or a moder at e- si zed t est spot ( di amet er > 0.5
deg) t akes over f r om t he cone " d a r k l i ght " l i mi t ed
behavi or at 10 td very rel i abl y.
Al t hough t he phot opi c t hr eshol ds f or spot s
fol l ow We be r ' s Law up t o t he poi nt where t he
pi gment is bl eached away, it has recent l y been
shown t hat sat ur at i on can be demons t r at ed in t he
cone syst em wi t h adapt i ng backgr ounds which are
t hemsel ves small in ar ea (Buss e t al . , 1982). Thi s
sat ur at i on can begi n at as low a backgr ound as
10 t d, in the low phot opi c range. On a small
di amet er (0.25 deg) backgr ound t he t hr eshol d of a
smal l spot cl i mbs much mor e st eepl y t han Weber ' s
Law ( obt ai ned wi t h a large backgr ound) woul d
predi ct . Thi s effect may be obser ved under
stabilized i mage condi t i ons ( Tul unay- Keesey and
Vassilev, 1974). The phot opi c sat ur at i on is t hought
to be due t o sat ur at i on of a cone-dri ven i nt erneuron
in the ret i na, one which has a cent er - sur r ound
i nt er act i on so t hat a backgr ound of large ar ea will
release t he put at i ve i nt er neur on f r om sat ur at i on.
Electrophysiological evidence on sensitization in the
phot opi c range is present l y scant and equivocal, but
t here are some i ndi cat i ons it may exist (see Section
3.7.).
2. 2. 2. CONTRAST SENSITIVITY AND MEAN LEVEL
For most t arget s, and in par t i cul ar moder at e-
sized spots with a sharp edge on a large backgr ound,
We be r ' s Law hol ds f r om 10 td to l 0 s td, i.e.
t hr oughout the phot opi c r ange of backgr ounds.
This is shown very clearly in the dat a of Whittle and
Chal l ands (1969), Fig. 17. The l ower curve for each
subj ect is t he i ncr ement t hr eshol d curve; above it
are curves of const ant bri ght ness as mat ched t o a
test fl ash in t he cont r al at er al eye. It is i nt erest i ng
t ha t t he c o n s t a n t b r i g h t n e s s c ur ve s ar e
appr oxi mat el y paral l el t o the i ncr ement t hr eshol d
curve. Thi s means t hat t he appar ent bri ght ness of
t wo di f f er ent i ncr ement s was pr opor t i onal t o t hei r
(Weber) cont r ast s. Thus, Whi t t l e and Chal l ands'
results i mpl y t hat (Weber) cont r ast r at her t han
l umi nance det er mi ned the appar ent bri ght ness.
They also poi nt out t hat ot her, cent ral , fact ors may
cont r i but e t o appar ent bri ght ness. Under t he
condi t i ons of t hei r experi ment s, t he mechani sms
which det ermi ned brightness were purel y monocul ar
and t her ef or e pr oba bl y retinal - - as evi denced by
t he fact t hat st i mul us cont r ast agai nst a fai rl y hi gh
backgr ound in one eye was needed t o mat ch a much
weaker flash l umi nance agai nst zero backgr ound in
t he ot her eye. These dat a of Whi t t l e and Chal l ands
suppor t t he mai n hypot heses we st art ed out wi t h
about t he f unct i onal si gni fi cance of adapt at i on in
est abl i shi ng bri ght ness const ancy cont i ngent on
cont rast , which cont rast depends on the reflectances
4
3
2
I
0
-I
-ao - 2
I . x Log Z
_ . L I L i I ! I I I
- I 0 I 2 3 4 5
291
4
3
2
!
0
- I
- - dO _
- I t
- o , 2 - " ~ / - " ' I i i i i " ; i
- I 0 I 2 3 4 $
FIG. 17. Increment threshold and constant brightness curves for two human subjects. A test patch subtending 56' by 28'
on a uniform background was presented to one eye, and a comparison patch, on zero background, was presented to the
other eye, except for the bottom curve in each panel, which is a monocular increment threshold curve for each subject.
For each of the constant brightness curves, the luminance of the comparison patch was held fixed, and the luminances
of the background and test patch were varied so that the test matched the comparison in brightness. Therefore, each such
curve represents test and comparisons matched at a constant fixed (subjective) brightness. The test and comparison patches
were flashed for 200 ms, every 1.5 s at the low backgrounds up to every 8 s at the high background levels. The curves
are similar at all brightness levels, having a flat portion and then a sloping portion with slope = 1. At the higher brightnesses,
the transition from flat to sloping portions was somewhat broader than at low brightness or at threshold brightness. Each
cross ( x ) marks the value of I at the intersection of the flat and sloping portions of the curve above it. Units are in log
(photopic) td. From Whittle and Challands (1969).
o f o b j e c t s .
T h e r e h a s b e e n a l o t o f wo r k o n s p a t i a l v i s i o n
o f t h e c o n e s ys t e m, i n p a r t i c u l a r f o v e a l c o n e v i s i o n .
T h e i d e a o f s p a t i a l c h a n n e l s is d e r i v e d f r o m t hi s
wo r k . T h e o u t s t a n d i n g r e s e a r c h o n t h e e f f e c t o f
me a n l u mi n a n c e s o n s p a t i a l c o n t r a s t s e n s i t i v i t y h a s
b e e n d o n e b y v a n Ne s a n d B o u ma n ( 1967) . T h e i r
wo r k wa s p r e s e n t e d b o t h as c o n t r a s t t h r e s h o l d vs
s p a t i a l f r e q u e n c y p a r a me t r i c i n me a n l e ve l s h o wn
i n Fi g . 18, a n d a l s o as t h r e s h o l d c o n t r a s t vs me a n
l e ve l , p a r a me t r i c i n s pa t i a l f r e q u e n c y , as i n Fi g. 19.
Wh a t c a n b e s e e n, e s p e c i a l l y f r o m Fi g. 19, is t h a t
t h e t r a n s i t i o n f r o m s q u a r e r o o t l a w b e h a v i o r t o
We b e r L a w b e h a v i o r d e p e n d s a l o t o n s p a t i a l
f r e q u e n c y . I f we c a l l t h e s p a t i a l f r e q u e n c y k, t h e n
t h e i r r e s ul t s i mp l y t h a t t h e t r a n s i t i o n i l l u mi n a t i o n
IBT is p r o p o r t i o n a l t o t h e s q u a r e o f t h e s p a t i a l
f r e q u e n c y
I aT=A "k 2 ( 18)
wh e r e A is s i mp l y a p r o p o r t i o n a l i t y c o n s t a n t . Th i s
292 R . M. SHAPLEY AND C. ENROTH- CUGELL
I 00
IC
8
0. 0009 0. 009
. /
0.09 9 90
O I I I 0 I 0 0
Spati al frequency in cycles per degree
FIG. 18. The dependence of cont r as t sensi t i vi t y on spat i al f r equency at di f f er ent me a n ret i nal i l l umi nat i ons in t he phot opi c
r ange. Act ual l y what is pl ot t ed is t hr e s hol d modul a t i on M ( what we woul d t e r m t he t hr e s hol d Rayl ei gh cont r as t ) of a si ne
gr at i ng as a f unc t i on o f spat i al f r equency at each of sever al levels o f me a n i l l umi nat i on, i ndi cat ed at t he t op o f t he f i gur e.
Li ght f r om a mo n o c h r o ma t o r was t r a ns mi t t e d t h r o u g h a phot ogr a phi c t r a ns pa r e nc y o f a si ne gr at i ng whi ch was i maged
by a Maxwel l i an vi ew s ys t em on t he s ubj e c t ' s r et i na. The gr at i ng s ubt e nde d 8. 25 deg by 4. 5 deg a nd was f i xat ed, t her ef or e
cent ered on t he fovea. The cont r ast of t he pat t er n was reduced by addi ng a cons t ant level of light f r om anot her monoc hr oma t or .
The t hr e s hol d mo d u l a t i o n is t he r eci pr ocal o f wha t we have cal l ed t he (Rayl ei gh) cont r as t sensi t i vi t y. I n t hi s f i gur e me a n
i l l umi nat i ons ar e i ndi cat ed in phot opi c t d. The wavel engt h was 525 n m. Co mp a r e t hes e da t a wi t h t hos e of Pa s t e r na k a nd
Mer i gan (1981), Fi g. 13. Fr o m va n Nes a nd Bo u ma n (1967).
has interesting consequences for model s of phot opi c
light adapt at i on and in part i cul ar for a model which
uses t he ideas of spat i al f r equency channel s and
adapt at i on pool s, pr esent ed l at er on.
An i nt erest i ng sidelight on Fig. 18 is t hat it
i ndi cat es t hat cont r ast sensitivity cont i nues t o
i mpr ove f or grat i ngs of high spat i al f r equency until
well i nt o t he phot opi c range, and Fig. 19 conf i r ms
t hat fine grat i ngs obey t he squar e r oot law even up
to quite high levels of i l l umi nat i on. I f one accept s
t he qua nt um f l uct uat i on expl anat i on f or this
behavi or , one must concl ude t hat vi si on of fine
pat t er ns is qua nt um limited up to qui t e hi gh light
levels. As before, we must add the qualification t hat
this result does not i ndi cat e defi ni t el y whet her or
not t he retinal gai n is af f ect ed at t hese light levels.
It is i mpor t ant t hat t he cones " s e e " so much
bet t er t han the rods when t he cri t eri on is t hr eshol d
cont r ast . Thi s can be seen in Figs. 8 - 1 0 , and
especially by compar i ng Fig. 11 f r om Dai t ch and
Gr een wi t h Fig. 18 f r om van Nes and Bouman.
Ther e' s a j ump of about a f act or of 10 or so f r om
the opt i mal rod-dri ven cont rast sensitivity of Dai t ch
and Gr een, at about 1 td backgr ound, t o t he best
cont r ast sensitivity of van Nes and Bouma n wi t h
peak c ont r a s t sensi t i vi t i es a bove 200. Thi s
cor r esponds t o a Weber f r act i on (AIT/ IB) of less
t han 0.01, in agr eement with t he sensitivities of
Bl ackwel l ' s subjects who had an asympt ot i cal l y low
Weber f r act i on of 0. 008 (Bl ackwel l , 1946).
However , the si t uat i on ma y be compl i cat ed by
retinal i nhomogenei t y. Koender i nk e t al . (1978)
M i n %
' / ' * " J ' " ' " - L ' ' . ' " ' ' " ' ' ' "
'
4 c o ~ *
~o * 4 8 c ml
4 0
. 3 = .
' l - : , , : 1
o ~ I I , . 1 . , I . . I , , 1 , , I . . I 1
10"3 t O t 10"1 1 10 10 2 10 3~ 10 4
Bo i n t el
FIG. 19. The dependence o f t hr e s hol d mo d u l a t i o n on r et i nal i l l umi nat i on f or di f f er ent spat i al f r equenci es. Wa ve l e ngt h was
525 n m i n t he s a me e xpe r i me nt s as i n Fi g. 18. B 0 is wha t v a n Nes a n d Bo u ma n cal l ed me a n r et i nal i l l umi nat i on, a n d i t
is gi ven i n t d. M is wha t we woul d cal l t hr e s hol d ( Rayl ei gh) c ont r a s t . The s l opi ng por t i ons o f t hes e cur ves ar e t her ef or e
r oughl y consi st ent wi t h t he s quar e r oot l aw, a nd t he fi at por t i ons , wher e cont r as t sensi t i vi t y is c ons t a nt as me a n level changes ,
ar e cons i s t ent wi t h We b e r ' s La w. The t r a ns i t i on bet ween t hes e t wo par t s o f t he cur ve a ppe a r s t o s hi f t t o t he r i ght , t o hi gher
i l l umi na t i ons , f or hi gher spat i al f r equenci es . F r o m va n Nes a n d Bo u ma n (1967).
measur ed cont r ast sensi t i vi t y in cent r al and
peri pheral r et i na (Fig. 12) as a f unct i on of mean
level. They f ound much less i mpr ovement in
cont r ast sensitivity with t he shift f r om r od t o cone
vision in t he per i pher al ret i na. Thi s result suggests
t here may be somet hi ng special about foveal cone
vision whi ch allows especially high cont r ast
sensitivities.
2 . 2 . 3 . TEMPORAL FREQUENCY RESPONSES AND MEAN
ILLUMINATION
As wi t h spat i al f r e que nc y, t he t e mpor a l
f r equency of a stimulus i nfl uences t he dependence
of sensitivity on mean level. Thi s has been shown
by Kel l y (1972). Fi gur e 20 f r om his wor k
demonst rat es the sensitivity f or gratings of di fferent
spatial frequenci es over a range of t empor al
frequenci es at several mean levels. At low spatial
f r equency and l ow t o i nt er medi at e t empor al
f r equency, he obt ai ned Weber ' s Law. At high
spatial f r equency and low t o i nt ermedi at e t empor al
frequenci es he observed t he square r oot law
( i ndi cat ed as D- R f or d e Vr i e s - Ro s e ) . He
di scovered t hat , at ver y high t empor al frequenci es
and low spatial frequencies, sensitivity was mor e or
less i ndependent of mean level. Thi s is t he " l i ne a r "
regi on, so-called because t he visual system appears
t o be behavi ng in a linear manner in t hat t he
sensitivity f or a modul at ed stimulus is not af f ect ed
by t he presence of di f f er ent steady levels. Figure 21
also f r om Kelly (1972) illustrates t hese results in
t erms of t wo s p a t i o - t e mp o r a l adapt at i on maps,
one at a mean i l l umi nat i on of 50 t d and t he ot her
at 200 t d. A compl et e t heoret i cal expl anat i on f or
all these results of Kelly is not available, but we can
i ndi cat e some basic ideas whi ch may account f or
t hem. The effect s of spatial f r equency have been
discussed above. The t endency t owards Weber Law
be ha vi or of l ower t e mpor a l f r equenci es is
compar abl e t o Bar l ow' s (1957) results on steeper
i ncr ement t hr eshol d curves with l onger dur at i on
stimuli. Bot h results suggest t hat t he adapt at i on
mechani sms in t he ret i na are somewhat sluggish in
t i me course and fail t o be as effect i ve on t he
responses t o stimuli which are hi gher in t empor al
f r equency t han 8 Hz as t hey are on responses t o
stimuli l ower in f r equency. Thi s is consi st ent with
Adel son' s (1982) observat i ons about t he onset of
light adapt at i on and with el ect rophysi ol ogi cal
measurement s (Enrot h-Cugel l and Shapley, 1973a;
Bayl or and Hodgki n, 1974; Derri ngt on and Lennie,
1982).
The " l i ne a r " range observed by Kelly (1972) is
somewhat har der t o under st and. Suppose t he gain
of t he r et i na f or high f r equency stimuli is
i ndependent of mean level. Still, one woul d expect
t hat t he great er quant al fl uct uat i ons at high light
levels woul d cause a r educt i on in sensitivity. Thi s
leads t o t he i nference t hat t he noise whi ch limits
per f or mance at high t empor al frequencies must not
294
| I ' \ ]
i o o o " '
D - R
~oo [ ' - 2 cpd l g 7 0 o
2OO
<3
500 O.S c:pd
2 [ ] r I I i~ RECTI LI NEAR PATTERNS
Subj . TZ
I C ) ~ a ; " ~ , ~ I ( d )
1 0 o
o
20 __ ~>
5 o r o o
100 ;
200
8 pd D- R 12 cpd O- R
~ T l , ] [ i J I I r
1 2 5 10 20 50 1 2 5 10 20 50
TEMPORAL FREQUENCY (Hz)
FIG. 20. Thr e s hol d i l l umi nat i on as a f unc t i on o f t e mpor a l
f r equency at di f f er ent spat i al f r equenci es. The t hr e s hol d
i l l umi nat i on AB was t he a mpl i t ude o f si ne gr at i ng whi ch
coul d j us t be seen on a me a n i l l umi nat i on o f B t d. I n each
o f t he f our panel s o f t he f i gur e, t he f our di f f er ent cur ves ar e
f r o m me a s u r e me n t s at t h e f ol l owi ng me a n r e t i na l
i l l umi nat i ons : 36 t d ( ar r owheads ) , 114 t d (t ri angl es), 360 t d
( di amonds ) , a nd 1140 t d (circles). The t est t ar get was a pal e-
green CRT whi ch subt ended 7 deg; it was viewed monocul ar l y
a nd f i xat ed. The gr at i ngs were modul a t e d i n t i me wi t h a
s i nus oi dal wa ve f or m; t he t e mpor a l f r equency o f t he
mo d u l a t i o n is pl ot t ed on t he hor i zont al axi s. Me a s u r e me n t s
f r o m f our spat i al f r equenci es ar e s hown: 0. 5 c deg -1,
2 c deg -1, 8 c deg -~, a nd 12 c deg-L Thr e s hol ds , whi ch ar e
separ at ed f r om t hos e at ot her me a n i l l umi nat i ons by a f act or
whi ch is equal t o t he r at i o o f t he me a n l evel s, c o n f o r m t o
We b e r ' s Law, a nd ha ve a W wr i t t en next t o t he cur ve.
Thr e s hol ds whi ch ri se like t he s qua r e r oot o f t he me a n level
are labeled D- R for t he de Vries-Rose law, s ynonymous wi t h
t he s qua r e r oot l aw. Fr o m Kel l y (1972).
be quant al noise and must be i ndependent of mean
light level. This is not implausible. Most sources of
noise in the visual system, e.g. channel opening and
closing in neur onal membr anes, or spont aneous
t r ans mi t t er r el ease, s houl d have wi de- band
component s. These component s may be relatively
larger at high t empor al frequenci es t han at low,
compar ed t o t he light evoked neural shot noise
caused by quant al fl uct uat i ons. One must suppose
t hat this high f r equency noise is i mmune to t he
a da pt a t i ona l ef f ect s of t he mean level of
i l l umi nat i on. Per haps the noise which limits
det ect i on of high f r equency responses is post-
retinal. In any case, a compl et e and adequat e
expl anat i on f or Kelly' s "l i near r ange" requires
f ut ur e research.
3. GAI N AND CONTRAST GAI N IN
RETI NAL GANGLI ON CELLS
At t he out set of this section on t he physi ol ogy
of ret i nal adapt at i on we concent r at e on retinal
gangl i on cells, t he out put stage of t he retina. All
i nf or mat i on which flows f r om t he ret i na t o the
brai n about t he visual appear ance of t he out si de
world passes along the axons of these ganglion cells.
The evidence of ret i nal adapt at i on in t he activity
of these neur ons allows us t o establish a link
bet ween t he visual, percept ual f unct i on of light
adapt at i on and t he underl yi ng retinal mechani sms.
We will f ur t her concent r at e our at t ent i on on t wo
kinds of retinal ganglion cells in t he cat ' s retina, t he
X and Y cells (see Appendi x 2), because most is
known about t hem. Compar i son with t he retinas
of ot her species and with human vision will be made
frequent l y. As in t he I nt r oduct i on, we stress t he
i mpor t ance of a hi er ar chy of gai n cont r ol
mechani sms at di f f er ent sites in t he ret i na.
Fur t her mor e, t he role of ret i nal gain cont rol s in
maki ng t he ret i na r espond t o cont r ast will be made
evident.
One can speak about the g a i n of retinal ganglion
cells because t hei r i mpul se rat e vari at i on caused by
i ncrement s (or decrement s) of i l l umi nat i on are
pr opor t i onal t o the magni t ude of the i ncrement (or
decrement ) over a consi derabl e range of response
ampl i t ude. Thi s is illustrated by Fig. 22 (Shapl ey
and Kapl an, unpubl i shed). The stimuli were fine
gratings which stimulated the center of the receptive
field. (In this initial discussion we will be dealing
with t he gain of t he cent er onl y, but will consi der
t he gain of t he sur r ound bel ow. )
The rat i o of t he change in impulse rat e with
change in stimulus magni t ude is t he gain, G
G = d R / d I . (19a)
50
20
10
5
2
1
0.5
0.2
>-
(J
Z
O
UL.
--I
<C
I--
'K
50
20
, 0
>-
3
Z 5
IAJ
O
u. 2
..J
k-
,< 1
0.5
0.2
I 2 5 10 20 50 1 2 5 10 20 50
TEMPORAL FREQUENCY (Hzl TEMPORAL FREQUENCY (Hz)
LI NEAR
(const)
FIG. 21. So-called Spat i o- Temporal Adaptation Maps. The adaptation behavior of a human observer is mapped on the
plane defined by spatial frequency and temporal frequency, as vertical and horizontal coordinates. Each of these maps
only applies to one mean retinal illumination: 50 td for the one on the left, and 200 td on the right. They indicate the
slopes of the curves which relate increment threshold to mean illumination, at the different points in the spatio - temporal
frequency plane, de Fries-Rose is equivalent to the square root law, as explained in connection with Fig. 20. Weber means
that, in this spatio - temporal region, increase of mean illumination will cause a corresponding and proportional increase
in the luminance required to reach threshold: in other words, contrast sensitivity will be constant in the region marked
Weber. Li near means that mean illumination does not affect the modulation threshold; in other words, in the Linear region,
contrast sensitivity grows in proportion with mean illumination. The shaded areas are transition zones between the other
regions. From Kelly (1972).
As Cl e l a n d a n d En r o t h - Cu g e l l (1968) s h o we d , t he
r e s p o n s e o f t he c e nt e r me c h a n i s m o f g a n g l i o n cel l s
a c t ua l l y d e p e n d s on t he l u mi n o u s f l ux f al l i ng on t he
c e nt e r o f t he r e c e pt i ve f i el d ( see Se c t i on 3. 5. 1. ) .
Th e r e f o r e , t he ga i n is mo r e p r o p e r l y e xpr e s s e d as,
G= d R / d F ( 19b)
a n d ha s uni t s i mp u l s e s / q u a n t u m ( i / q ) o f l i ght . Th e
f l ux F is t he s t i mul us i l l umi na t i on t i mes t he s t i mul us
a r e a , or , i f t he s t i mu l u s is l a r ge r t h a n t he r e c e pt i ve
f i e l d c e nt e r , s t i mu l u s i l l u mi n a t i o n t i me s t he
s u mmi n g a r e a o f t he c e nt e r .
Th e l i nk b e t we e n vi s ua l s e ns i t i vi t y a n d r e t i na l
ga i n i s ve r y s t r ong. Ba r l o w a n d Le vi c k (1969)
pr e s e nt e d t he a r g u me n t t ha t t hr e e f a c t or s d e t e r mi n e
t he a b i l i t y o f r e t i n a l g a n g l i o n cel l s t o de t e c t a
s t i mul us : (i) t he v a r i a n c e i n t he d i s c h a r g e o f ne r ve
i mpul s e s ; (ii) t he t i me c our s e o f t he r e s pons e whi c h
d e t e r mi n e s t he o p t i ma l i n t e g r a t i o n t i me ove r whi c h
ne r ve i mpul s e s s h o u l d be c o u n t e d b y t he n e r v o u s
s ys t em i n or de r t o de t e r mi ne i f a s t i mul us is pr es ent ;
a n d (i i i ) t he r e t i n a l ga i n. The ga i n wi l l be di s c us s e d
at l e ngt h s u b s e q u e n t l y .
Th e f i r s t o f Ba r l o w a n d Le v i c k ' s t hr e e f a c t o r s ,
t he v a r i a n c e o f t he d i s c h a r g e o f ne r ve i mpul s e s ,
c o u l d c o n c e i v a b l y be i n f l u e n c e d b y p h o t o r e c e p t o r
" n o i s e " , o r b y f l u c t u a t i o n s i n n e u r a l r e s p o n s e due
t o f l u c t u a t i o n s i n t he n u mb e r o f q u a n t a a r r i v i n g
f r o m t he b a c k g r o u n d , or b y p o s t - r e c e p t o r a l ,
i n t r a r e t i n a l " n o i s e " , e. g. s y n a p t i c " n o i s e " . The
s e c o n d f a c t o r , t he o p t i ma l i n t e g r a t i o n t i me i n
Ba r l ow a nd Le v i c k ' s s cheme, is t he d u r a t i o n o f t i me
ove r whi c h ner ve i mpul s e s s h o u l d be c o u n t e d t o
o b t a i n t he be s t s e p a r a t i o n o f s i gnal f r o m noi s e. I t
is gr e a t e r t h a n zer o b e c a u s e t he p h o t o r e c e p t o r s a n d
296
5 0 . . " "
~ 5 0 /
~ 2o
g
I I I I
( o , o ) t 2 3 4
I I I I b
( ) I O 0 2 0 0 5 0 0 4 0 0
F L U X ( x ] O 4 q u o n t o / s e c )
FIG. 22. The proportionality of response with stimulus flux
at different mean levels of illumination in cat retinal ganglion
cells. These data were taken from an X on-center retinal
ganglion cell in a decerebrate, paralyzed cat. The stimuli were
drifting sine grating patterns. The response measure was the
amplitude of the response at 4 I-Iz, the temporal frequency
of the drift. The spatial frequency was chosen to stimulate
the center of the receptive field only; it was 1 c deg -~ (cf.
Linsenmeier et al . , 1982, p. 1175 for a discussion of how
gratings can pick out the center). The stimulus was produced
on a CRT with a white P4 phosphor and subtended 8 deg
by 10 deg on the retina. The center of the receptive field had
a summing area of 0.02 deg 2, approximately, and the stimulus
display was centered on the middle of the receptive field with
a mirror. The mean retinal illumination was controlled with
neutral density filters interposed between the CRT and the
cat. The responses plotted as filled circles were obtained with
a mean retinal illumination of approximately 5.10 s
quanta(507 nm) (deg 2 s)-'. The other two curves were
obtained at ten (open circles), and one thousand (diamonds)
times higher mean retinal illuminations. The stimulus contrast
ranged from 0.02 up to 0.64, but only part of this range is
shown for each background level. The stimulus flux was
estimated by multiplying the amplitude of the stimulus retinal
illumination by the central summing area of the cell. At the
highest mean retinal illumination, the stimulus fluxes would
be off the scale for the two lower means, and so the data
are plotted on a reduced horizontal scale, as indicated in the
figure. The two scales were chosen so that equal horizontal
distance is equal contrast for the open circles and diamonds,
the results from the experiments with the two higher mean
illuminations. The approximate equality of the slopes of the
response curves for these two sets of results implies equal
contrast gain for these two mean levels. However, the main
point of the figure is the linear range of response. Shapley
and Kaplan, unpublished results.
the fol l owi ng ret i nal stages have a pr ol onged
response to each quant um of light (see for exampl e
Fig. 55), and t hus i nt egrat i ng over some finite t i me
allows one to add up the neural consequences of
each qua nt um abs or pt i on. But t he opt i mal
R. M. SHAPLEY AND C . E N R O T H - C U G E L L
i nt egr at i on t i me is less t han i nf i ni t y because the
r et i na' s response to each quant um event ual l y dies
away, so there is no poi nt i nt egrat i ng the neural
response beyond the t i me at which the signal
out wei ghs the noise. Therefore, there is some
opt i mum t i me, about 100 ms, over which the
nervous system shoul d count nerve i mpul ses in
order to detect t hat a st i mul us has been present ed
to the gangl i on cell.
Barl ow and Levick measured how these three
factors depended on backgr ound light i n order to
discover whi ch was most i mpor t ant in cont rol l i ng
the abi l i t y of gangl i on cells to detect a st i mul us-
initiated signal. The mot i vat i on for this analysis was
t hat if these t hree factors cont rol l ed gangl i on cell
per f or mance t hey shoul d al so cont r i but e to
behavi oral sensitivity. They demonst r at ed t hat the
gangl i on cell gai n was reduced dr amat i cal l y by
backgr ound i l l umi nat i on even t hough the vari ance
of the impulse discharge and the opt i mal i nt egrat i on
t i me for retinal responses changed rat her little with
backgr ound. Thi s is i l l ust rat ed i n Fig. 23. They
t herefore f ound compel l i ng evi dence for the
pr oposi t i on t hat the mai n l i nk bet ween visual
adapt at i on and ret i nal adapt at i on is the cont r ol of
ret i nal gai n by steady backgr ound i l l umi nat i on.
Fur t her work by Der r i ngt on and Lenni e (1982), on
the relative const ancy of the vari abi l i t y of the
ma i nt a i ne d di schar ge wi t h me a n level, has
st rengt hened this concl usi on.
3.1. Gain Control in the Scotopic Range
3. I. I. GAIN AND BACKGROUND
Al l of the X and Y cat gangl i on cells st udi ed so
far have received i nput from ret i nal rod and cone
pat hways (Daw and Pear l man, 1969). Thi s gives an
experi ment er the oppor t uni t y to st udy the gai n
cont rol s for the rod and cone pat hways i n an
i ndi vi dual cell. Represent at i ve results on the gai n
of the receptive field cent er as a f unct i on of
backgr ound i n the scotopic range are gi ven i n
Fig. 24 from Enr ot h- Cugel l and Shapl ey (1973a).
The st i mul i were smal l spots placed in the cent er
of the receptive field and modul at ed with a slow
square wave t i me course. The gai n [the i / q rat i o
equi val ent to the gai n as i n equat i on (19)] is pl ot t ed
on doubl e- l ogar i t hmi c coordi nat es vs backgr ound
9
o / e Log (AT o'A'T)
l o g s
Ao
g
-
I " 7 / / I I I I I I I I I
0 I 2 5 4 5 6 7 8
l o g q u o n o ( 5 0 7 ) p e r s q . d e g r e e p e r s e c
FIG. 23. Three factors limit the reliable detection of light by retinal ganglion cells in the cat, and the dominant factor is
the gain. The incremental "threshold" (labeled M 0. A. T, and having units of quanta) of a ganglion cell is plotted here
as filled circles against the background retinal illumination. The open circles are the quant um- spike ratios at different
backgrounds. The quantum - spike ratio is the reciprocal of what we have called gai n. The empty squares are the estimated
optimal averaging time; the empty triangles are the standard deviations of the impulse number distributions. The vertical
coordinates were chosen so that changes in log "threshold" are the sum of the changes in the logarithms of the underlying
factors. Clearly the quantum - spike ratio, the reciprocal of the gain, is the dominant factor. From Barlow and Levick (1969).
i l l umi nat i on. It is seen t hat the gain is const ant for
backgrounds below a critical level, and t hat above
this level the gai n declines al most inversely with
backgr ound. Act ual l y, the typical behavi or of
retinal gangl i on cells is described by the following
equat i on:
GR = GRO / ( 1 +I B/I Ro) P (20)
G R is the gain for rod-driven ganglion cell activity.
GRO is the dark-adapt ed gain for the rod pat hway.
IRO is the i l l umi nat i on at which the gai n has
dr oppe d by 2 -P and is r ef er r ed t o as t he
"t r ans i t i on i l l umi nat i on". P is the exponent of the
t erm in the denomi nat or which depends on the
act i on of the gai n cont rol ; P is also the slope of the
gain vs background curve on log - log cooordinates.
For the cells in the Enrot h-Cugel l and Shapley
(1973a) st udy, the average value of P was 0.9. This
is very close t o Weber' s Law which woul d have an
exponent of 1 instead of 0.9 in the denomi nat or .
At mean ret i nal i l l umi nat i ons above 5.108
quanta(507 nm) (deg 2 s)-' the gain of the rod
pat hway declines more steeply t han equat i on 20
woul d indicate, because of " r o d s at ur at i on"
(Lennie e t al . , 1976).
The value of the t ransi t i on i l l umi nat i on IRO,
varied over a range of two log units, f r om about
300 quant a( 507 nm) (deg 2 s)-I up t o 3.104
quant a(deg 2 s)-' . The ganglion cells with the largest
centers, presumabl y large peripherally located Y
cells, had the lowest values of the t ransi t i on
i l l umi nat i on.
Barlow and Levick (1976) and Barlow (1977) have
suggested t hat the transition illumination, IRO, may
be anal ogous to the " da r k l i ght " inferred from the
pl at eau in the human psychophysi cal increment
sensitivity at low backgrounds. There is a similarity,
2 . 5 x 1 0 s
~ 2 . 5 x 10 4
E 2"5 x 103
I I I I I i
iS
I I I I 1
10 2 10 4 10'
0 . 0 ~ 4
0 . ~ 4
0-04
Backgr . r et . i l i um, q(507 nm) / sec, deg 2
o"
o v
,,J
m
2"5 x 105
2 5 x 10"
2.5 x 102
I I I I I _ I
i ,
10 = 10 4 10'
Backgr. rec. i l i um, q(507 nm) / sec, deg 2
0.0004
0 . 0 0 4
0 . 0 4
o
FIG. 24. Gai n vs backgr ound i l l umi nat i on, in t he scot opi c range, f or cat ret i nal gangl i on cell cent ers. Ret i nal fl ux [in uni t s
o f quant a(507 nm) s-' ] r equi r ed f or a smal l cent r al st i mul us t o elicit a cr i t er i on r esponse (30 i mpul ses s -~) is pl ot t ed vs t he
ret i nal i l l umi nat i on o f a 12 deg concent ri cal l y l ocat ed backgr ound. The gai n in i mpul s e s / qua nt um ( i / q) is i ndi cat ed al so
on t he ri ght hand vert i cal scales. The l at t er quant i t y was cal cul at ed by mul t i pl yi ng t he st i mul us ret i nal i l l umi nat i on by t he
ar ea o f t he st i mul us, 0.03 deg 2, and by a f act or o f 1/ 3, t he est i mat ed f r act i on o f qua nt a i nci dent on t he ret i na whi ch were
abs or bed. I n t he l eft ha nd panel , t he filled circles are f or whi t e st i mul i on a whi t e backgr ound; t he open circles ar e f or
b l u e - gr een st i mul i on a r ed backgr ound, t o demons t r at e r od i sol at i on. I n t he ri ght panel all t he poi nt s ar e f or whi t e on
whi t e. The resul t s in t he l eft panel ar e f r om an on- cent er gangl i on cell; t he resul t s in t he r i ght panel ar e f r om an of f - cent er
cell. Fr om Enr ot h- Cugel l and Shapl ey (1973a).
because bot h t he " d a r k l i ght " and t he t ransi t i on
i l l umi nat i on are needed t o account f or observed
plateaus: the backgr ound i l l umi nat i on must exceed
IRO f or t he gain t o dr op f r om its dar k adapt ed
val ue in gangl i on cells, while t he backgr ound
illumination must exceed I D, the " da r k l i ght ", f or
the psychophysi cal sensitivity t o dr op f r om its dar k
adapt ed value. However , t he f unct i onal di fference
out wei ghs t he appar ent similarity. The t ransi t i on
i l l umi nat i on is i nvol ved in gain cont rol ; t he " da r k
l i ght " (either estimated f r om psychophysics or f r om
physiological experiments) sets the noise level of the
ret i na in t he dark. This ar gument is suppor t ed by
the est i mat ed values of " d a r k l i ght " and t he
t ransi t i on i l l umi nat i on, which are qui t e di fferent .
The " dar k l i ght " of cat ganglion cells was estimated
by Barl ow et al. (1971), as follows. Based on t he
value of t he mai nt ai ned discharge in t he dark, and
the slope of t he stimulus - response curve obt ai ned
in t he dark, these aut hor s est i mat ed t he magni t ude
of t he light flux which woul d have been requi red
t o generat e t he mai nt ai ned di scharge in t he dark,
and called this val ue t he " d a r k l i ght ". They f ound
a wide variation in this estimate of the " dar k l i ght ".
However , t aki ng t hei r highest value, t he " d a r k
l i ght " was equivalent to about 100 quant a s -1 retinal
flux. For a cell with a small cent er, say about
0.1 deg 2 in area, this woul d be pr oduced by 103
quant a(deg 2 s) -t retinal illumination; f or the largest
cells it woul d be pr oduced by about 3 q(deg 2 s) -1.
These values for the feline " da r k l i ght " are t oo low,
by at least a f act or of t en, f or t he " d a r k l i ght " t o
be equi val ent t o t he t ransi t i on i l l umi nat i on in cat
ret i nal gangl i on cells. Rat her, some cri t eri on
amount of voltage or current or subst ance in a
retinal cell, much larger t han t hat caused by " d a r k
l i ght ", must be exceeded, and t hen t he gain cont rol
of adapt at i on begins t o act. As argued in Sect i on
2.1.1.2., " da r k l i ght " pr obabl y limits sensitivity by
provi di ng a noise, t he " da r k noi se", against which
a signal must be pi cked out , r at her t han by setting
t he gain.
3. 1. 2. GAIN AND DYNAMICS
Ther e are dynami c consequences of adapt at i on
which are hi dden in t he simple pi ct ure of Fig. 24.
As shown in Fig. 25, t he t i me course of response
of t he recept i ve field cent er varies with adapt at i on
level, as f ound bot h by Yoon (1972) and by Enr ot h-
Cugell and Shapl ey (1973a). The nat ure of t he
change is t hat t he response of t he cent er t o an
i ncrement al step of i l l umi nat i on becomes mor e
t ransi ent , t he mor e light adapt ed t he cell is in t he
q Q t/Q
r a t i o - J . e - - 1 . 2 5 sec ~ l [ O n r a t i o
- - - I O n I I ~
0 0 2 .
0 0 0 6 1 5 0 i m p u l s e s ] s e c
( a )
0 .0 8
0-01
I 5 0 im p u ls e s / s e e
( b )
FIG. 25. Ti me cour se o f ( r od- dr i ven) squar e wave r esponses at di f f er ent adapt at i on levels i n cat ret i nal gangl i on cells.
(a) The r esponses (averaged over many st i mul us cycles and s moot hed) o f t he recept i ve fi el d cent er o f an on- cent er cell at
fi ve di f f er ent levels o f ba c kgr ound ret i nal i l l umi nat i on: (a) l - - 5 0 quant a( deg 2 s) "1, ( a ) 2- - 6. l & quant a( deg a s) - ' , ( a) - - 6" l &
quant a( deg 2 s) -1, (a)4---9.104 quant a( deg 2 s) -t , a nd ( a) 5- - 5" l & qua nt a (deg 2 s) -1.
(b) A similar result is shown for an off-center cell at three background illuminations: (b)l--100 quanta (deg 2 s) -t, (b)2--3. l&
quanta(deg 2 s) -l, (b)3--103 quanta (deg 2 s)-'. Note that in the cat 1 deg2= 0.048 mm a, approximately.
For each response the i / q ratio, the gain, is shown at the left of the averaged response histogram. The time courses of
the responses and the i / q ratios at the top of each column were the same as those obtained in total dark adaptation. The
drop in gain with increase in background illumination goes hand in hand with the change in time course observed in the
histograms. From Enroth-Cugell and Shapley (1973a).
scotopic range. This finding applies to off-center
as well as to on-center cells, and to X as well as Y
cells (Jakiela e t al . , 1976).
This change in time course of response with
adapt at i on is related to another observation: the
steepness of the decline in gain with background
depends on the temporal pattern of the stimulus
(and response). For example, the results in Fig. 24
were derived from measurements of the peak
response to an incremental step of illumination on
a background. One would obtain rather similar data
from measurements of the gain of the response to
a sinusoidally modul at ed small spot for temporal
frequencies of 2 Hz or less. In this case, either peak-
to-peak impulse rate modul at i on or the amplitude
of the sinusoid which is the best approxi mat i on to
the neural response are two response measures
which would give the same dependence on
background. Similar measurements at 8 Hz or
above have a shallower dependence on background,
i.e. the exponent P in equation (20) would be
around 0.6 for intermediate temporal frequencies
of modul at i on (between 3 and 10 Hz; Enroth-
Cugell and Shapley, 1973a; Derrington and Lennie,
1982). The responses to temporal frequencies above
16 Hz suffer almost no attenuation in amplitude
with increases in mean level; for such high temporal
frequencies, the exponent P in equation (20) is near
zero (Shapley e t al . , 1983). Previously, Sakmann
and Creutzfeldt (1969) and Barlow and Levick (1976)
also observed shallow slopes of gain vs background
curves with brief incremental stimuli. The responses
to such brief pulses of light, which contain a wide
range of temporal frequency components, follow
a gain vs background curve which obeys equation
(20) with an exponent of about 0.6 on the average.
However, as presented earlier, the gain of the peak
of the response to a prolonged flash has a steeper
dr opof f of gain with background; the exponent in
this case is about 0.8, according to Barlow and
300
Levi ck (1976; however, cf. Cl el and and Enr ot h-
Cugell, 1970; and Enr ot h- Cugel l and Shapl ey,
1973a in whi ch P = 0.9). The st eeper sl ope f or t he
l onger fl ash makes sense because t he pr ol onged
flash can be vi ewed as t he sum of pr edomi nant l y
l ow f r equency component s , which t end t o be
at t enuat ed mor e by i ncreases in backgr ound
( adapt i ng) light.
Ther e is a good r eason t o consi der t he effect s of
a da pt a t i on on di f f er ent t e mpor a l f r equency
component s . As ment i oned in Sect i on 1.2.2., t he
response of the ret i na t o st i mul at i on by light shoul d
be considered t o be a f unct i onal , or t ransf ormat i on,
of t he st i mul us. I f L ( t ) is t he st i mul us, t hen t he
r esponse is R = R{ ( t , L( t ) } . That is, t he response R
depends on t i me and, f ur t her mor e, t he response at
t i me t depends on t he val ue of t he st i mul us at t i me
t and also the values of the stimulus in the past. This
is a f or mal way of expressi ng what is well known
about the retina: it has a finite i nt egrat i on time, and
there are sluggish gai n cont rol s, in the recept ors and
t he net wor k, which modi f y the r et i na' s r esponse
cont i ngent on t he past hi st or y of i l l umi nat i on.
Ther e is a st andar d mat hemat i cal appar at us for
anal yzi ng f unct i onal s; it is called syst ems anal ysi s.
A par t i cul ar l y useful subset of this appar at us is
l i near syst ems anal ysi s, a mat hemat i cal t echni que
f or anal yzi ng f unct i onal s whi ch are linear, i.e.
systems in which the response to t wo separat e inputs
is si mpl y t he sum of the responses t o each of the
inputs presented alone. In analyzing a linear system,
si nusoi ds are t he st i mul us of choi ce because t hey
pass t hr ough such a s ys t em unc ha nge d in
wavef or m, t hough scaled in ampl i t ude and shi ft ed
in phase. Whi l e t he ret i na is deci dedl y not l i near
under all condi t i ons, it may behave like a l i near
syst em ar ound an oper at i ng poi nt set by t he mean
level of i l l umi nat i on, and t her ef or e the retinal
responses to si nusoi ds of di f f er ent t empor al
f r equency serve t o pr ovi de a good quant i t at i ve
descri pt i on of how t he retinal f unct i onal behaves
at di f f er ent mean levels of i l l umi nat i on.
The di f f er ent effect s of backgr ound on t he
responses of gangl i on cells t o di f f er ent t empor al
frequenci es can be expl ai ned by a t heor y in which
the centerpiece is a gai n cont rol which is a nonl i near
negat i ve f eedback ( Enr ot h- Cugel l and Shapl ey,
1973a). In or der t o account f or t he i ncreased
t ransi ence of squar e wave responses in t he light
adapt ed st at e (Fig. 25), one must assume in this
t heor y t hat t he gai n cont r ol has a s omewhat mor e
prol onged i nt egrat i on t i me t han the phot orecept ors.
Accor di ng t o this view, t he decay seen in t he
gangl i on cel l ' s st ep r esponse is due to t he
i ncrement al increase in the val ue of the gai n cont rol
signal due t o t he st ep st i mul us.
3.1.3. ADAPXAXION or THE SURROUNO MECHANISM
The sur r ound of t he recept i ve field also adapt s
to backgr ound light in the scotopic range. Figure 26
o"
g
E
__=
E
10 5
10 4
10 3
Su r r o u n d X
Z (
. ~ e ~ / ~ ' C e n t r e
1 ;I ] I I I
0 10 3 10 4 10 "~ 10 6
10 5
10 4
10 ~
- - o - - - / ~ -
- - 0 - - / ;
sur
7 Ce n t r e
j = j
I 4 k , , I I I |
0 10 3 10 4 qO ~ 10 6
B a c k g r o u n d i l l u m i n a t i o n ( q u a n t . a / d e g 2 s e c )
FIG. 26. Comparison of center and surround gains in cat
retinal ganglion cells. Plotted vertically is the stimulus retinal
illumination required to evoke criterion responses as a
function of the background retinal illumination plotted on
the horizontal axis. Upper and lower panels are from two
different on-center X ceils. For the centre responses (filled
symbols) the criterion was ten extra impulses evoked during
a one second presentation of an increment of the illumination
of an opt i mum spot which just filled the center. For the
surrounds (empty symbols) the criterion was determined from
st i mul us- r esponse curves for opt i mum spots and diffuse
illumination. The criterion illumination for the surround was
such that the response to diffuse illumination of this amount
was ten impulses less than the response to an opt i mum spot
of the same retinal illumination. Retinal illuminations are
given as quanta (507 nm) (deg 2 s)-' incident on the retina,
under the assumption that 75% of the quant a incident on
the cornea reach the retina. Rod isolation was insured by the
use of bl ue- green stimuli on red backgrounds. From Enroth-
Cugell and Lennie (1975).
from Enroth-Cugell and Lennie (1975) reveals the
kinds of surround adaptation which are seen. In
these experiments, the surround response was
estimated by subtracting the center response from
that obtained by illumination of both center and
surround. The data are the incremental illumination
required to elicit a criterion surround response; thus
these curves may be interpreted as indications of
changes in surround gain with background
illumination. In the upper panel, the surround and
center begin to reduce their gains together at
roughly the same level of background. In the lower
panel the surround starts off with a lower dark-
adapted gain, but reduces its gain with background
at a higher level than the center. The result is that
in both cases the center and surround have roughly
the same gains (integrated over their respective total
summing areas) in the Weber-Law, light adapted
scotopic range. But there are differences across the
population of retinal ganglion cells in the relative
gain of center and surround in the low scotopic
range (see also Kaplan et al . , 1979).
The results of the well-known investigation of
Barlow et al. (1957) are sometimes interpreted to
mean that the gain of the surround goes to zero in
total dark adaptation. This, however, is not
precisely what Barlow et al. found. Their results on
the dependence of gain on area at different
backgrounds implied that the ratio of the gain of
the center to the gain of the surround increased in
total dark adaptation. However, the extent of the
increase in the cent er - sur r ound ratio was not
determined in their study. It was later shown by
Enroth-Cugell and Lennie (1975) and by Kaplan et
al. (1979) that this ratio may increase from a value
of 1.2 in the light adapted state to as much as 3 in
the dark adapted state. That is, the surround is
relatively weaker compared to the center in the
dark, but it is not gone. In fact, the gain of the
surround is always maximal when the retina is dark
adapted (see Fig. 26). In other words, as the
background level is increased from total darkness,
the center gain usually is reduced at a lower level
of background than is the surround' s gain.
There is a methodological reason for the
differences in conclusions about the strength of the
surround in the dark. Barlow et al. (1957) used
auditory threshold for an "off-response" to
measure the magnitude of the response of the
301
surround in on-center cells. This method has the
disadvantage that, in these cells, the surround
response consists of sustained inhibition when the
surround mechanism is dark adapted (Enroth-
Cugell and Lennie, 1975). The presence and
magnitude of the "off-response" is associated with
the adaptation level, just as the magnitude of the
center's transient overshoot depends on the center
being somewhat light-adapted (see Fig. 25). Enroth-
Cugell and Lennie (1975) and Kaplan et al. (1979)
measured magnitude of inhibition as an indicator
of surround response strength, and they did it with
objective averaging techniques. Their work reveals
that there are marked variations across the
population of ganglion cells in the degree to which
background illumination affects the ratio of the
center and surround gains (see Fig. 26). The finding
of variability in the degree of cent er-surround
balance in the dark has also been reported by
Barlow and Levick (1976).
The fact that background light in the scotopic
range can affect the gains of center and surround
differently implies that, in this range, the gains of
these receptive field mechanisms are controlled at
a site (or sites) in the retina more proximal than the
photoreceptors. If the only site of gain reduction
were the photoreceptors, one would observe that
the gains of center and surround would begin to
drop at the same background level. There is good
evidence that at higher backgrounds some of the
reduction in gain in the mammalian retina is due
to photoreceptor adaptation (Sakmann and Filion,
1972; Valeton and van Norren, 1983). These
observations are consistent with our assertion in the
Introduction that there is a hierarchy of gain
controls.
The ratio of the total integrated gains of center
and surround in the light-adapted state is
approximately 1.2 for a large population of retinal
ganglion cells (Linsenmeier et al . , 1982). There is
considerable variance in this ratio among the
ganglion cell population. In any one cell, the ratio
is approximately constant from 10-2-5cd m -2 back-
ground luminance on up (Enroth-Cugell and
Lennie, 1975). Thus, in cat ganglion cells the
balance between center and surround is established
in the low- to mid- scotopic range and is invariant
with adaptation level throughout the mid- to high
scotopic and photopic ranges.
302
3.2. Gain Control in the Photopic Range
The i nput s f r om cones t o cat gangl i on cells can
be isolated f r om t hose f r om rods by means of Stiles'
t wo-col or t echni que (see Wyszecki and Stiles, 1967,
p. 572). When this is done, it is f ound t hat cone
signals have a const ant gai n over t he r ange t hat t he
gai n of r od signals dr ops by a f act or of one
t hous and or mor e ( Enr ot h- Cugel l e t a l . , 1977a),
f r om t ot al dar k adapt at i on t o t he high scot opi c
range. Thi s can be seen in Fig. 27. Pl ot t ed t here are
the t hreshol d illuminations for criterion cone-dri ven
and r od- dr i ven responses t o be elicited by a test
stimulus on a bl ue backgr ound, as a funct i on of the
level of backgr ound. For a single gangl i on cell one
obt ai ns a t wo- br anched gai n vs backgr ound curve
whi ch is r emi ni s cent of t he t wo- br a nc he d,
psychophysi cal sensitivity vs backgr ound curves
(Fig. 8). This indicates t hat the separat e gai n cont rol
of r od and cone signals is achi eved by t he ret i na
pr i or t o t he gangl i on cells, and t hat r od and cone
signals are kept segregat ed at least up t o t he poi nt s
at which t he gains are set in t he paral l el " r o d " and
" c o n e " pat hways t hr ough the retina. These results
are f ound for receptive field centers of bot h on- and
of f - cent er cells, and f or bot h X and Y cells. Thi s
has the added i mpl i cat i on t hat r od and cone signals
are segregat ed in bot h t he X and Y pat hways until
the gai n is set.
The results in Fig. 27 i mpl y i ndependence of
adapt at i on mechani sms for the r od and cone
pat hways t o the gangl i on cells in the cat. However ,
Nel son (1977) f ound t hat r od signals are coupl ed
i nt o cones. Hi s wor k led hi m to the concl usi on t hat
t he mai n pat hway of r od signals t o hor i zont al cells
was t hr ough t he cones. Pr es umabl y a si mi l ar
concl usi on woul d appl y t o t he bi pol ar cells. That
is, r od signals shoul d t ravel t hr ough cone bi pol ar
cells because of t he large amount of coupl i ng of rod
signals i nt o cones. Thi s poses a pr obl em, namel y
how can the cone and r od signals adapt separ at el y
when t hey are carri ed by t he same i nt er neur ons?
One possi bl e expl anat i on is t hat all adapt at i on may
t ake pl ace in r ecept or s, but t hat expl anat i on has
1 0 -
' ~ L _
~s
- o 8
A
E
C
o
o 6
O .
4
On-centre X ~ , , " /
L - - . / , , l I I I I I I I I
--o0 3 5 7 9 11
L o g background (photons (500 nm) deg -2 sec -1)
_ ----
11 ?
" V
E
c
9 e
7 ~
FIG. 27. Gain for the rod and cone systems in a cat retinal ganglion cell. The illumination required to evoke a criterion
response is graphed vs the background illumination. The points plotted as filled symbols were obtained with a blue - green
stimulus light on a bl ue - green background, and were taken to represent the gain of the rod pathway. Their values a r e
given by their heights on the left vertical axis, in equivalent quanta of a monochromatic 507 nm light. The empty symbols
are the criterion illuminations for a red spot of light on the same blue - green background, and are interpreted as indicating
the cone pathway' s gain. The response criterion was just-audible synchrony of the cell's firing rate with the 4 Hz square
wave modulation of the small stimulus spot (0.2 deg diameter), which was located in the middle of the receptive field.
In this figure, retinal illuminations are referred to quanta at the cornea, before losses in the eye. From Enroth-Cugell e t
al . (1977a).
ot her pr obl ems wi t h t he spat i al i nt er act i ons whi ch
are i nvol ved in adapt at i on. At present we can onl y
rai se this issue as one whi ch mus t be resol ved by
f ut ur e r esear ch.
The gai n in t he phot opi c r ange is pr opor t i onal
t o 1 / I B, on t he a ve r a ge , a b o v e a cr i t i cal
ba c kgr ound i l l umi nat i on/ co ( Daw and Pear l man,
1969; Enr ot h- Cugel l e t al . , 1977a). Thus a
descri pt i on of t he gai n f or t he cone syst em in Fig. 27
is (with Gc0 t he dar k adapt ed gai n of t he cone
si gnal s, /co t he i l l umi nat i on at whi ch t he gai n is
hal ved):
303
respect t o t hei r dar k adapt ed val ues ( Jaki el a e t al . ,
1976; Enrot h-Cugel l e t al. 1977a). I f the t i me course
of t he st ep r esponses are a resul t of t he act i on of
ret i nal gai n cont r ol s, t hese resul t s i ndi cat e t hat t he
gai n cont r ol mechani s m f or X cells is not t he same
as f or Y cells. I t suggests t hat t he X cel l ' s gai n is
cont r ol l ed by a mechani s m wi t h a l onger t i me
const ant t han t he gai n cont r ol f or t he Y cell. Such
a concept of t wo gai n cont r ol s, one f or X and one
f or Y, arises also in t he consi der at i on of t he spat i al
pr oper t i es of ret i nal gai n cont r ol s, and will be
di scussed bel ow.
G c = Gc0/(1 +I a/ I c o) (21)
and t he gai n of t he gangl i on cell woul d be
G = G c + G R (22)
i f we assume t hat r od and cone signals are si mpl y
added ( Enr ot h- Cugel l e t al . , 1977b).
The t i me cour se of t he gangl i on cel l ' s r esponse
under goes anot her change at t he r od - cone br eak.
Thi s is i l l ust rat ed in Fig. 28 f r om Enr ot h- Cugel l e t
al. (1977a). When t he backgr ound put s t he cell i nt o
t he me s opi c r ange, but is less t ha n /co, t he
response t o a small i ncrement of i l l umi nat i on which
onl y st i mul at es t he cones is sust ai ned, like t he
r esponse t o a st i mul us whi ch onl y st i mul at es t he
r ods in t he dar k adapt ed st at e. As t he backgr ound
is i ncr eased a bove / c o, t he st ep r esponse becomes
mor e t ransi ent , recapi t ul at i ng the r od results. Thus,
t he r esponse t o a st ep of light in a cat gangl i on cell
is sust ai ned in t ot al dar k adapt at i on, becomes mor e
t r ansi ent t hr oughout t he scot opi c range, becomes
sustained agai n j ust above the r od - cone t ransi t i on,
t hen becomes mor e t r ansi ent agai n in t he mi d- t o
hi gh- phot opi c range. The r emar ks above about t he
expl anat i on of t he effects of adapt at i on on response
t i me cour se in t he scot opi c r ange shoul d al so appl y
t o t he phot opi c range. One shoul d expect t hat a
nonl i near f eedback is t he mechani s m whi ch links
gai n r educt i on wi t h t he change in r esponse t i me
course.
Bot h in t he scot opi c and phot opi c ranges, t he
i ncr ement al st ep r esponses of Y cells decay at a
f ast er rat e t han X cells when bot h cell t ypes are in
t he Weber Law regi ons of t he gai n vs. backgr ound
curve and have suf f er ed t he same dr op in gai n wi t h
3 . 3 . Co n t r a s t Ga i n
We have pr esent ed t he ar gument earlier t hat one
pur pose, per haps t he mos t i mpor t a nt pur pose, of
light adapt at i on is t o maxi mi ze t he vi sual cont r ast
sensitivity and to keep it const ant as the backgr ound
or mean level vari es. One of t he det er mi nant s of
cont r ast sensi t i vi t y is cont r ast gai n, or how l arge
a r esponse is pr oduced by a gi ven a mount of
cont r ast . The cont r ast gai n Gcon is t he backgr ound
i l l umi nat i on I B t i mes t he Gai n G as defi ned in
equat i on (19a), so
Gcnn = ]B" (GR + Gc) (23a)
Gon = GR0"IB/ ( 1 + I a/I Ro) P +
Gco" I B/ (1 + I s / Ico). (23b)
I f t he gai n is expressed as i mpul s e s / qua nt um as in
equat i on (19b), t hen t he cont r ast gai n is equal t o
ga i n. ba c kgr ound fl ux. I n ei t her case, t he cont r ast
gai n has uni t s of [i mpul ses s- ' ] [ cont r ast ] -1, or ma y
somet i mes be expressed as [i mpul ses s- ' ] [ per cent
cont r ast ] -1 i f cont r ast is gi ven in per cent age r at her
t han as a f r act i on.
A gr aph of t he cont r ast gai n in single gangl i on
cells is shown in Fig. 29 (Shapl ey e t al . , 1983). The
cont r ast gai n i ncreases st eadi l y in t he scot opi c
range, t hen levels of f (or somet i mes may even dr op
s omewhat ) as t he cell ent ers t he phot opi c range. X
and Y cells have a si mi l ar dependence of cont r ast
gai n on mean level.
The dependence of cont r ast gai n on mean level
is rel at ed t o t he dependence of gai n on mean level.
I n t he r ange of backgr ounds in whi ch I a is much
i
E
c
o
0
1 3 - -
11
On-centre X
/
I 5 0 i m p u l s e s s e c - 1
I , I , I , I , I , I , I , I , I
5 7 9 11 13
Log b a c k g r o u n d ( p h o t o n s (560 nm) deg - I sec -~)
FIG. 28. Change of time course and gain in cone-driven X ganglion cell responses as a function of increasing background
illumination. The curve plots the retinal illumination (referred to the cornea) required to evoke a criterion peak response
of 35 impulses s -~ above the mean impulse rate. Stimuli were 0.2 diameter red spots located at the midpoint of the receptive
field center, and were modulated in a square wave manner at 0.5 Hz. The background was blue - green, in order to suppress
the rods and yield an isolated cone-driven response. From Enroth-Cugell et al. (1977a).
l arger t han t he t ransi t i on i l l umi nat i on IRO, and the
response is dri ven by rods, t he slope of the cont r ast
gai n curve on l o g - log coor di nat es is 1 - P , when
t he slope of t he gai n curve is - P. Thus, Weber ' s
Law, when the slope of the gain curve is - 1, implies
a sl ope of t he cont r ast gai n curve of zero. When
P is great er t han 1, in t he regi on of r od sat ur at i on,
t he slope of t he cont r ast gai n curve becomes
negat i ve, and t he cont r ast gai n act ual l y dr ops.
3. 4. Effect of Adaptati on on the Size of the
Receptive Field Center
Ther e is evi dence t hat t he size of the recept i ve
field center in cat retinal gangl i on cells is pract i cal l y
const ant over wi de ranges of mean level or
backgr ound level of i l l umi nat i on. Smal l er and
larger spots which fall compl et el y within the central-
summi ng ar ea of a recept i ve field have al most
i dent i cal gai n vs backgr ound curves, as i mpl i ed in
Fig. 30 (Cl el and and Enr ot h- Cugel l , 1968). I n t he
fi gure, gai n vs ar ea was measur ed f or a single
ga ngl i on cell at sever al di f f e r e nt s c ot opi c
backgrounds. The parallelism of the curves suggests
t hat all these spot s of di f f er ent sizes were af f ect ed
t o t he same ext ent by the i ncrease in backgr ound
illumination. Cleland and Enrot h-Cugel l (1968) also
showed t hat t he di st r i but i on of l umi nous flux
a mong several spot s pr oduced exact l y t he same
response in magni t ude and t i me course as t he same
l umi nous flux concent r at ed in a single spot , as l ong
as all stimulus spots were pl aced at equally sensitive
poi nt s in t he recept i ve field cent er. Thi s led t o t he
concept of a single cent er - mechani sm or cent ral
s umma t i on pool wi t hi n which neural signals are
added; the evidence of Fig. 30 suggests t hat , at least
under some exper i ment al condi t i ons, t he recept i ve
field cent er adapt s as a uni t at a site in t he ret i na
at which t he cent er' s signals have been pool ed. Thi s
finding applies t o the receptive field in the phot opi c
as well as t he scot opi c r ange ( Enr ot h- Cugel l e t al . ,
1977a).
However , t here are some dat a i ndi cat i ng some
var i at i on of recept i ve field cent er size wi t h mean
level. All t hese results have been obt ai ned f r om
exper i ment s which used si nusoi dal grat i ng stimuli
t o est i mat e t he size of t he center. The first result
VI SUAL ADAPTATI ON AND RETI NAL GAI N CONTROLS
305
o
5
o
4
-%
~3
E
2
z
c9
1
z
8
O
o
I
- 5 2
A
I I I I
- 2 -1 0 1
LOG MEAN LUMINANCE ( c d / mZ )
FIG. 29. Cont r ast gain in cat retinal gangl i on cells as a
funct i on of mean luminance. The stimuli were drifting sine
gratings, presented at (Rayleigh) cont rast s f r om 0.02 (2%)
up to 0.64 (64%). The t emporal frequency of t he dri ft was
4 Hz. Mean stimulus l umi nance was varied over a four to
five log unit range with neutral density f'dters. The CRT screen
had a white P4 phosphor. The phot opi c l umi nance of t he
screen was measured; t he scotopic equivalent l umi nance is
approxi mat el y twice t he phot opi c for t hi s light. Artificial
pupils, 3 mm in diameter, were used. With such a pupil, 1 cd
m -2 produces a retinal i l l umi nat i on of approxi mat el y 4.106
quanta(507 nm) (deg 2 s) -' on t he cat ' s retina. The slope of
t he linear por t i on of t he response - cont rast curve provided
an estimate of t he cont rast gain in impulses s -1 [contrast]-L
These are t he results from t hree different on-cent re X cells;
off-cent er and Y cells gave essentially similar results. The
responses at t he highest mean l umi nance used, 100 cd m -s,
were cone-driven, but responses at lower mean levels were
rod-driven. Fr om Shapley et al. (1983).
i s t h a t o f E n r o t h - C u g e l l a n d R o b s o n ( 1 9 6 6 ) wh o
f o u n d a t wo - f o l d r e d u c t i o n i n t h e r e c e p t i v e f i e l d
c e n t e r d i a me t e r o f a n X c e l l wh e n t h e me a n l e ve l
wa s v a r i e d f r o m 5" 10 .4 t o 16 c d m -2, a p p a r e n t l y
mo s t o f t h e c h a n g e t a k i n g p l a c e a t t h e l o w e n d o f
t h e r a n g e o f me a n l e ve l s , a s s e e n i n Fi g . 31. S i mi l a r
r e s u l t s h a v e r e c e n t l y b e e n o b t a i n e d b y De r r i n g t o n
a n d L e n n i e ( 1 9 8 2 ) wh o r e p o r t a 32070 r e d u c t i o n i n
c e n t e r d i a me t e r wh e n t h e a v e r a g e i l l u mi n a t i o n wa s
i n c r e a s e d f r o m 2 . 1 0 -3 t o 2 0 0 c d m- L S i n c e t h e s e
me a n l e v e l s s p a n t h e r o d - c o n e t r a n s i t i o n i n t h e c a t
wh i c h o c c u r s a r o u n d 1 0 - 100 c d m -2 i n wh i t e l i g h t
( wh e n a 3 mm p u p i l d i a me t e r i s u s e d ; c f . E n r o t h -
Cu g e l l et al . , 1 9 7 7 a ) , o n e wo u l d wi s h t o h a v e mo r e
d e t a i l e d k n o wl e d g e a b o u t h o w t h e c e n t e r s i ze v a r i e d
wi t h a v e r a g e l i g h t l e ve l b e f o r e f o r mu l a t i n g a n
e x p l a n a t i o n o f t h e c e n t e r ' s c o n t r a c t i o n i n t h e l i g h t .
Ho we v e r , t h e r e s u l t s o f E n r o t h - C u g e l l et al. ( 1 9 7 7 b )
o n t h e r e l a t i v e s i z e s o f t h e r e c e p t i v e f i e l d c e n t e r
7
6 ~ i . e
|
.~_
- ~ 1,e ~
p ~
2 2"6
1
0 t t I I I I I
0.1 0. 2 0-3 O . S 0 . 7 1 2 3
Bt i mu] us c ~ me t e r , degrees
FIG. 30. Ar ea- s ens i t i vi t y curves at several backgr ound
luminances in cat ganglion cells. In this figure t he label on
t he ordi nat e, "sensi t i vi t y", is used t o mean what we have
called " ga i n" . The diameter of a circular spot centered on
t he receptive field was varied in steps and t he l umi nance
required to produce a criterion response was measured at each
value of t he diameter. The t emporal modul at i on was a 4 Hz
si newave. The cr i t er i on r esponse was j us t - audi bl e
synchroni zat i on of t he cell' s discharge with t he stimulus
modul at i on. The sloping and flat port i ons of these curves
intersect at a diameter denot ed D, which is t aken t o be t he
di amet er of t he central summing area of t he receptive field
cent er. In t hese experi ment s t he val ue of D, was
approximately constant across background level. Zero on t he
"Rel at i ve sensitivity" scale corresponds t o a stimulus
amplitude modul at i on of approximately 109 quanta(507 nm)
(deg 2 s)-' retinal illumination. The stimulus dept h of
modulation was 0.6. The background was a circular spot with
a di amet er of 8.5 deg. The retinal i l l umi nat i ons of t he
backgr ound are given in log td, but these are " cat t d " , and
1 " c a t t d " is equi val ent t o appr oxi mat el y 6. 105
quanta(507 nm) (deg 2 s)-' on t he retina. Thus t he lowest
backgr ound illumination used in these experiments was
approxi mat el y 3.6. los quant a(deg 2 s) -1 on t he retina. The
l umi nance required, t hr ough t he 4 mm di am artificial pupil
used, t o produce this lowest backgr ound i l l umi nat i on was
5.10-4 cd m 2. The brightest background was l 0 s brighter. This
was an on-center cell, presumabl y a Y-cell. Fr om Cleland
and Enrot h-Cugel l (1968).
wh e n i t i s d r i v e n b y r o d s o r d r i v e n b y c o n e s s u g g e s t
t h a t t h e t r a n s i t i o n f r o m r o d s t o c o n e s d o e s n o t
p r o d u c e t h e c e n t e r ' s c o n t r a c t i o n . R a t h e r , i t a p p e a r s
mo r e l i k e l y t h a t t h e c e n t e r s i ze i s r e l a t i v e l y c o n s t a n t
f r o m mi d - s c o t o p i c t o mi d - p h o t o p i c l e ve l s , a n d o n l y
b e c o me s l a r g e r i n t h e l o w s c o t o p i c r a n g e . T h i s
i n f e r e n c e s h o u l d b e t e s t e d f u r t h e r s i n c e i t ma y b e
306
100
10
I I I I 1 1 i I I I I I I I I 1111111
0 0 1 0+1 1
S p a t i a l f r e q u e n c y ( c / d e g )
o f r e t i na l a d a p t i v e s i gnal s has be e n i nf e r r e d f r o m
p s y c h o p h y s i c a l e x p e r i me n t s . F u r t h e r mo r e ,
que s t i ons a b o u t t he i nf l ue nc e o f b a c k g r o u n d l i ght
at one pl a c e i n t he vi s ual f i el d on t he r e s p o n s e t o
a t es t l i ght at a n o t h e r pl a c e ha ve be e n r a i s e d i n
t he or i e s o f vi s i on by ( a mo n g ot he r s ) He r i n g (1920),
He l s o n (1964), Spe r l i ng (1970), a n d Gr o s s b e r g
(1981). A we a l t h o f p h y s i o l o g i c a l r es ul t s s u p p o r t s
t he c o n c e p t o f a d a p t a t i o n a l p o o l i n g , b u t i ndi c a t e s
t h a t t he p o o l s a r e s ma l l e r t h a n mo s t t he or i s t s ha ve
i expect ed. Fu r t h e r mo r e , t her e is evi dence f or pool i ng
o f a d a p t i v e s i gnal s ove r t he e nt i r e c e nt e r o f t he
r e c e pt i ve f i el d, a n d al s o mo r e l oc a l i z e d a d a p t i v e
p o o l i n g i n s u b - r e g i o n s o f t he r e c e pt i ve f i el d c e nt e r
a n d s u r r o u n d . Ho we v e r , i n t he cat , s t e a d y
i l l u mi n a t i o n o f t he s u r r o u n d has l i t t l e or no ef f ect
on t he ga i n o f t he cent er .
I n t he cat r et i na, t he gai n o f t he cent er me c ha ni s m
o f t he r e c e pt i ve f i el d o f a r e t i na l g a n g l i o n cel l is
d e t e r mi n e d by t he s um o f al l t he s t e a d y l i ght f al l i ng
on t he cent er , a n d onl y on t he cent er . Thi s has been
p r o v e n by a n u mb e r o f di f f e r e nt e xpe r i me nt s whi ch
a r e c ons i s t e nt wi t h each ot he r . Th e f i r st was t he
e x p e r i me n t o f Cl e l a n d a n d En r o t h - Cu g e l l (1968),
t he r es ul t s o f whi c h a r e s h o wn i n Fi g. 32. I n t hi s
e x p e r i me n t , t he signal summat i on area was
me a s u r e d wi t h s t i mul us di s ks o f v a r i o u s a r e a s .
I l l u mi n a t i o n was a d j u s t e d t o gi ve a c o n s t a n t
cr i t er i on r es pons e. Ri c c o ' s La w hel d a p p r o x i ma t e l y
f or di s k a r e a s l ess t h a n t he s i gnal s u mma t i o n a r e a ,
i . e . I . A- - k R s , whe r e kRs is t he c o n s t a n t f or Ri c c o
s i gnal s u mma t i o n . F o r a r e a s l a r ge r t h a n t he s i gnal
s u mma t i o n a r e a , Ri c c o ' s La w no l o n g e r hel d a n d
a c o n s t a n t i l l u mi n a t i o n was r e q u i r e d t o el i ci t a
cr i t er i on r es pons e. The a r e a over whi ch Ri c c o' s La w
hel d was e q u a t e d wi t h t he c e n t e r ' s a r e a o f s i gnal
s u mma t i o n . F o r t he s a me cel l t he adaptive
summat i on area was d e t e r mi n e d , a g a i n wi t h a
c o n s t a n t r e s p o n s e c r i t e r i on. I n t hi s case, a r e a a n d
i l l u mi n a t i o n o f a n a d a p t i n g di s k wer e v a r i e d
r e c i p r o c a l l y i n o r d e r t h a t t he g a n g l i o n cel l wo u l d
p r o d u c e a c o n s t a n t r e s pons e t o t he t est s pot . The
t est s pot was c o n s t a n t i n a r e a a n d i l l u mi n a t i o n ; it
was p l a c e d i n t he cent er o f t he r e c e pt i ve f i el d.
Ad a p t i v e s u mma t i o n f ol l owe d Ri c c o ' s La w al so f or
di s ks wi t h a r e a s l ess t h a n t he a d a p t i v e s u mma t i o n
ar ea. Tha t is, f or a d a p t a t i o n , I . A = kRA, wher e kRA
is t he c o n s t a n t f or Ri c c o a d a p t i v e s u mma t i o n . Fo r
l a r ge r di s ks , s u mma t i o n o f a d a p t i v e s e ns i t i vi t y
FIG. 31. The effect of mean luminance on the dependence
of a ganglion cell's contrast gain on spatial frequency. Four
mean luminance levels were used: 16 (empty circles), 0.5 (f'dled
triangles), 1.6" 10 -2 (filled circles), and 5" 10 -4 cd m -2 (empty
triangles). The highest mean luminance corresponds to
approximately 108 quanta(507 nm) (deg 2 s) -1 retinal
illumination. What we have called "contrast gain" is labeled
"contrast sensitivity" in the figure. A 3.5 mm diameter
artificial pupil was used. The criterion response was audible
impulse rate modulation at the drift rate of the grating, 4 Hz.
The data were fit with smooth curves calculated from a
Difference of Gaussians model, where the smaller Gaussian
represents the receptive field center. The estimated diameter
of the center changed by about a factor of two over the range
of mean luminances studied. The cell studied here was an
on-center X cell. From Enroth-Cugell and Robson (1966).
a wa y t o f or ge a s t r o n g e r l i nk b e t we e n t he
mi c r o c i r c u i t r y o f t he r e t i na a n d i t s f unc t i on. I n a n y
case, t he d a t a on t he r e l a t i ve l y s ma l l c ha nge s o f
r e c e pt i ve f i el d c e nt e r si ze wi t h b a c k g r o u n d or me a n
l evel ser ve t o r e i n f o r c e even mo r e s t r o n g l y t he
c o n c l u s i o n t h a t s i gnal s f r o m d i f f e r e n t pa r t s o f t he
r e c e pt i ve f i el d c e nt e r a d a p t t o g e t h e r a n d wi t h
a p p r o x i ma t e l y t he s a me s l ope o n t he ga i n vs
b a c k g r o u n d cur ve.
3. 5. Adaptati onal Pool i ng and Receptive Field Size
3.5.1. SIGNAL POOLS AND ADAPTATION POOLS
I n v e s t i g a t i o n o f t he s p a t i a l s u mma t i o n o f
d e s e n s i t i z a t i o n by a d a p t i n g l i ght s is i mp o r t a n t f or
an u n d e r s t a n d i n g o f t he f unc t i ons a n d me c h a n i s ms
o f l i ght a d a p t a t i o n . As we di s c us s e d i n Se c t i ons
1. 2. 1. a n d 2. 1. 6. i n c o n n e c t i o n wi t h t he i de a s o f
Wh i t t l e a n d Ch a l l a n d s , L a n d a n d Mc Ca n n ,
Ru s h t o n , a n d We s t h e i me r , t he s p a t i a l s u mma t i o n
307
3 i f i ' : f b r j
0.1 0 2 0 3 0 5 0.7 I 2 3 0 0 I 0 2 03 0 5 0 7 I 2 3
Di a me t e r o f a d a p t i n g s p o t , d e g r e e s
St i muLus d i a me t e r , degrees
F[6. 32. Compar i son of adaptive (a) and signal (b) summat i on areas of an on-center cat ganglion cell.
(a) The hori zont al axis gives t he log of t he di amet er of unmodul at ed adapting spots. The vertical axis gives t he log of
t he reciprocal of t he adapt i ng spot i l l umi nat i on in relative units. The adapt i ng i l l umi nat i on was set so t hat t he cell produced
a criterion response t o a small (0.13 deg) centrally located spot of fixed luminance, which was sinusoidally modulated (4 Hz,
0.6 contrast).
(b) The horizontal axis gives the log of the diameter of the stimulus, which was again a spot modulated at 4 Hz, sinusoidally,
at 0.6 contrast. But in this experiment the stimulus diameter was varied. The vertical axis in (10) gives the log of the relative
gain for the spots of different size; it is also the log of the reciprocal of the illumination required to elicit a constant response.
In 0a), the spots were presented on a steady background of 6.10 ~ quanta(deg a s)-'. The criterion response in both (a) and
(b) was just audible synchronization of the cell's discharge with the stimulus modulation. From Cleland and Enroth-Cugell
(1968).
st opped. The i mpor t a nt resul t of this exper i ment
is t hat t he signal s umma t i on ar ea and t he adapt i ve
s umma t i on ar ea were t he same. Pr oba bl y mos t i f
not all of t hese exper i ment s were on Y ret i nal
gangl i on cells, but l at er wor k i ndi cat es si mi l ar
results hol d f or X cells ( Har di ng, 1977). The results
are t he s ame f or on- and off-cel l s. Very si mi l ar
resul t s have been obt ai ned wi t h t hi s exper i ment al
design on rat opt i c t ract fibers by Green et al. (1977)
and Tong and Gr een (1977). Resul t s of this ki nd
have also been obt ai ned in l ower vert ebrat es: in frog
gangl i on cells (Reut er, 1969; Bur khar dt and
Ber nt son, 1972), and in gol dfi sh gangl i on cells
(Schel l art and Spekrei j se, 1972).
Rel at ed exper i ment s by Shapl ey et al. (1972) and
by Enrot h-Cugel l and Shapl ey (1973b) indicate t hat ,
as t he ar ea of an adapt i ng spot of f i xed l umi nance
is i ncreased, t he gai n declines. Thi s is i l l ust rat ed in
Fig. 33. The (fixed) l umi nance of t he adapt i ng spot
was chosen so t hat f or t he smal l est adapt i ng spot
the gai n had not been reduced f r om its dar k adapt ed
ma xi mum. As t he ar ea of t he adapt i ng spot was
i ncreased, gai n declined and t he response t o t he test
st i mul us became mor e t r ansi ent . Resul t s si mi l ar t o
t hese were obt ai ned by Schel l art and Spekrei j se
(1972) in t he gol df i sh ret i na. They f ound t hat t he
t empor al i mpul se r esponse was speeded up and
made mor e di phasi c by i ncreasi ng t he ar ea of a
backgr ound spot of const ant l umi nance.
Anot he r exper i ment whi ch demons t r at es t he
si gni fi cance of t he ar ea as well as t he l umi nance of
t he backgr ound is i l l ust rat ed in Fig. 34. The fi gure
shows t he act ual responses of a gangl i on cell t o
t ur ni ng on adapting spot s of qui t e di f f er ent ar ea
and l umi nances. The l umi nance of t he l arger one
had been adj ust ed unt i l it pr oduced t he same gai n
r educt i on as t he smal l er adapt i ng spot , as i ndi cat ed
by the response t o t he super i mposed br i ef test flash.
Equal adapt i ve effect is associ at ed wi t h equal
responses of t he gangl i on cell t o t he " a d a p t i n g "
spot s. The concl usi on f r om all t hese exper i ment s
is t hat t he gai n of t he gangl i on cell cent er
mechani s m is set by t he sum of all t he st eady st at e
i nput t o t he cent er. Thi s in t ur n i mpl i es t hat t he
adapt i ve effect of a backgr ound on t he cent er
mechani s m of a gangl i on cell is, under t he
condi t i ons of these experi ment s, det er mi ned by t he
total effective f l ux: t he sum of all t he light per uni t
t i me which falls on t he center f r om t he backgr ound,
wei ght ed by t he spat i al "sensi t i vi t y pr of i l e "
(Cl el and and Enr ot h- Cugel l , 1968; Enr ot h- Cugel l
and Shapl ey, 1973b).
The meani ng of these results in a psychophysi cal
cont ext is t hat t he s umma t i on pool of a gangl i on
cell is t he same size as t he adapt at i on pool . The
meani ng in a neur oanat omi cal cont ext is t hat
what ever i nt er neur on det er mi nes t he size of t he
recept i ve field cent er is al so i mpl i cat ed in t he gai n
cont r ol process.
I n t he light o f t hese results on t he dependence of
308 R, M. SHAPLEY AND C. ENROTH- CUGELL
Area a d a p t a t i o n f~eLd Gain
{ i mpul se/ quant um)
(a) ~ i ' ~ 014 degrees 2
_ _ @ o2
{b) 0
O05
I 5 0 imp s p
FIG. 33. Re duc t i on in gai n wi t h i ncr ease i n ar ea o f a n a da pt i ng s pot of c ons t a nt r et i nal i l l umi nat i on. Thr ee aver aged
r es pons es were el i ci t ed by a smal l (0. 18 deg) cent r al l y l ocat ed s pot ( a, b, c) . I n each r un, t he a r e a o f a n a da pt i ng di sk o f
c ons t a nt r et i nal i l l u mi n a t i o n - - 6 - 10 a quant a( 507 nm) (deg ~ s) -1 was var i ed; t he ar ea in deg 2 is gi ven in t he f i gur e. Ga i n was
cal cul at ed by di vi di ng r es pons e in i mpul s es s " by t he r et i nal s t i mul us f l ux in q u a n t a s- ' . Thi s exper i ment was done on a n
on- cent er cat gangl i on cell, pr oba bl y a Y cell. Fr o m Shapl ey et a/ . (1972).
i m p u l s e s / s e c
0
impuh;es/sec ~ - Dt ~-
I
!
0
impulses/see
I
50 i m p u l s e s / s e e
FIG. 34. Ga i n r educt i on wi t h t wo a da pt i ng s pot s of di f f er ent ar ea but t he s a me effect i ve f l ux. The t est s t i mul us was a 50 ms
pul s e o f l i ght , 0.1 deg i n di amet er , 2. 107 qua nt a ( de g 2 s) -t r et i nal i l l umi nat i on.
(a) Th e condi t i oni ng s t i mul us ( hat ched) was 0.1 deg s pot s upe r i mpos e d on t he t est s pot , modul a t e d i n a s quar e wave
ma n n e r at 0. 4 Hz. Th e i l l umi nat i on i n t he l i ght pha s e was 3" 107 qua nt a ( de g 2 s) -t .
(b) The condi t i oni ng s t i mul us was a 1.57 deg di amet er di sk, concent r i c wi t h t he t est s pot . It s i l l umi nat i on was 2. 5" 104
qua nt a ( de g 2 s) -1, a n d al so 0. 4 Hz.
(c) Tes t s pot was pr es ent ed wi t hout a ny condi t i oni ng s t i mul us . The t wo condi t i oni ng st i mul i mu s t have ha d t he s a me
ef f ect i ve f l ux, by def i ni t i on, becaus e t he y pr oduc e d i dent i cal r es pons es . Thes e r esul t s ar e f r o m a n on- cent er gangl i on cell,
pr e s uma bl y a Y cell. Fr o m Enr ot h- Cuge l l a n d Shapl ey (1973b).
gai n cont r ol on t he pr oduct of i l l umi nat i on and
area, we must revise equat i ons (20) and (21) whi ch
expressed t he gai n in t erms of i l l umi nat i on. The
earlier equat i ons were cor r ect under t he condi t i ons
of full field i l l umi nat i on when t he ent i re recept i ve
field woul d be covered by t he uni f or m backgr ound.
In this case t he gain woul d j ust be scaled down by
a f act or equal t o t he area of t he cent er of t he
recept i ve field. But a mor e general equat i on can be
written which applies t o backgr ounds of any spatial
conf i gur at i on. For t he r od pat hway:
GR = GR0/(1 + FB/ FRo) p (24)
and a similar equat i on describes the gain of the cone
pat hway, Go Fl ux is i l l umi nat i on mul t i pl i ed by
area, in this case t he t ot al summi ng area of t he
cent er of the recept i ve field. For step responses, t he
exponent P has t he val ue 0.9 f or t he r od pat hway
and is somewhat higher f or the cone pat hway. What
equat i on (24) means is t hat t he gain depends on
backgr ound fl ux, F B, not retinal i l l umi nat i on, flux
added up over t he entire cent er of t he receptive field
and wei ght ed by t he di st ri but i on of sensitivity of
t he recept i ve field cent er. Al so, t he adapt i ng flux
has t o exceed a critical value, denot ed FRO f or t he
scot opi c system, in or der f or t he cell t o under go t he
transition f r om dark adapt at i on t o light adapt at i on.
It may help t o concei ve of this critical fl ux as t he
backgr ound flux requi red t o pr oduce a critical level
of D. C. neural signal which, when exceeded, t urns
on t he retinal gai n cont r ol . The val ue of t he critical
fl ux, FRO, is about 104 quant a s -1 at t he r et i na on
t he average ( Enr ot h- Cugel l and Shapl ey, 1973b).
3.5.2. LOCAL AND GLOBAL GAIN CONTROLS WHICH
DEPEND ON FLUX
Fur t her investigation of t he spatial summat i on of
adapt i on in cat gangl i on cells was per f or med by
Har di ng (1977). One of his maj or results is
illustrated in Fig. 35. The experi ment was designed
t o measure t he spatial weighting of adapt at i on with
a t wo- spot par adi gm: one test and one adapt i ng
spot . The test spot was fixed in posi t i on in t he
mi ddl e of t he recept i ve field. Then t he posi t i on of
t he adapt i ng spot was vari ed and its l umi nance
adj ust ed so t hat t he gain of t he response t o t he test
was reduced by a criterion amount . In the same cells
t he sensitivity pr of i l e f or eliciting a response was
also measured. This latter profi l e is called the signal
sensitivity profi l e. As can be seen f r om t he results
in Fig. 35, t he signal sensitivity pr of i l e and t he
adapt at i on profi l e were appr oxi mat el y t he same in
X cells. In some Y cells t he gain r educt i on f or a test
spot near t he adapt i ng spot was great er t han f or a
test spot f ar t her f r om t he adapt i ng spot , by mor e
t han woul d be predi ct ed f r om t he Y cell' s signal
sensitivity profi l e. That is, t her e were i ndi cat i ons
of local adapt at i on in t he Y cell cent er. A similar
sort of ef f ect was seen in an i nvest i gat i on of light
adapt at i on of t he receptive field sur r ound of Y cells
(Cleland et al . , 1973). There is thus evidence for t wo
di fferent gain controls in the Y cell center: one local,
one mor e global. Ther e is also evi dence f or local
adapt at i on in some X cells ( Har di ng, 1978). A
discussion of t he i mpl i cat i ons of these experi ment s
f or X/ Y recept i ve field or gani zat i on woul d car r y
us t oo far f r om t he cent ral issues of this paper. But
a br i ef comment about these di f f er ent adapt at i on
profiles in X and Y cells may pr ovoke some t hought
a bout t he r et i nal mi c r oc i r c ui t r y under l yi ng
adapt at i on.
It is known t hat at any ret i nal locus t he receptive
field cent ers of X cells are about t en times smaller
in area t han t hose of Y cells ( Hochst ei n and
Shapl ey, 1976b; Cl el and e t al . , 1979; So and
Shapley, 1979; Linsenmeier e t al . , 1982). There exist
subuni t s of t he Y cell' s recept i ve field which are
r oughl y t he same size as X cell cent ers at t he same
retinal eccentricity (Hochst ei n and Shapl ey, 1976b;
So and Shapl ey, 1979; cf. Appendi x 2). It has been
suggested t hat X cell centers and Y cell subunits are
appr oxi mat el y det er mi ned by t he spatial summi ng
areas of bi pol ar cells ( Hochst ei n and Shapl ey,
1976b; Vi ct or and Shapl ey, 1979). While recent
neuroanat omi cal investigation of the retina suggests
this is only an approxi mat i on to the actual situation,
it seems now t o be an appr oxi mat i on r at her t han
mere specul at i on (see Sterling, 1983). Thus, i f one
accepts our previ ous assert i on t hat t he i nt er neur on
which determines t he size of the X cell' s center must
set t he gain of t he center, t hen t he bi pol ar cells must
cont r ol t he gai n of t he X cent er, in some way. I f
these same bi pol ar cells feed i nt o t he Y cells'
subuni t s, one must suppose t hey cont r ol t he gain
of t he subuni t s. The local effect s of gain r educt i on
in Y cells seen in Fig. 35 coul d be expl ai ned by this
" b i p o l a r " gain cont r ol , whi ch we i nfer t o be
X-cells Y-cells Y-cells
, o x I
2 9 2 : ; "
1 9 / 2 }
d '~
18/1 ~/ ~ ,
_3' ' 0
2O/
2 3 /
2 4 / 4 "/
3 1 / 6
- 3 ' 6 ' 3
d i s t a n c e on r e t i n a (deg.)
j d , ~ . 2 3 / 4
' ~ 31/3
5'
:~) 29/5
v,
, ~ 3 2 / 3
0
- 3 0 3
FIG. 35. Adaptive and signal gain profiles from four X and eight Y cells. The stimulus used to obtain each profile was
a spot 0.2 deg in diameter, modulated by a 2 Hz squarewave. The response criterion was 3 extra impulses over 100 ms
at the beginning of each response. Signal gain: the circles indicate the relative gain at each position with respect to the
peak gain at position zero, the middle of the receptive field center. The vertical scale is logarithmic and a vertical calibration
for 10x is given in the figure. Adaptive effectiveness: The horizontal position of the triangles indicates the location within
the receptive field center of a steady adapting spot of 0.2 deg diameter. The modulated test stimulus was fixed in the middle
of the receptive field center. The test stimulus was set to be 3x brighter than required to reach criterion. Then the luminance
of the adapting spot was adjusted to reduce the response to the criterion level, at each position of the adapting spot. The
log, of the ratio of the adapting luminance at position zero divided by the adapting luminance at each of the other positions
tested, is given by the vertical position of the triangles. Signal and adaptive profiles have been superimposed at position
zero to allow comparison of their respective spread. From Harding (1977).
c o mmo n t o X cel l cent er s a nd Y cel l s ubuni t s . The r e
mu s t al s o be a s e c o n d ga i n c o n t r o l f or t he mu c h
l a r ge r Y cel l cent er ; a l i ke l y c a n d i d a t e is one o f t he
l a r ge f i el d a ma c r i n e cel l s whi c h s h o u l d ha ve a
d e n d r i t i c s p r e a d r o u g h l y t e n t i me s l a r ge r i n a r e a
t h a n t he d e n d r i t i c s p r e a d o f an X g a n g l i o n cel l .
Loc a l a d a p t a t i o n ef f ect s l i ke t hos e i n Fi g. 35 have
been seen p r e v i o u s l y i n g a n g l i o n cel l s f r o m o t h e r
speci es: r a t ( Gr e e n et al . , 1977; To n g a n d Gr e e n ,
1977), f r o g ( Bu r k h a r d t a n d Be r n t s o n , 1972),
gol df i s h ( Eas t er , 1968). The f unc t i ona l a na l ogi e s o f
t hes e cel l s wi t h cat X or Y cel l s is obs c ur e , b u t i n
e ve r y cas e t he cel l s s t u d i e d b a d r e l a t i ve l y l a r ge
r e c e pt i ve f i el ds c o mp a r e d t o t he si ze o f d e n d r i t i c
s p r e a d s o f b i p o l a r cel l s. Mo r e o v e r , e vi de nc e f or a
s e c o n d ga i n c o n t r o l wi t h a l ar ge s u mmi n g a r e a
c o mp a r a b l e t o t he cent er size has been f o u n d i n each
o f t he s e r e t i na s : i n r a t ( Gr e e n et al . , 1977), i n f r og
( Re ut e r , 1969; Bu r k h a r d t a n d Be r nt s on, 1972), a nd
i n g o l d f i s h ( Sc he l l a r t a n d Spe kr e i j s e , 1972). Thus ,
l ocal a d a p t a t i o n ef f ect s i n each o f t hese cases mi ght
be due t o l oc a l i z e d " b i p o l a r " ga i n c o n t r o l s whi c h
a r e p r e s e n t i n a d d i t i o n t o a s e c ond, " a ma c r i n e " ,
ga i n c o n t r o l whi c h s ums l i ght e v o k e d ne ur a l s i gnal s
ove r a l a r ge r a r e a . Thi s s h o u l d be c l e a r l y l a be l l e d
as a c ha i n o f i nf e r e nc e r a t he r t h a n e s t a bl i s he d f act .
Yet i t is i nt er es t i ng be c a us e i t ser ves t o r e i nf or c e t he
i de a t ha t t he r e is a h i e r a r c h y o f ga i n c o n t r o l s , a
" b i p o l a r " ga i n c o n t r o l a n d an " a ma c r i n e " ga i n
c ont r ol as wel l as p h o t o r e c e p t o r gai n c ont r ol s whi ch
wi l l be di s c us s e d be l ow.
3.5.3. OPTICAL AND NEURAL FACTORS IN
ADAPTATIONAL POOLING
One mus t c ons i de r t he p r o p o s i t i o n t ha t al l r et i nal
ga i n c o n t r o l by l i ght is a p u r e l y l oc a l , r e c e p t o r a l
p h e n o me n o n . I t ma y s eem an a b s u r d p r o p o s i t i o n
i n t he f ace o f al l t he e vi de nc e ci t ed a b o v e a b o u t t he
a d a p t i v e s u mmi n g a r e a be i ng e qua l i n si ze t o t he
r e c e pt i ve f i el d c e nt e r , b u t i t de s e r ve s s e r i ous
consi der at i on because of t he pr obl em of light
scat t eri ng wi t hi n t he eye and of opt i cal aber r at i ons
in t he lens and cor nea. I f t he measur ed size of t he
recept i ve field cent er and adapt i ve summi ng area
were great l y i nfl uenced by such i mperfect i ons in
physiological optics, one woul d have to discount the
concl usi ons about t he site or sites of gain cont rol (s)
whi ch were based on t he cor r el at i on of t he spat i al
ext ent s of t hese t wo di f f er ent mechani sms.
However , direct measurement s of t he physiological
optics of t he cat ' s eye (Bonds, 1974; Robs on and
Enr ot h- Cugel l , 1978) i ndi cat e t hat , except f or rare
cells with t he smallest recept i ve fields, t he opt i cal
effect on the measured size of the receptive field and
adapt i ve summi ng area is small. It is i nt erest i ng t o
not e t ha t t he exi s t ence o f t he pos t ul a t e d
" amacr i ne" gain cont rol of t he Y cells is not subject
t o any doubt s based on opt i cal bl ur or scat t er,
because t he adapt i ve summi ng ar ea and recept i ve
field cent er of Y cells are so large. The presence of
nei ghbor i ng X cells with fields t en t i mes smal l er in
ar ea serves as a cont r ol on t he opt i cal cont r i but i on
t o t he size of t he Y cells' fields. However , t here
coul d be some quest i on about whet her t he size of
t he recept i ve fields of X cells, whi ch can be qui t e
small in area, might be due t o optical blur or scatter.
It becomes a quant i t at i ve quest i on in t he case of t he
X cells. However , even f or X cells, t he opt i cal bl ur
seems t o be less t han t he neural summat i on ar ea
( Robson and Enr ot h- Cugel l , 1978) when t he
physi ol ogi cal opt i cs are opt i mi zed wi t h best
r ef r act i on and a small artificial pupil. Thr oughout
this paper , ar gument s based on recept i ve fields'
sizes have onl y cited as evi dence t he results of
experi ment s in whi ch t he physi ol ogi cal optics were
opt i mi zed.
That some of t he ret i nal gai n - - setting
mechani sms must i nvol ve pool i ng of signals f r om
many recept ors is t he concl usi on of a physiological
ext ensi on of Rus ht on' s reasoni ng about t he low
l evel of b a c k g r o u n d s whi ch pr oduc e l i ght
adapt at i on (Enrot h-Cugel l and Shapley, 1973a). As
di s cus s ed a bove , Ru s h t o n f o u n d t ha t t he
psychophysi cal scot opi c t hr eshol d was raised by a
fact or of t wo f r om its dark adapt ed value when onl y
one r od in a hundr ed act ual l y caught a quant um
of light. However , as st at ed bef or e, this result
implies not hi ng about gai n cont r ol in t he ret i na. It
coul d be expl ai ned in t erms of an i ncrease in
PRR3-I
" noi s e " f r om t he backgr ound. Appl yi ng Rusht on' s
reasoni ng t o ret i nal gain, we measur ed how much
backgr ound light is requi red t o r educe t he gain of
a gangl i on cell by a f act or of t wo. In several cells
with large receptive fields, t he requi red backgr ound
light yields one quant um absor bed per second per
hundr ed rods. The i nt egrat i on t i me of feline r ods
is al most cert ai nl y shor t er t han a second; i ndeed,
ot her wor k indicates a maxi mum i nt egr at i on t i me
of 0.1 s. Thus, one r od in a t housand per
integration time receiving a quant um of background
light is enough t o reduce t he gain by hal f a log unit.
Thi s is solid suppor t f or Rusht on' s concl usi on t hat
signals f r om a pool of rods must set t he gain f or
signals f r om rods which have not themselves
received light quant a f r om t he backgr ound.
In ceils with smal l er recept i ve fields, t he
l umi nance requi red t o reduce gai n was hi gher, so
t hat in t he worst case appr oxi mat el y one r od in t en
received a quant um of light per i nt egr at i on time.
We now presume t hat these ganglion cells with small
fields were X cells, on t he basis of t he receptive field
cent er size. So agai n t he ver y l ow level of
backgr ound l umi nance whi ch is requi red t o reduce
t he gain may suggest t hat phot or ecept or signals
must be pool ed to set the gain in the cat retina. Not e
t ha t l i ght s c a t t e r woul d not a f f e c t t hes e
measur ement s because t hey were made wi t h large
uni f or m backgr ounds whi ch were at least one
t housand times larger in area t han t he opt i cal poi nt
spread f unct i on at hal f hei ght . Fur t her mor e, t he
f or ce of these ar gument s is not af f ect ed by t he fact
t hat not all phot or ecept or s which lie within t he
spread of t he dendritic tree of a ganglion cell proj ect
t o t hat gangl i on cell. The statistical r andomness of
t he quant um cat ch makes t he f r act i on of recept ors
hit by quant a t he same whet her one consi ders t he
ent i re popul at i on of phot or ecept or s, or onl y t hat
popul at i on which projects t o the ganglion cell under
st udy, as l ong as t he backgr ound is t rul y uni f or m.
That t here are di f f er ent t r ansi t i on levels, f r om
dar k t o light adapt ed, f or scot opi c recept i ve field
cent er and sur r ound mechani sms (Fig. 26) also
suppor t s t he idea of a gain cont r ol pr oxi mal t o t he
phot orecept ors. The same rods must drive the center
and sur r ound. I f onl y t he rods adapt ed, t he cent er
and sur r ound woul d have t o lose t hei r gain in
parallel. Since this is not observed, we must
concl ude t hat gain must be cont r ol l ed at a site in
312
t he ret i na af t er cent er and s ur r ound have been
segregated. The neur oanat omy of the cat retina tells
us t hat all post - r ecept or al i nt er neur ons pool t he
act i vi t y of ma ny phot or ecept or s. Ther ef or e, t he
p o s t - r e c e p t o r a l ga i n c o n t r o l mu s t p o o l
phot or ecept or signals.
R. M. S H A P L E Y A N D C . E N R O T H - C U G E L L
3.6. Gain Control and Receptive Field Size Across
the Popul ati on of Gangl i on Cells
Since l i g h t - e v o k e d neural signals are s ummed
over t he recept i ve field cent er t o set t he gai n of the
cent er of a par t i cul ar gangl i on cell, one nat ur al l y
woul d guess t hat gangl i on cells wi t h cent ers of
di f f er ent sizes woul d be light adapt ed t o di f f er ent
extents by a large uni f or m backgr ound. The results
on the spatial s ummat i on of adapt i ve effect suggest
t hat gai n depends on the total, st eady state, effective
flux, i.e. i l l umi nat i on mul t i pl i ed by ar ea wei ght ed
by the cent er' s gain per unit area. The t ot al effective
fl ux falling on the cent er of a cell wi t h a small
recept i ve field will be less t han t he flux falling on
a l arge recept i ve field center; t he gai n shoul d be
reduced less in t he smal l recept i ve field cent er.
The initial test of this i dea is of f er ed in Fig. 36,
f r om Enr ot h- Cugel l and Shapl ey (1973b). What is
pl ot t ed in Fig. 36 is t he t r ansi t i on i l l umi nat i on at
the knee of t he curve rel at i ng gai n and backgr ound
i l l umi nat i on. The t ransi t i on i l l umi nat i on is defi ned
here empi r i cal l y as t he i l l umi nat i on at which t he
gai n has dr opped by a f act or of t wo f r om t he dar k
adapt ed gain (Not e the slight di fference between this
def i ni t i on and t he mor e r i gor ous defi ni t i on of
t ransi t i on i l l umi nat i on in connect i on with equat i on
(20)). Because t he dat a in Fig. 36 were col l ect ed
f r om ma ny di f f er ent cats, possi bl y in di f f er ent
physi ol ogi cal states, the t ransi t i on i l l umi nat i on was
mul t i pl i ed by t he dar k adapt ed gai n t o obt ai n a
cor r ect ed t r ansi t i on i l l umi nat i on. Thi s cor r ect ed
t r ansi t i on i l l umi nat i on is pl ot t ed agai nst cent er
summi ng area, det ermi ned f r om an area - t hreshol d
curve (Cl el and and Enr ot h- Cugel l , 1968). I t can be
seen in Fig. 36 t hat the cells with l arger centers have
a l ower effect i ve t r ansi t i on level, and t hat t he
t ransi t i on level is appr oxi mat el y pr opor t i onal to t he
cent er s ummi ng ar ea. These dat a mi ght be
compat i bl e wi t h ot her f unct i ons of cent er size
besides area, because of the large vari ance. The cells
U
E
c
E
c
c
o
c
10
10 ~
1 0 2
] l I I I I I
o U ~ o o O o o o o o
o o o
o ~ o o
o ~o
o
o
I I I I 1 1 I
025 05 10 25 50 10 25
Total summing area of centr resp mech (deg ~)
FIG. 36. Transition level as a function of center area for a
population of cat retinal ganglion cells. The value of the
transition level from the horizontal to the sloping portions
of the gain vs background illumination curves (as in Fig. 24)
is plotted against center summing area. Empty circles are from
on-center cells, while filled circles are from off-center cells.
The cells were not grouped into X and Y classes. From
Enroth-Cugell and Shapley (1973b).
in this st udy were not classified as X or Y.
Ther ef or e, a quest i on unr esol ved by these results
is whet her X and Y cells have t he same dependence
of effect i ve t r ansi t i on level on cent er area.
Fur t her evi dence on t he dependence of gai n
setting on recept i ve field cent er size across t he pop-
ul at i on of gangl i on cells comes f r om t he concor dant
studies of Fi scher and Ma y (1970) and Cl el and et
al. (1973). The results of bot h studies i mpl i ed t hat
t he cent er ' s gai n, def i ned as G = d R / d F where F
is l umi nous fl ux (i l l umi nat i on t i mes area), is
inversely pr opor t i onal t o t he cent er' s summi ng area
when t he gangl i on cell is well light adapt ed in t he
mi d- scot opi c t o mesopi c r ange by large uni f or m
backgr ounds . Thi s is consi st ent wi t h t he result of
Enr ot h- Cugel l and Shapl ey (1973b) on t he " ef f ec-
t i ve t r ansi t i on l evel " and wi t h t he appr oxi mat el y
i nverse r el at i onshi p bet ween gai n and backgr ound
above the t ransi t i on level, equat i on (21). Thus, three
studies seem consistent in suppor t i ng t he hypot hesi s
t hat gangl i on cells with larger centers are mor e light-
adapt ed t han t hose wi t h smal l er cent ers under t he
same fixed uni f or m backgr ound conditions, because
of spat i al s umma t i on of adapt i ng signals.
RETINAL GAIN CONTROLS 313 VISUAL ADAPTATION AND
Recently, Linsenmeier et al . (1982) have taken a
fresh look at this question by measuring the gain
of X and Y ganglion cells in the cat in response to
drifting gratings on high scotopic or mesopic
backgrounds. They also gauged the size of the
center of each ganglion cell by fitting the observed
dependence of contrast gain on spatial frequency
with a "Di fference of Gaussi ans" model. The
spatial sensitivity profiles of receptive field center
and surround are approximated by Gaussian
functions in this model. The spatial spread of the
center' s Gaussian is a measure of the effective
radius of the center' s distribution of sensitivity (or,
more precisely, gain). Figure 37 is their graph of
the peak gain of the center plotted vs the center' s
effective radius, for a large population of cat retinal
ganglion cells. The figure demonstrates that the cells
with the largest centers had the lowest peak gain,
and that the gain was approximately the inverse of
the center' s r adi us . While this result is qualitatively
like the earlier results of Enroth-Cugell and
Shapley, Fischer and May, and Cleland et al . , it is
quantitatively different in that gain in the light
adapted state is inverse to the radius and not the
area of the center. However, there is quite a lot of
variance of gain across the population of ganglion
cells, so much so that Linsenmeier et al . ' s results
do not conclusively disprove the a r e a - ga i n
relation. Furthermore, since their measurements
were made at backgrounds which might be in the
high scotopic or in the mesopic range, the precise
value of the slope of the gain vs area line might be
influenced by the degree to which rods or cones are
the predomi nant phot orecept or input for cells of
different sizes. These qualifying remarks suggest
that the book is not closed on the dependence of
gain on area of the receptive field center. As
suggested below, the hypothesis of Enroth-Cugell
and Shapley (1973b), that gain varies inversely with
center ar ea in the light-adapted state, is useful in
rat i onal i zi ng psychophysi cal results on the
dependence of sensitivity vs background curves on
target size.
The interpretation of these area effects in
adapt at i on must be modified by the discovery that
there is not a wide variation in receptive field center
size among ganglion cells of one type, X or Y, at
a given retinal locus (Cleland et al . , 1979; So and
Shapley, 1979). The coefficient of variation of the
1 0 0 0
~ - O
7 o
-~ 3 0 0 o O ~ , , ' ,
Z~ A Z ~

I n 1 0 0 ~ ~,,v~
f...
o 30
2~
0 ix
a. 1 0 z~
O, 0 , 3 1 3
C e n T e r - r - e d i u s ( d e g )
FiG. 37. Relation between t he center's size and its peak gain
in the middle of the receptive field. The dependence of
(Rayleigh) contrast gain on spatial frequency was determined
for X and Y cells by adjustment of contrast to reach a
constant response criterion. The experimental curves were
fit with a Difference of Gaussians model as in Fig. 31, from
which both the center's radius and its gain at the peak of
its sensitivity profile could be determined. These two values
are plotted against each other to show that, at the same mean
luminance, cells with larger centers have lower gain. The
empty symbols are for on-center cells, the filled symbols are
for off-center cells. Circles denote X cells; triangles denote
Y cells. The pupillary area was 16 mmL The mean luminance
was around 14 cd m-L From Linsenmeier et al. (1982).
center-diameter distribution at any one retinal locus
is at most 0.25 (So and Shapley, 1979) and is
probabl y less in an individual animal. There is a
marked increase in receptive field center-diameter
at retinal loci away from the ar ea cent r al i s ; the
di amet er of t he cent er is appr oxi mat el y
proport i onal to the distance from ar ea cent r al i s .
This is true for both X and Y cells, and for bot h
on- and off-center cells. On- and off-cells have
approximately the same size at any one locus on the
retina. As stated above, Y cells have an
approximately ten times larger area than X cells at
each locus. The combination of these facts with the
preceding results on the effects of area on
adaptation leads to the following conclusions. First,
cells with larger receptive fields in the periphery of
the retina ought to be more light-adapted than
central ganglion cells with smaller centers, under
condi t i ons of uni form const ant backgr ound
illumination. Second, Y ganglion cells ought to be
more light-adapted than X ganglion cells at the same
retinal locus. By the degree of light-adaptation we
mean the degree to which gain has been reduced
314
r el at i ve t o i t s d a r k - a d a p t e d val ue. Thes e concl us i ons
have t o be q u a l i f i e d t o i nc l ude t he p r o v i s o t ha t t he
b a c k g r o u n d c o n d i t i o n s ha ve t o be s uch t ha t al l t he
g a n g l i o n cel l s a r e d r i v e n b y t he r o d p a t h wa y . At
pr e s e nt t he r e a r e no f i r m d a t a a b o u t t he ef f ect o f
t he si ze o f cent er s o n t he de gr e e o f a d a p t a t i o n o f
t he g a n g l i o n cel l p o p u l a t i o n i n t he p h o t o p i c r a nge .
R. M. S H A P L E Y A N D C . E N R O T H - C U G E L L
3. 7. The Effect of the Receptive Field Surround on
the Gai n of the Center
1 0 '
1 0 5
o
1 0 ~
1 0 4
( a )
The s u r r o u n d o f t he r e c e pt i ve f i el d pl a ys no r ol e,
or at mos t a mi n o r r ol e , i n s et t i ng t he ga i n o f t he
cent er . Thi s is t he c o n c l u s i o n whi c h is i mpl i c i t i n
t he p r o f u s i o n o f r es ul t s p r e s e n t e d a b o v e whi c h
d e mo n s t r a t e t h a t t h e s u mma t i o n a r e a f o r
a d a p t a t i o n is ei t her e qua l t o or s ma l l e r t h a n t he
s i gnal s u mma t i o n a r e a o f t he r e c e pt i ve f i el d c e nt e r
i t sel f . Ho we v e r , t hi s c onc l us i on is c ount e r - i nt ui t i ve
t o a n u mb e r o f t h e o r i s t s who have p r o p o s e d t h a t
t he c e n t e r ' s ga i n o u g h t t o be r e g u l a t e d b y t he
s u r r o u n d ( He l s on, 1964; Sper l i ng, 1970; Gr os s be r g,
1981). Suc h a n i mp o r t a n t p o i n t de s e r ve s di r e c t
s c r ut i ny.
Th e i nf l ue nc e o f t he s u r r o u n d on t he c e nt e r i n
t he s c o t o p i c r a nge was me a s u r e d b y En r o t h - Cu g e l l
et al . (1975). The i r r es ul t s a r e g r a p h e d i n Fi g. 38.
Th e ga i n a n d t he me a n i mp u l s e r a t e as a f u n c t i o n
o f b a c k g r o u n d a r e a a r e s hown f or t wo cel l s, one
X o n - c e n t e r cel l , a n d one Y on- c e nt e r cel l . The gai n
d r o p s as t he a r e a o f a b a c k g r o u n d s pot , o f c ons t a nt
l umi na nc e , is i ncr eas ed so t ha t it j us t fills t he cent er .
I nc r e a s e o f a r e a b e y o n d t hi s va l ue p r o d u c e s no
f ur t he r i ncr eas e or decr eas e i n gai n. Ho we v e r , t her e
is s t e a d y s t at e i n p u t f r o m t he s u r r o u n d c a u s e d by
t he l a r ge b a c k g r o u n d s b e c a u s e t he me a n i mp u l s e
r a t e does de c l i ne whe n t he b a c k g r o u n d s pot gr ows
l a r ge r i n si ze t h a n t he g a n g l i o n c e l l ' s c e nt e r a n d
i n t r u d e s i nt o t he s u r r o u n d . Th u s s t e a d y s u r r o u n d
i n p u t doe s not r e g u l a t e c e nt e r ga i n i n t hi s
e x p e r i me n t .
Th e q u e s t i o n o f wh e t h e r t he s u r r o u n d mi ght
r e gul a t e t he gai n o f t he cent er i n t he p h o t o p i c r a nge
c a n n o t be a n s we r e d so de f i ni t i ve l y i n t he ne ga t i ve .
En r o t h - Cu g e l l et al . ( 1977a) f o u n d t h a t Y cel l s
b e h a v e d t he s a me wa y i n t he p h o t o p i c a n d s c ot opi c
r a nge s , i . e. t he r e was no c h a n g e i n ga i n whe n t he
a r e a o f a b a c k g r o u n d s p o t o f f i xe d l u mi n a n c e was
10 ~ t
0.01
i i ~ , h H l t ] i l HI l [ ~ , i ~ JJ~l ~ i ~[ : I l d
0 1 1 0 10 100
Background area (deg ~)
( b) Mai ntai ned f requency
g 4 0
- ?
_E
2 0
0 01 0 1 1 0 10 100
Background area (deg z)
F1G. 38. No ef f ect of the sur r ound on the gai n o f the center
in cat retinal ganglion cells in the scotopic range. Red steady
spots, centered on the receptive field middle, and of diameters
indicated by their horizontal coordinates, were used as
backgrounds. Their illuminations were 4. 104 quanta(507 nm)
(deg a s) -1 for the Y cell (filled symbols) and 2.5. l0 s for the
X cell (empty symbols). For both cells the stimulus was a
blue - green test spot (0.18 deg diameter for the Y cell, 1 deg
diameter for the X cell). The stimulus illumination was
adjusted to produce an approximately constant peak
response, and the gain calculated from response magnitude
and stimulus flux. The gain (i/q ratio) fell as the background
diameter was increased so long as the background diameter
was less than the diameter of the center (marked with the
empty arrow for the X cell, with the filled arrow for the Y
cell). To determine whether light falling outside the center
did indeed activate the surround, the maintained firing was
measured and is displayed in the lower panel. The cells'
maintained firing rates were reduced by the light failing
beyond the center, indicating sustained surround antagonism
of the center, even though the gains of the centers were not
affected by this same light. From Enroth-Cugell et al. (1975).
i nc r e a s e d b e y o n d t ha t o f t he c e nt r a l s u mmi n g a r e a ,
as i l l us t r a t e d i n Fi g. 39 ( Not e t ha t i n Fi gs 39 a n d
40 t he ve r t i c a l axi s is l og t h r e s h o l d f or a c r i t e r i o n
r e s pons e , whi c h is e qui va l e nt t o t he l og o f t he
r eci pr ocal o f t he gai n) . Howe ve r , t he d a t a on X cel l s
wer e i nc ompl e t e . On l y one X cel l was s t udi e d i n t he
p h o t o p i c r a nge , a n d i t s h o we d a s ma l l but
s i gni f i cant i ncr eas e o f cent er gai n when t he a d a p t i n g
s p o t wa s e n l a r g e d t o c o v e r t h e s u r r o u n d , a s s h o wn t o i n c l u d e t h e s u r r o u n d wa s s ma l l e r t h a n t h e
i n Fi g . 4 0 ( a ) f r o m u n p u b l i s h e d r e s u l t s o f L e n n i e , f r a c t i o n a l l o s s o f g a i n wh e n a s t i mu l u s s p o t wa s
He r t z a n d E n r o t h - C u g e l l . T h e f r a c t i o n a l r e c o v e r y e n l a r g e d t o i n c l u d e t h e s u r r o u n d a s i s i n d i c a t e d i n
o f c e n t e r g a i n wh e n t h e b a c k g r o u n d wa s e n l a r g e d Fi g . 4 0 ( b ) . T h i s c o u l d b e b e c a u s e t h e s u r r o u n d
A
T
7
E
c
0
" ( a )
0
9 On- cent r e Y
0
0
8 0
O
O
0 0
OO o
O
( b)
0
I
10 On-centre Y
N
g
~ 0
~ ~,~. 9 0
o 0
00000 O
8
I J I J l l l l Jl I J i i l i ; l I I OI I 1 J l l Jl l l t I J I l l l i J :
0.1 1. 0 10 1-0 10
Test di amet er (deg) Background di amet er (deg)
FIG. 39. Signal and adaptive summat i on in a Y gangl i on cell in t he phot opi c range: no effect of surround on adaptive
summat i on.
(a) The phot opi c cent er' s size was det ermi ned as in Figs 30 and 32, by obt ai ni ng t hreshol d i l l umi nat i on for a const ant
response, as a funct i on of area. Thi s was done with red spots (modul at ed at 4 Hz) on a steady b l u e - green backgr ound
which had a retinal i l l umi nat i on of 8.108 quanta(507 nm) (deg ~ s) -1.
(b) The size of t he " adapt at i on pool " of t he center was det ermi ned with an a r e a - a d a p t a t i o n curve as in Fig. 32(b).
A fixed 0.2 deg di amet er stimulus was set t o be at t hreshol d on a 15 deg background. The backgr ound was reduced in
area, in discrete steps, and t he i l l umi nat i on of t he backgr ound was adj ust ed t o keep t he response t o t he central test spot
at criterion. The required i l l umi nat i on of t he backgr ound is pl ot t ed against its diameter. Fr om Enrot h-Cugel l et al. (1977a).
ON-CENTER X
(b)
- ( a) o
I00 B O ~.
~ , o
-o
o
o
O 0
p 9.0 o o 70
O o
g
o
B O 60
S
I I I I / l l I I I I
0.1 0. 5 1.0 ,5.0 I O0 O1 0. 5 1.0 5. 0 I 0. 0
BACKGROUND DI AMETER ( deg) TEST DI AMETER (deQ)
FIG. 40. Signal and adapt i ve summat i on i n an individual X gangl i on cell in t he phot opi c range.
(a) The left panel shows t he backgr ound i l l umi nat i on required t o keep a 0.2 deg di amet er red test stimulus (modul at ed
at 4 hz) at audi t ory t hreshol d for modul at i on, as t he ( bl ue - gr e e n) backgr ound di amet er was varied f r om 0.2 t o 10 deg.
(b) The ri ght panel shows t he test i l l umi nat i on required for a 4 Hz modul at ed, red, 0.2 deg diameter, spot t o produce
a t hreshol d response, on a b l u e - green 15 deg backgr ound of retinal i l l umi nat i on 8-10 a quanta(507 nm) (deg 2 s)-' . Fr om
Lennie, Hert z and Enroth-Cugell, unpubl i shed results.
316
mi ght be rel at i vel y less sensitive t o st eady st at e
i l l umi nat i on t han is the center; the measur ement of
surround - center gai n in (b) was made at a stimulus
modul at i on r at e of 4 Hz, while t he i l l umi nat i on of
cent er and sur r ound in t he adapt at i on exper i ment ,
plotted in (a), was const ant in time. This experi ment
needs t o be repl i cat ed on a l arger popul at i on of X
cells t han one, in or der t o be abl e t o eval uat e the
s ur r ound' s cont r ol of cent er gain. However , it is
an indication t hat the surround may pl ay a di fferent
rol e in X cells in t he phot opi c r ange f r om its
i neffect ual per f or mance in the scot opi c range. Thi s
resul t is t ant al i zi ng f r om t he s t andpoi nt of
s t r u c t u r e - f u n c t i o n correl at i ons. The absence of
either sensi t i zat i on or desensi t i zat i on (in the cat
retina) caused by the surround in the scot opi c range
implies t hat the i nt erneuron which cont rol s the gain
of t he gangl i on cell cent er has a recept i ve field the
size of the cent er, with no spat i al l y ant agoni st i c
i nput . The absence of s ur r ound gai n cont r ol of the
cent er in the phot opi c range f or Y cells carries the
same i mpl i cat i on. The presence of a smal l but
si gni fi cant sensi t i zat i on of t he cent er by t he
sur r ound in t he phot opi c r ange in X cells suggests
t hat t he gai n of t he X cent er in t he phot opi c range
mi ght be set with an i nt er neur on wi t h a cent er the
size of the X cel l ' s phot opi c cent er but with an
addi t i onal sur r ound. One possi bl e specul at i on is
t hat X cells al ways have their gai n set by the bi pol ar
cells f r om which t hey receive di rect i nput , and t hat
t he r od bi pol ar cells have a weak or non-exi st ent
surround mechani sm while the cone bi pol ar cells do
possess a s ur r ound (cf. Nel son et al. , 1981). The Y
cells whi ch receive mos t of t hei r i nput vi a the
amacr i ne r out e woul d al ways have t hei r gai n set by
i nt e r ne ur ons whi ch do not ha ve s u r r o u n d
ant agoni sm.
Ther e is a compl et el y di f f er ent expl anat i on f or
sensi t i zat i on which shoul d be consi dered. Suppose
t hat t he sensi t i zat i on exper i ment is done agai nst a
low di ffuse backgr ound. Scat t ered light f r o m t he
test spot may excite the sur r ound when the adapt i ng
spot is smal l , and not when t he adapt i ng spot is
l arge, and effect i ve in desensitizing t he sur r ound.
Thus, t he " c o n t r o l " response t o a test spot on t he
small backgr ound may be a " mi xe d" response f r om
cent er and sur r ound, which is cl eansed of sur r ound
c o n t a mi n a t i o n by t he e n l a r g e me n t o f t he
backgr ound. Occasi onal l y, such mi xed responses t o
test stimuli on small adapt i ng spot s were seen, bot h
in t he Enr ot h- Cugel l et al. (1975) st udy (Figs 2, 3
and 4 in t hei r paper ) and in l at er wor k on
sensitization of the cone pat hway by Lenni e, Her t z
and Enr ot h- Cugel l (unpubl i shed). Removal of
sur r ound cont ami nat i on pr oduces a l arger peak
response, and a much l arger sust ai ned response, t o
a test spot pl aced in the center of the receptive field.
The l ar ge s ens i t i zat i on ef f ect s obs e r ve d in
psychophysi cal experi ment s may be due mor e to this
"r el ease f r om sur r ound c ont a mi na t i on" t han f r om
t he possi bl e but pr obabl y weaker i nfl uences of
sur r ound signals on t he gai n of t he cent er.
3 . 8 . A D i f f e r e n t Ki n d o f Ga i n Co n t r o l : T h e
Co n t r a s t Ga i n Co n t r o l
Up to this poi nt we have onl y consi dered the
effect of st eady i l l umi nat i on on t he cont r ol of
retinal gai n and dynami cs. However , t here is
anot her gai n cont r ol which depends not on t he
st eady light level but r at her on the aver age
modul at i on of opt i cal stimuli over a wide regi on of
visual space. This is what Shapl ey and Vi ct or (1978,
1979, 1980, 1981) have t er med t he cont rast gain
control. It is pr oba bl y equi val ent t o the "si l ent
s ur r ound" di scovered by H. B. Barl ow (1953), and
t o t he "s uppr es s i ve s ur r ound" f ound in t he ret i na
by Cl el and and Levi ck (1974). Anal ogous retinal
mechani sms have been f ound in pre-gangl i oni c
i nt er neur ons in t he mudpuppy ret i na by Werbl i n
and Copenhagen (1974) and Thi bos and Werbl i n
(1978b). Pl ease not e t hat t he t er mi nol ogy may be
conf usi ng in this case; t he cont r ast gai n cont r ol
adj ust s the gai n of the ret i na cont i ngent on cont rast
r at her t han flux. Per haps we shoul d call it t he
cont rast gai ncont rol , t o distinguish it f r om t he flux
gai ncont r ol s.
Thi s new ki nd of gai n cont r ol was ori gi nal l y
di scovered in exper i ment s in whi ch t he t empor al
frequency response of cat retinal gangl i on cells was
measur ed as a f unct i on of cont r ast . The results of
such an exper i ment are shown in Fig. 41. The dat a
are di spl ayed in a Bode pl ot , wi t h log ampl i t ude vs
log t empor al frequency in t he upper gr aph and with
linear phase vs log t empor al f r equency in the l ower
panel . I f t here were no cont r ast gai ncont r ol , t he
ampl i t ude curves woul d be the same shape, i.e. they
coul d be super i mposed by means of a vertical shift.
VISUAL ADAPTATI ON AND
Fur t her mor e, the phase curves at di fferent contrasts
woul d be superi mposabl e. This is not t he case. The
ampl i t ude curve is shi ft ed t owar ds hi gher t empor al
frequenci es at hi gher cont rast s, and t he phases of
i nt ermedi at e frequenci es are advanced at hi gher
cont rast s. At an r . m. s, average cont r ast of 0.2, t he
ampl i t ude of the response t o 0.5 Hz may be reduced
by 507o on account of t he act i on of t he cont r ast
gai ncont r ol . The phase may be shi ft ed at 8 Hz by
as much as 60 deg. Anot her way t o l ook at t he
cont rast gai ncont rol is t hat it produces what appears
t o be a f r e q u e n c y - d e p e n d e n t sat ur at i on. The
ampl i t udes of r esponses t o hi gher t empor al
frequencies grow approxi mat el y proport i onal l y with
cont r ast . The ampl i t udes of responses t o l ower
t empor al frequenci es grow less t han pr opor t i onal l y
with cont r ast , and appear t o sat urat e at a l ower
cont r ast . That this ef f ect is not simple sat ur at i on
is pr oven by t he t empor al f r equency dependence.
The spatial and t empor al dependence of t he
cont rast gai ncont rol ' s act i on indicate t hat it has t he
same characteristics as t he nonl i near recept i ve field
subuni t s whi ch feed exci t at i on t o Y cells (Shapl ey
and Vi ct or, 1978; cf. Appendi x 2). It appear s t hat
t he subuni t s precede t he cont r ast gai ncont r ol in
ret i nal processi ng; t he subuni t s comput e t he t ot al
average cont r ast whi ch is t hen used t o cont r ol
t he r et i na' s dynami c responses. The way t hat t he
cont r ast gai ncont r ol modi fi es t he t i me cour se of
ret i nal responses appear s t o be by modul at i on of
t he st rengt h of pre-existing f eedback pat hways.
That is, increase of cont r ast t ends t o t ur n on t he
cont r ast gai ncont r ol whi ch t hen increases t he
st rengt h of negative f eedback in bot h X and Y
ret i nal pat hways (Shapl ey and Vi ct or, 1981).
The cont r ast gai ncont r ol calculates a cont r ast
signal by averagi ng t he cont r ast modul at i on over
a wide expanse of ret i na. The spatial ext ent of t he
area of cont r ast averagi ng has not been det ermi ned
precisely, but it must be consi der abl y l arger t han
t he ext ent of t he cent er mechani sm of Y gangl i on
cells. Rough estimates of its spatial ext ent may be
based on t he area over which t he pr oduct , cont r ast
times area, pr oduces a given amount of low
f r equency suppressi on or mi d- f r equency phase
advance. Thi s area is on t he or der of t en degrees,
i.e. about 2 mm on t he ret i na. Fur t her mor e, t he
cont r ast gai ncont r ol may receive weaker but still
si gni fi cant i nput f r om still f ur t her reaches of t he
RETI NAL GAI N CONTROLS 3 1 7
ret i na, in this way also resembl i ng t he exci t at or y
nonl i near subuni t s of Y cells. Thus t he cont r ast
gai ncont rol must involve a t hi rd type of i nt erneuron
di fferent f r om t he previ ousl y i nferred i nt erneurons
whi ch are needed t o account f or t he f l ux
gaincontrols of the X and Y cell center mechanisms.
Because of its wide summi ng area, t he cont r ast
gai ncont r ol can account f or nonl i near spatial
summat i on of responses pr oduced by cont r ast
modul at i on in t he cent er and per i pher y of X and
Y ganglion cell receptive fields (Shapley and Victor,
1979). Thi s has been observed with sinusoidal test
stimuli by Shapley and Victor and with square wave
Y CELL
C o n f r a s t
o 0 . I
3 2 . 0 0 o 0 0 1 2 5
,o.oo
_ E
3 2 o
1 , 0 0
< 0 3 2
I ] [ I I I
~ -0. 5
E -1.0
< -1.5
I
- 2. 0
T E M P O R A L F R E Q U E N C Y
FIG. 41. The c ont r a s t ga i nc ont r ol r eveal ed i n t e mpor a l
f r equency r e s pons e s o f r et i nal ga ngl i on cells. The s e ar e da t a
f r om a n on- cent er Y cell. The me a n l umi nance was 20 cd m -2,
a n d t he pupi l di amet er was 3 mm. The s t i mul us was a 0. 25
c deg- ' si ne gr at i ng whi ch was modul a t e d i n a mpl i t ude by
a s u m o f s i nus oi ds , wi t h t e mpor a l f r equenci es f r o m 0. 2 up
t o 32 Hz. The e mp t y circles were obt ai ned whe n t he cont r as t
was 0. 0125 per si nusoi d, i. e. i f any one o f t he ei ght s i nus oi ds
ha d been pr esent ed al one, t he peak cont r as t o f t he modul a t e d
gr a t i ng woul d have been 0. 0125. The filled circles were
obt ai ned wi t h 0. 1/ s i nus oi d cont r as t . The ampl i t udes pl ot t ed
ar e t he Four i er a mpl i t ude s i n t he cel l ' s i mpul s e t r ai n whi ch
wer e at t he t e mpor a l f r equenci es pr es ent i n t he s t i mul us ; t he
pha s e s ar e t he pha s e s hi f t s o f t hos e Four i er c o mp o n e n t s i n
t he i mpul s e t r ai n wi t h r espect t o t he c or r e s pondi ng
c o mp o n e n t in t he i nput si gnal . I f t he r et i na were l i near , or
i f t he nonl i near i t y were a si mpl e sat ur at i on, t he t wo ampl i t ude
cur ves s houl d be paral l el , a n d t he pha s e cur ves s houl d be
paral l el , a nd t he pha s e cur ves s houl d s upe r i mpos e . The
accent uat i on o f r es pons es at hi gh f r equenci es, a nd t he pha s e
a dva nc e at mi d- r a nge f r equenci es , as c ont r a s t i ncr eases, is
t he s i gna t ur e o f t he c ont r a s t gai ncont r ol . Fr o m Shapl ey a n d
Vi ct or (1979).
318
test stimuli by Enr ot h- Cugel l and Jaki el a (1980).
The effect of t he cont r ast gai ncont r ol on square
wave responses is t o make t hem smaller and mor e
t ransi ent , as can be seen in Fig. 42 f r om Enr ot h-
Cugell and Jaki el a (1980). Thi s is an exampl e of
nonl i near spatial summat i on because the peripheral
stimulus generat es no response when present ed
al one but suppresses t he response t o t he cent ral l y
pl aced bar stimulus when bot h are present ed
t oget her. This ki nd of suppressive ef f ect f r om
peri pheral st i mul at i on has been observed in many
gangl i on cell types in several di f f er ent species.
-.~u I001
50]
~ 0
~ 100
~ 5 0 ]
L
o
ON-CENTERY-CELL
grating
3 . 9 . T i me C o u r s e o f Ga i n Ad j u s t me n t i n Re t i n a l
Ga n g l i o n Ce l l s
drifting
( a )
(b)
t ( c )
~ ( d )
0 l 2 3 sec
FIG. 42. Re duc t i on o f t he c e nt e r ' s ga i n by a movi ng pat t er n
in t he per i pher y o f t he recept i ve field in a cat ret i nal gangl i on
cell. Res pons es o f an on- cent er Y cell t o a cent er ed bar , 1 deg
wi de, 13 deg hi gh, o f l umi na nc e 0. 25 cd m "2 f l as hi ng at
0. 4 Hz.
(a) The bar was s upe r i mpos e d on a b a c k g r o u n d o f
l umi nance 5 c d m -~. Bot h bar a nd backgr ound were generat ed
on a CRT whi ch s ubt e nde d 13 deg by 16 deg.
(b) A dri ft i ng si ne gr at i ng wi t h a cont r ast o f 0. 5, and spat i al
f r equency 1.25 c deg -1 cover ed t he CRT scr een except f or
a 2 deg wi de b a n d down t he cent er o f t he scr een wher e t he
s t i mul us ba r was pr es ent ed. The gr at i ng was dr i f t i ng wi t h
a t e mpor a l f r e que nc y o f 1.14 Hz.
(c) Shows t he t i me cour s e o f t he bar s t i mul us .
(d) I ndi cat es t he t i me cour s e o f t he l umi na nc e c ha nge at
a poi nt in t he field over whi ch t he gr at i ng was dr i f t i ng. Fr o m
Enr ot h- Cuge l l a n d Jaki el a (1980).
The ret i nal gain as measured in gangl i on cells is
readj ust ed rapi dl y but not i nst ant aneousl y by
sudden changes in backgr ound level. This has been
det ermi ned in physi ol ogi cal experi ment s which are
anal ogous t o Cr awf or d' s psychophysi cal experi-
ment on t he t i me course of light adapt at i on in
humans ( Cr awf or d, 1947).
=
c
o22:
E
2 1 0
N 0.6
~02
~ I 1 I I I 1 I [ t
}- 0 1 O0 300 500 700
Del ay bet ween ' on" of condi t i oni ng
and ' o n ' of t est l i ght (rnsec)
FtG. 43. Ti me cour s e of gai n change in cat gangl i on cells:
modi f i e d Cr a wf or d exper i ment . On a 12 deg s t eady
ba c kgr ound of r et i nal i l l umi nat i on 5' l os quant a( 507 nm)
(deg 2 s) -1 were cent er ed: (a) a s qua r e wave modul a t e d
condi t i oni ng spot (1.5 s on, 3.5 s off), di am. 0. 57 deg, ret i nal
i l l umi nat i on 2. 5. los qua nt a ( de g 2 s)-' ; (b) a t est spot , f l as hed
on f or 20 ms in one cell (filled circles) a n d for 50 ms in
a not he r cell ( empt y circles), of di am. 0.1 deg, wi t h r et i nal
i l l umi nat i on 3. l 0 s quant a( 507 nm) (deg ~ s)-' . The t est st i mul i
were pr es ent ed wi t h var yi ng del ays wi t h r espect t o t he ons et
o f t he condi t i oni ng l i ght . Pl ot t ed in t he f i gur e f or t wo
di f f er ent on- cent er cells ar e t he ma gni t ude s o f t he r es pons es
t o t he t est pul ses of l i ght at di f f er ent del ay t i mes bet ween
onset of condi t i oni ng light and onset of t est pulse. The arrows
poi nt t o t he r es pons es to t he t est st i mul i whi ch gener at ed
r es pons es whi ch coi nci ded in t i me wi t h t he peak o f t he
r es pons e t o t he condi t i oni ng l i ght . Fr o m Enr ot h- Cuge l l a nd
Shapl ey (1973a).
In this experi ment retinal gain is pr obed by
measur ement of t he magni t ude of t he response t o
a br i ef test pulse of light. The test pulse is appl i ed
in the dar k and at various times aft er a conditioning
light is t ur ned on. The results of an experi ment of
this sort are shown in Fig. 43 f r om Enr ot h- Cugel l
and Shapl ey (1973a). The response t o t he test pulse
of light is t he same a hal f second af t er t he
condi t i oni ng light is of f as it is when t he
condi t i oni ng light has been of f f or several minutes.
The response is defi ni t el y reduced within 200 ms
f r om t he time t he condi t i oni ng light is t ur ned on.
VISUAL ADAPTATION AND RETINAL GAI N CONTROLS
Bet ween zero and 200 ms, t he response declines
uni f or ml y in magni t ude. In rel at ed experi ment s, it
was shown t hat t he gain st ayed at t he same new
val ue f r om 200 ms until 5 s af t er t he condi t i oni ng
light was t ur ned on. These experi ment s were done
in Y ceils under low scot opi c condi t i ons.
Si mi l ar results have been obt ai ned in X cells of
t he cat, by Sai t o and Fukada (1975), who st udi ed
t he t i me course of gain adj ust ment in X and Y cells
under mesopi c or l ow phot opi c condi t i ons. Ther e
is a gap in our knowl edge about t he t i me course of
gai n adj us t ment in X cells under scot opi c
condi t i ons, and a quest i on about whet her t he t i me
course of adapt at i on changes mar kedl y bet ween
scot opi c and phot opi c levels.
Sai t o and Fukada (1975) f ound t hat Y cells
showed a much sharper, mor e t ransi ent , gain
r educt i on i mmedi at el y af t er t he condi t i oni ng light
was t ur ned on, and t hen agai n a r educt i on
i mmedi at el y af t er it was ext i ngui shed, as i ndi cat ed
in Fig. 44. Thi s was at hi gher levels of backgr ound
XON
Co)
(c)
k . . . . I
319
illumination t han t he earlier experiments of Enr ot h-
Cugell and Shapl ey (1973a), which may explain t he
di fferences in findings. The gain r educt i on at bot h
" o n " and " o f f " of t he condi t i oni ng light seen by
Sai t o and Fukada may possi bl y have been due t o
one of t he " a ma c r i n e " gain cont r ol s we have
post ul at ed, ei t her t he cont r ast gai ncont r ol or t he
st eady-st at e fl ux gai ncont r ol of t he Y cell cent er.
It seems mor e likely t hat t he cont r ast gai ncont r ol
is i nvol ved in this phenomenon. The cont r ast
gai ncont rol contains t he kind of nonl i neari t y which
woul d cause r educt i on at bot h " o n " and " o f f " ;
it is an even- or der nonl i near i t y which generat es
responses of t he same sign at " o n " and " o f f " ,
responses like t hose seen in amacr i ne cells and Y
cells. It is i nt erest i ng t hat similar gain reduct i ons
at " o n " and " o f f " are seen psychophysically in t he
ori gi nal Cr awf or d (1947) exper i ment and in
i nt raret i nal recordi ng f r om t he amacr i ne cell l ayer
( Gor don and Gr aham, 1973; also unpubl i shed
results). It may be t hat t ransi ent gain reduct i ons in
YON
(e)
1.0
0 . 5 -
(d)
S ' - -
/ .
[ ! i i
I 2
0 i 2
Time, sec
| ( h )
I - 0 ]
i
o i 2 3
3 4 0
Ti me,
f -
/
J 2 3
sec
FIG. 44. Cr a wf or d exper i ment f or X a nd Y cells under l ow phot opi c or hi gh scot opi c condi t i ons. X cell dat a ar e in (a) - (d);
Y cell dat a ar e ( e ) - (h). PST hi s t ogr ams s how aver aged r esponses t o t he t est s pot ( shor t bar under hi s t ogr ams i ndi cat es
st i mul us t i me) and t o t he condi t i oni ng spot (l onger bar under hi st ograms). The backgr ound l umi nance was 5.9 cd m -2 t hr ough
a 4 mm di amet er art i fi ci al pupi l . The unat t enuat ed st i mul i wer e : t est , 3.9" 103, a nd condi t i oni ng, 6. 8- 10 ~ cd m "2. They
each s ubt ended 5' di amet er . The t est s pot was pl aced i n t he mi ddl e o f t he recept i ve fi el d cent er , whi l e t he condi t i oni ng
s pot was pl aced 15' t o t he side, still wi t hi n t he cent er. (a) and (e): t he t est spot was pr esent ed 2 s af t er onset o f t he condi t i oni ng
spot . (b) a nd (f): t est s pot al one, as a cont r ol . (c) a nd (g): t est s pot pr es ent ed 2 s af t er of f s et o f t he condi t i oni ng spot .
The dur at i on o f t he t est s pot was 200 ms f or t he X cell, 100 ms f or t he Y cell. The dur at i on o f t he condi t i oni ng s pot wa s
3 s. The vert i cal cal i br at i on is 50 i mpul ses s - ' . (d) a nd (h): The t i me courses o f t he change o f magni t ude o f t he r esponse
t o t he t est caus ed by pr es ent at i on o f t he condi t i oni ng spot . The rel at i ve magni t ude o f t he r es pons e is pl ot t ed agai nst t he
del ay bet ween t he onset t i mes o f t est and condi t i oni ng spot s. Fr om Sai t o and Fuka da (1975).
PRR3-1*
320 R. M. SHAPLEY AND
Y cells, due t o subst ant i al amacri ne i nput t o these
cells, are t he basis f or t he ps ychophys i cal
" o n - o f f " t ransi ent sensitivity losses.
While t he above results indicate t he rapi di t y of
some gain cont r ol processes in the retina, t hey do
not rule out t he existence of slower gain cont rol s.
These slower processes have not been studied with
t he Cr awf or d paradi gm, but t hey shoul d be.
Adel son' s (1982) results on t he t i me course of
human light adapt at i on i ndi cat e t he presence of
slower adapt at i on processes t han have been studied
in gangl i on cells up t o now. It is well known but
poor l y document ed t hat when t he mean level of
i l l umi nat i on is st epped up or down by t wo or mor e
log units in an adapt at i on experi ment , the gain may
t ake several mi nut es t o settle down or up to its new
steady value. Such slow adapt at i on processes
requi re f ur t her research.
4. GAI N AS A FUNCTI ON OF
I LLUMI NATI ON IN AMACRI NE CELLS,
BI POLAR CELLS, AND HORI ZONTAL
CELLS
The phenomena of gain cont r ol in gangl i on cells
requi re an expl anat i on in t erms of t he funct i onal
connect i ons of t he retinal net wor k a nd/ or t he
i nt r i ns i c p r o p e r t i e s of t he r e c e p t o r s a nd
i nt er neur ons in t he retina. The f undament al
quest i on is, where does t he cont r ol of gain begin?
C. ENROTH-CUGELL
Ideally, one woul d want t o have t he answer t o this
quest i on f or t he cat ret i na f r om whi ch so much of
t he results on gain cont r ol in gangl i on cells have
been obt ai ned. While t here are some f r agment ar y
results on the cat, t he t echni cal difficulties of
i n t r a c e l l u l a r r e c o r d i n g ha ve p r e v e n t e d a
compr ehensi ve st udy of gain cont r ol in cat ret i nal
i nt erneurons. We will t her ef or e concent r at e on t he
results f r om t he retinas of t wo col d- bl ooded
vert ebrat es whi ch have been studied t he most : t he
mudpuppy ( Nor mann and Werblin, 1974; Werblin,
1974; Werbl i n and Copenhagen, 1974; Thi bos and
Werbl i n, 1978a, b) and t he channel cat fi sh ( Naka
et al . , 1979).
4.1. Amacrine Cells
In the mudpuppy t he amacri ne cells have a steep
response versus i l l umi nat i on curve which can be
shi ft ed al ong t he log i l l umi nat i on axis by st eady
backgr ound i l l umi nat i on. This is illustrated in Fig.
45 f r om the wor k of Werbl i n and Copenhagen
(1974). This " cur ve shi ft i ng" is evidence f or a gain
cont r ol at or pr i or t o t he amacr i ne cell (see Sect i on
1 . 2 . 2 . ) .
In t he catfish, Naka et al. (1975) divided t he
amacri ne cells into t wo classes, t he t ype N and t ype
C cells. The type C cells correspond t o what Werblin
and colleagues (Werbl i n and Dowling, 1969;
Werblin and Copenhagen, 1974) call amacrine cells;
m i l l l v o l t s
I o
8 5 . 0
~ . ~ 4 . 5 ~ -
/ / .s
4 - / I
I / " - " ~ - ~ - ~ - 2 . 5 ~"
I / ~ z . o
2 - I I ~ " - - , . ~ - - - - , . 5
I
0 ~ ' = l ' I J I t n
L o 2 . 0 3 . 0 4 . 0 .... J [ ] I o mv
LOG I STIMULUS
Is
Flo. 45. Curve-shifting in mudpuppy amacrine cells, recorded intracellularly. Diffuse illumination was used as a test
stimulus. The dashed curves are inferred in regions where no data were taken. The peak value of the response is plotted
against log flash illumination. The retinal illumination from the tungsten source used was about one quant um per rod per
second for log I = 0. This works out to roughly 6" 103 quanta (522 nm) (mm 2 s) -~ for log I = 0. From Werblin and Copenhagen
(1974).
they produce " on- off" responses to spots or full-
field flashes. The type N cells are like the so-called
"sustained" amacrine cells found by Kaneko (1973)
and Naka and Ohtsuka (1975). The change of gain
of these two types of cell with background is
illustrated in Fig. 46 from Naka et al. (1979). They
clearly are affected similarly by backgrounds and
also greatly resemble the ganglion cells in the way
they adapt. That is, the gain is approximately the
reciprocal of background, approximately Weber's
Law.
We have to make a brief digression to make clear
that the results in Figs 45 and 46 were obtained in
compl et el y di fferent ways. Werblin and
Copenhagen (1974) used standard rectangular
increments of light on a steady background, and
measured the peak of the change in intracellularly 4.2. Bipalar Cells
recorded membrane potential. Naka et al . (1979)
measured first-order Wiener kernels by cross-
1 0 4
z
~
10 3
~ 10 2
b
I--
_ ~ i O +
io o
~ . / - - THEORETICAL IO 4
" ~ " \ HORJZONTAL
o,
\XX~, IO 2
" G A N G L I O N C ~
BIPOLAR CELL
I I I I
IO 0 IO I i0 z iO 3
MEAN INTENSITY
I I I
I0 0 I01 10 2
OFF CENTER
~BIPOLAR CELL
f T Y P E N CELL
1 0 4
FIG. 46. I nc r e me nt a l ga i n o f cat f i s h ne ur ons , r ecor ded
i nt r aeel l ul ar l y. The or di na t e is t he i nc r e me nt a l gai n, t he
a mpl i t ude o f t he fi rst or der Wi ener ker nel nor ma l i z e d by t he
ma g n i t u d e o f t he whi t e- noi s e mo d u l a t i o n . Th e hor i z ont a l
c oor di na t e is t he me a n i l l umi nat i on. Th e dot t e d l i ne is a
pr edi ct i on f r o m t he Na k a - Ru s h t o n r el at i on f or t he ga i n i f
t her e were no a da pt a t i on, j us t s at ur at i on. I ns et is a n aver age
o f t en s i mul t aneous r ecor di ngs f r om hor i zont al a n d gangl i on
cells. Res ul t s f or va r i ous cell t ypes ar e l abel ed i n t he f i gur e.
We bel i eve t he l owest me a n i nt ens i t y was a r et i nal i r r adi ance
o f 0.1 ~ wat t s crn -2 o n t he ret i na. The light sour ce was i n mos t
c a s e s a g l o w- mo d u l a t o r t ube whi c h was a t t e nua t e d by
neut r al dens i t y fi l t ers. F r o m Na k a e t al . (1979).
321
correlating a white-noise modulated light stimulus
with the resulting "noi sy" modulation of the cells'
membrane potential. The gain for the type N cells,
and for all the other cells the results of which are
shown in Fig. 46, is the gain at the peak of the first
order Wiener kernel. The peak value of the kernel
(first or second order) at each background level,
divided by the standard deviation of the white noise
stimulus, may be taken as a measure of gain at that
background level.
The bipolar cells form the main link between
photoreceptors and ganglion cells and thus the
dependence of gain on background for these cells
is of crucial importance for understanding the site
of adaptation.
The available data on gain control in bipolars
come mainly from Naka et al. (1979) and from
Thibos and Werblin (1978a). The results of Naka
et al . (1979) on catfish bipolars are displayed in
Fig. 46, on the same graph as the amacrine cell
data. Clearly, the bipolars' gain begins to drop at
about the same level of illumination as the
amacrines, and falls with a similar but somewhat
shallower slope. Since bipolar cells are the input to
amacrine cells in catfish (Naka and Ohtsuka, 1975)
as in other animals (Dowling and Boycott, 1965),
it is reasonable to suppose that the dependence of
gain on background observed in the amacrines is
already largely determined at the bipolar level.
The results on light adaptation in bipolars in
mudpuppy (Thibos and Werblin, 1978a) have
concentrated on the way in which the surround of
the bipolar receptive field sets the gain of the center.
This is illustrated in Fig. 47, which shows response
vs log illumination under two conditions: (i) no
background i l l umi nat i on; (ii) background
illumination falls on the bipolar's surround. In case
(i), the i nt ens i t y- r es pons e funct i on is
approximately fit by the Naka - Rushton relation,
equation (6). In case (ii), the response vs
illumination curve of the same form is shifted to
322
t he right as woul d fol l ow f r om gain r e- adj ust ment
by illumination of t he surround (see Section 1.2.2.).
Cont r ol experi ment s established t hat this was not
a result of light scat t er ont o t he cent er (Werbl i n
1974). This is evidence t hat , in t he mudpuppy
ret i na, t he gain of t he bi pol ar cell is set by signals
comi ng f r om its sur r ound, whi ch in this species is
believed t o be medi at ed by hori zont al cells (Werblin
and Dowl i ng, 1969; Thi bos and Werbl i n, 1978a).
Such results suggest t hat , in t he mudpuppy,
horizontal cells act as a gain cont rol on bipolar cells.
Two poi nt s of compar i s on wi t h pr evi ousl y
present ed psychophysi cal and physi ol ogi cal results
are needed here, to prevent the (probabl y erroneous)
inference t hat this conclusion is generally applicable
t o all vert ebrat es.
The first compar i son of Fig. 47 is with t he
sensi t i zat i on p h e n o me n o n in huma n vi si on
di scovered by West hei mer (1965). The results in
Fi g. 47 ar e t he opposi t e o f We s t h e i me r
sensitization. Il l umi nat i on in t he per i pher y of t he
mudpuppy bi pol ar' s receptive field desensitizes the
cent er in Wer bl i n' s (1974) and Thi bos' and
Wer bl i n' s (1978a) experi ment s. Ther e is, however,
a puzzling and unresol ved cont r adi ct i on with
Bur khar dt ' s (1974) r epor t of sensitization in
mudpuppy bi pol ar cells. Per haps it has t o do with
di f f er ent r ecept or i nput t o t he bi pol ar cells in the
t wo sets of experi ment s. Thi bos and Werbl i n
(1978a) were worki ng at low backgr ounds at which
rods were t he pr edomi nant i nput while Bur khar dt
was worki ng with a highly light adapt ed mudpuppy
ret i na in which it is pr obabl e t hat cones were t he
pr edomi nant phot or ecept or inputs t o t he proxi mal
retinal neurons. I f this is t he expl anat i on f or t he
opposi t e results, it woul d be an i nt erest i ng and
unusual exampl e of a reversal in funct i onal
characteristics because of t he t ransi t i on f r om r od
t o cone pat hways.
A second compar i son wor t h pursui ng is t hat
bet ween t he st rong effect on t he gain of the cent er
exert ed by t he sur r ound of mudpuppy bi pol ar cells
(Fig. 47) vis-a-vis negligible or, at most , weak effect
of t he sur r ound on t he gain of t he cent er in X and
Y cat ret i nal gangl i on cells (Figs 3 8 - 4 0 ) . This
di fference bet ween results on t he spatial ext ent of
" adapt at i on pool s " suggests t hat qui t e di f f er ent
mechani sms are i nvol ved in t he cont r ol of gain in
t he mudpuppy and cat retinas. In a sense such a
di fference woul d not be surprising because t he
mudpuppy and cat have evol ved quite di f f er ent l y
with widely di f f er ent visual capacities. The details
of exact l y how t he retinal net wor k is connect ed
spatially to regul at e gain mi ght well di f f er bet ween
t wo such di st ant l y rel at ed animals.
Ashmore and Falk (1980) have demonst rat ed t hat
t he gain of bi pol ar cells, in t he al most all-rod ret i na
of t he dogfi sh, begins t o dr op at ext remel y low
backgr ounds because of sat ur at i on in t he bi pol ar
cell itself. In the dogfi sh ret i na, t here is a very high
ampl i fi cat i on of r od signals at t he r od- bi pol ar
synapse, and as a result t he bi pol ar cells appr oach
t hei r response ceilings at very low backgr ounds.
Ther e is no evi dence f or a gain cont r ol , and
t h e r e f o r e t r ue l i ght a d a p t a t i o n , in t hes e
experiments. However, the results of Werblin (1974)
and Naka et al. (1979) illustrate how an aut omat i c
gain cont rol , acting on signals f r om phot orecept ors
t o bi pol ar cells, staves of f sat ur at i on in mudpuppy
and cat fi sh bi pol ars. In Fig. 46 f or exampl e, the
catfish bi pol ar' s gain begins t o dr op at a lower mean
level t han the hori zont al cell' s gain, presumabl y due
-17-
E
-6
"- --i 8-
4-'
o
- 19-
E
- - 2 0 ,,~
T I i " I I ~ I I
- 7 - - 6 5 4
FIG. 47. The ef f ect of a st eady i l l umi nat i on in t he per i pher y
o f t he recept i ve fi el d on t he s t i mul us - r e s pons e f unc t i on o f
mu d p u p p y bi pol ar cells; i nt racel l ul ar recordi ng. The s t i mul us
was a f l as hi ng s pot cent er ed on t he r ecept i ve fi el d o f t he
bi pol ar cell. The s pot ' s di amet er , 0. 4 mm, was chos en t o
s t i mul at e t he cent er opt i mal l y. St i mul us dur a t i on was 1 s.
The r e s pons e me a s ur e was t he s t eady s t at e pl at eau o f t he 1 s
response. Filled circles ar e f or no i l l umi nat i on i n t he peri phery
o f t he r ecept i ve fi el d; e mp t y circles ar e r e s pons e ma gni t ude s
whe n a - 4 l og uni t st eadi l y i l l umi nat ed a n n u l u s was pl aced
i n t he per i pher y o f t he fi el d. A modi f i e d Na k a - Ru s h t o n
f unc t i on was f i t t ed t o t he da t a i n t he condi t i on o f no
per i pher al i l l umi nat i on, a n d t he n t r ans l at ed l at er al l y t o fi t
the r esul t s obt a i ne d wi t h t he a nnul us . The l i ght s our ce was
a t ungs t e n l a mp, a t t e nua t e d by neut r al fi l t ers. The
una t t e nua t e d r et i nal i l l umi nat i on was cal cul at ed t o be a bout
10 '3 quant a( 522 nm) (cm ~ s) -t . I l l umi nat i ons ar e gi ven as l og
a t t e nua t i on rel at i ve t o t hi s val ue. Fr o m Thi bos a n d Wer bl i n
(1978a).
VI SUAL ADAPTATI ON AND RETI NAL GAI N CONTROLS
t o a neural gain cont rol acting on the bi pol ar and
not on the hori zont al cell. But at higher levels of
mean i l l umi nat i on, the hori zont al cell pot ent i al
starts sat urat i ng and its gain pl ummet s, failing
below the bi pol ar' s gain. Since bipolar cells appear
t o have steeper i nt e ns i t y- response funct i ons t han
horizontal cells (Werblin, 1974), t hey might saturate
at even lower mean levels t han the hori zont al cells,
were it not for the saving action of the gain control.
The aut omat i c gai n cont rol causes the bipolar cells
(and the more proxi mal retinal neurons t hey feed)
to lose some gain at lower levels in order t o preserve
gain at higher levels which woul d otherwise be lost
because of sat ur at i on (see Section 1.2.2.).
4. 3. Hori zont al Cells
There is quite a lot of i nf or mat i on on the control
of gai n in hori zont al cells because t hey are easier
to record f r om intracellularly t han the other retinal
interneurons. Since horizontal cells are anatomically
one synapse away f r om phot orecept ors, t hey of t en
mimic the receptors' adapt at i onal properties. One
of the significant out comes of this fact is t hat the
regul at i on of gain in phot orecept ors may be
i nferred, wi t h caut i on, f r om studies of the
regul at i on by light of the gain of hori zont al cells.
- 5 0
- 4 O
E - 3 0
== - 2 0
- i o
10
~ / j " ,
I I
Dar k adapt ed
- 6 3 BG
O 5. 3 BG
- 4 . 2 BG
- 3 2 BG
~ f I I f
- 7 . 0 - 6 . 0 - 5 0
323
We can begin t o see some of the diversity in
phot or ecept or a da pt a t i on in t he var i et y of
hori zont al cells' adapt at i onal behavi or (cf. also
Section 5).
Perhaps the best studied receptor - horizontal cell
system is in the t urt l e retina. Results on adapt at i on
in t urt l e hori zont al cells are quite clear, as shown
in Fig. 48 ( Nor mann and Perl man, 1979b). The
i nt ens i t y- r es pons e curves shift t o the right with
backgr ound, and the gain follows Weber' s Law.
These horizontal cells are driven exclusively by long-
wavelength cones, and their adapt at i onal properties
are mai nl y det ermi ned by their cone inputs
( Nor mann and Perl man, 1979a). The curve-
shifting in Fig. 48 is clear evidence for adapt at i on
of the t ype suggested in equat i on (10), with an
aut omat i c gain cont rol located in the cones.
To illustrate inter-species diversity we compare
the t urt l e hori zont al cell with the hori zont al cell of
the catfish retina, the gain vs backgr ound curve of
which is illustrated in Fig. 46. Here the hori zont al
cell curve is not like the curve of Weber' s Law.
Rat her, it follows the dashed curve, which is a
predi ct i on based on the Na k a - Ru s h t o n rel at i on
[equations (6) and (7)]. That is, the loss of gai n is
caused by saturation. Under the conditions of these
experiments, the catfish horizontal cells were driven
exclusively f r om long-wavelength cones (Naka,
I I I
- 4 0 ~ 3 0 - 2 0
LOg rel at i ve intL~r~Slly
F{G. 48. Ad a p t a t i o n i n t ur t l e hor i z ont a l cells; i nt r acel l ul ar r ecor di ng. The st i mul i were 0. 5 s i nc r e me nt s or de c r e me nt s on
a b a c k g r o u n d , except f or t he r es ul t s on t he da r k a da pt e d eye, whi ch were i nc r e me nt s onl y. The st i mul i wer e l ar ge 3. 2 mm
di a me t e r s pot s on t he r et i na. Pe a k r e s pons e s me a s u r e d f r o m t he da r k- a da pt e d r est i ng pot ent i al ( dot t ed line) were pl ot t ed
as a f unc t i on o f t est i l l umi nat i on. The cur ves were dr a wn by eye. The hor i zont al bar t h r o u g h each cur ve i ndi cat es t he st eady
me mb r a n e pot ent i al me a s u r e d at l east t wo mi nut e s af t er b a c k g r o u n d ons et . The i l l umi na t i ons ar e gi ven as l og a t t e nua t i on.
Th e u n a t t e n u a t e d t est s t i mul us (0 l og) was 6. 4- 10 ~ qua nt a ( 640 nm) ( cm 2 s) -1 on t he r et i na. Th e u n a t t e n u a t e d b a c k g r o u n d
i l l umi na t i on was 9 . 1 . 1 0 TM qua nt a ( 640 n m) ( cm 2 s) -1. Fr o m No r ma n n a n d Pe r l ma n (1979b).
324
per sonal communi cat i on) . Fi gure 46 i ndi cat es t hat
hor i zont al cells, and by i nference t he cones, of the
cat fi sh ret i na do not adapt but mer el y sat urat e, but
t hat bi pol ar cells, amacr i ne, and gangl i on cells do
adapt . In t he cat fi sh, much of t he adapt at i on t o
st eady light mus t t ake pl ace bet ween cones and
bi pol ar cells, t hough Fig. 46 also implies t hat t here
are addi t i onal stages of gai n cont r ol in t he i nner
pl exi f or m l ayer.
Ther e are dat a on t he dependence of gai n on
backgr ound in cat hori zont al cells, under conditions
such t hat t he responses were due t o phot or ecept or
i nput f r om rods only. The gr aph in Fig. 49 indicates
t hat cat hori zont al cells, driven by rods, have a gai n
vs backgr ound dependence whi ch appr oxi mat el y
follows Weber ' s Law above 1 td [Not e this is a " cat
t d " and t her ef or e is equi val ent t o about 8. 10 s
quant a(507 nm) (deg 2 s)-' ; St ei nberg, 1971]. Not e
t hat t hese hor i zont al cells t ypi cal l y receive mi xed
phot or ecept or i nput (Steinberg, 1971), even t hough
their maj or direct synapt i c cont act is with cones (see
Appendi x 1). Thi s suggests t hat r od - cone coupl i ng
is i ndeed i mpor t ant f or det er mi ni ng t he response
pr oper t i es of hor i zont al cells. In compar i ng
hor i zont al cell r esponses wi t h gangl i on cell
responses (Fig. 24), one notices t hat hor i zont al cell
gai n does not begi n t o dr op until t he backgr ound
is 1 td, which is t wo t o f our log units hi gher t han
the t r ansi t i on level of i l l umi nat i on f or gangl i on
cells. Thi s suggests t hat in the cat , as in t he cat fi sh,
t here must be gai n cont r ol mechani sms mor e
pr oxi mal in t he ret i na t han t he rods or the
hori zont al cells. However , the Weber Law behavi or
of hor i zont al ceils in the cat suggests t hat the rods
may also adapt when the level of illumination is high
enough (but see Section 5). Gai n versus backgr ound
curves are not avai l abl e f or cone- dr i ven hor i zont al
cell responses in cat .
The di versi t y of hor i zont al cell gai n changes due
to backgr ounds i ndi cat ed so far is represent at i ve of
t hat seen general l y. For i nst ance, in mu d p u p p y t he
hori zont al cells behave as if influenced by sat urat i on
and adapt at i on in t he scot opi c range, but resembl e
turtle hor i zont al cells - - al most pur e adapt at i on - -
in t he phot opi c r ange ( Nor ma nn and Werbl i n,
1974). However , car p hor i zont al cells show onl y
sat urat i on in the phot opi c range (Wi t kovsky, 1967).
But the r od- dr i ven skat e hor i zont al cells do adapt
to light by gai n r educt i on af t er an initial peri od of
sat ur at i on (Dowl i ng and Ri pps, 1971). Ther e is not
one st or y f or all ver t ebr at es. The pr oxi mi t y of
hor i zont al cells t o phot or ecept or s suggests t hat t he
recept ors mi ght also be very diverse in how t hey deal
wi t h changes in mean or backgr ound i l l umi nat i on.
Thi s expect ed di versi t y is f ound.
5. G A I N C O N T R O L I N P H O T O R E C E P T O R S
Some phot or ecept or s adj ust t hei r gai n by
adapt i ng in t he presence of st eady i l l umi nat i on and
onl y sat ur at e in very bri ght light, and ot her
phot or ecept or s adapt ver y little bef or e t hey
sat ur at e. Thi s di versi t y of r ecept or f unct i on wi t h
respect to gai n cont r ol and sat ur at i on has been
suggest ed al ready in t he discussion of gai n cont rol s
in hor i zont al cells. In order to organi ze this diverse
mat er i al , we will present t he dat a on r ecept or s as
fol l ows: (a) phot or ecept or s which adapt a lot a n d
al so sat urat e; and (b) phot or ecept or s which adapt
very little and mai nl y sat ur at e.
30
.~_
o_
~ 25
m
~20
<1
o ~ P5
4O
55
l ii
I 0
05 -
05 0 0.5 ~0 r 5 20 25
Log l~z, ,~ ( scol : opi c t d)
1
30
FIG. 49. Log test illumination (at 440 nm) plotted as a
function of log background illumination (620 nm) for a
constant amplitude peak horizontal cell response
intracellularly recorded in the cat retina. The background
duration was 5.5 - 6.5 s; the stimulus was 0.5 s in duration
applied after the response to the background had settled to
a constant value. The stimulus was a spot on a larger
background. The criterion response was 2.25 mV, and was
rod-driven. From Steinberg (1971).
5. 1. Pho t o r e c e pt o r s whi ch Adapt a l ot and Sat urat e
The photoreceptors which actually adapt, i.e.
more or less rapidly adjust their gain to avoid 10
saturation, include the following r o d s : skate,
(Dowling and Ripps, 1972); gecko, (Kleinschmidt
and Dowling, 1975); toad (Fain, 1976; Baylor e t al . ,
1979). The adapting c o n e s include: turtle (Baylor
and Hodgkin, 1974; Normann and Perlman,
1979a); mudpuppy (Normann and Werblin, 1974);
frog (Hood and Hock, 1975); ground squirrel
(Dawis and Purple, 1982); perhaps monkey
(Valeton and van Norren, 1983). The results on
cone adaptation in ground squirrel, frog, and
monkey are from massed potential recordings which
in one way or another isolated the cones.
Figure 50 illustrates photoreceptor adaptation in
rods from the toad B u f o m a r i n u s (Fain, 1976).
There is evidence of saturation (in the decline of the
peak response on background illumination), but
there is also clear curve-shifting of the V-log/curve,
consistent with the idea of an automatic gain
control, equation (10) (cf. Normann and Werblin,
1974; Dawis and Purple, 1982). Furthermore, the
gain of the toad rod follows Weber's Law (Fain, lo
1976), and this can even be seen in the photocurrent
recorded from the outer segment by the suction
electrode technique (Baylor e t al . , 1980) as in '~
Fig. 51. In Fig. 51 the vertical axis is labeled ~ lo
"sensitivity", but it is equivalent to what we have _
defined as "gai n". Log gain vs log background has
a flat portion and then a declining portion with a 01
slope about - 1. The slope of unity suggests an
adaptive gain control rather than the steeper slope
associated with pure saturation (see Section 1.2.2.).
The transition from flat to sloping is at about an
illumination of 0.28 quanta/am -2 s -1, which is about
forty times greater than the "dark light" of the
rods, the spontaneous current fluctuations in the
dark, measured independently. Baylor e t al. (1980)
make the point that this implies that the gain control
transition level in rods is not determined by the
"dark light". Similarly, we have pointed out in
connection with gain reduction in ganglion cells,
that the "dark light" in the cat retina is too small
to be responsible for determining the illumination
at which gain starts to fall (see Section 3.1.1.).
The gain reduction of the rod photocurrent is
accompanied by a very significant speeding up of
1
O 5
I I
7 8
s
o
o .
l o g
I I I I
1 0 1 1 1 2 1 3
( q u a n t a c r n - 2 f l a s h 1 )
FIG. 50. Effect of background light on the intensity-
response curves of toad rods; intracellular recording. Peak
response amplitude to a brief (around 100 ms) flash is plotted
against log flash energy per unit area (quanta cm-2), for the
dark adapted rod and for several background levels of
illumination. The stimulus and background were diffuse. The
illumination of the backgrounds is given in log units to the
left of each curve, and the units are log quanta(505 nm)
(cm 2 s) -1. From Fain (1976).
1 0 0 - -
~ s d
7 " . " I ! I I I
0-01 0"I I 0 1 0 I(}(3
l e ( p h o t o n s ~ m - 2 s e c - I )
FIG. 51. Gain vs background in the photocurrent of a toad
rod outer segment; recorded with suction electrode. The gain
is plotted on the vertical axis with units picoamps/(photon
/~m-2), but could really be given in picoamps/photon since
the rods are of fixed cross-sectional area. The background
illumination is plotted on the horizontal axis. The transition
from horizontal to sloping portions of the curve occurs at
0.28 quanta(507 nm) (/am 2 s) -1. The arrow points to this
illumination. Background and test were diffuse. From Baylor
e t al . (1980).
the rod response. The gain declines by about a
factor of one hundred over a range of backgrounds
which speed up the time to peak of the photocurrent
(in response to a brief flash) by a factor of seven.
326 R . M. S H A P L E Y A N D C . E N R O T H - C U G E L L
- 1 5
- 1 0
g -5
g.
0
I I I
D a r k a d a p t e d
- 4 " 4 B G
D - 3 . 2 B G
- 2 . 1 B G
121
I I I
- - 6- 0 - - 5"0 - 4 . 0
I I I I
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
I I I I
- 3 " 0 - 2 . 0 - 1 . 0 0 . 0
Log r e l a t i v e i nt e ns i t y
FIG. 52. Gain adjustment in turtle cones (recorded intracellularly) caused by background illumination. The stimuli were
0.5 s increments or decrements on a steady background (except for the curve for the dark adapted cone which only is for
increments). The stimulus spot was 3.2 mm in diameter on the retina. Peak responses measured from the dark-adapted
resting potential (dotted line) were plotted as a function of test illumination. The curves are Naka- Rushton functions.
The horizontal bar through each curve indicates the steady membrane potential measured at least two minutes after background
onset. The illuminations are given as log attenuation. The unattenuated test stimulus (0 log) was 6.4.10" quanta(640 nm)
(cm 2 s)-' on the retina. The unattenuated background illumination was 9.1.10 is quanta(640 nm) (cm 2 s)-L From Normann
and Perlman (1979a).
Bayl or e t al . (1980) f ound t hat G R ~ (tpeak) 25, 2-
wher e G R is t he gai n of t he r od i n
pi c oa mp/ qua nt um and t p e a k is the t i me from the
onset of the bri ef flash st i mul us to the peak of the 1
response.
Adj us t ment of gai n i n cones by adapt at i on and
sat ur at i on is represent ed i n Fig. 52 from the dat a
of Nor ma nn and Per l man (1979a). The paral l el ~ 0 -
I
curves are the response t empl at e f r om the dark ,-I
adapt ed cone, and are descri bed by the Naka-
Rus ht on r el at i on, e qua t i on (6). Whe n t he _o
backgr ound is raised, the response to i ncrement s is
somewhat compressed (consi st ent wi t h sat ur at i on) - 2
because the steady state response increases t owards
the maxi mal pot ent i al the cone is capabl e of
produci ng, as i ndi cat ed by the short hori zont al bars - 3
i nt ersect i ng each operat i ng curve. Fr om the shift of 2
the operat i ng curves, one may i nfer Weber ' s Law
since there seems t o be about a one log uni t shift
for each log uni t increase in background. That turtle
cones appr oxi mat el y fol l ow Weber ' s Law is
i ndi cat ed i n Fig. 53 from Bayl or e t al . (1974b). The
solid line is Weber ' s Law up t o about log Is = 4.5,
and t hen rises due t o sat ur at i on. It is based on a
t heory for the cone' s gai n cont r ol mechani sm by
Bayl or e t al . (1974b). Act ual l y the cone' s gai n
follows Weber ' s Law for about a log uni t more t han
the Bayl or e t al . t heory predi ct s, and sat urat es
rat her less t han the t heory predicts. One possibility
not consi dered by Bayl or e t al . is t hat some of the
/
/ ~ 0
I I I I I
3 4 , 5 6 7
l o g I ,
FIG. 53. Turtle cones' gain as a function of background;
intracellular recording. The ordinate of this unique plot is
the logarithm of the difference between the reciprocal of the
gain in the light adapted cone and the reciprocal of the gain
in the dark adapted cone, i.e. Iog{1/SF-I/SFD}. This number
unfortunately goes to minus infinity when the background
is so low that the gain of the cone is the same as in the dark
adapted state, but that region of the curve is not plotted here
anyway. The gain S F is in gV quantum-' effectively
absorbed. The horizontal axis is log background flux; the
units are quanta/sec effectively absorbed by the cone. The
stimuli were 10 ms flashes, and the gain is calculated for the
peak of the flash response. These are data from a red turtle
cone. The smooth curve is from Baylor et al.' s theory for
cone adaptation. From Baylor et aL (1974).
deviation at the high backgrounds might be due to
pigment bleaching, which is not included in their
theory. Cones also speed up their response with
background and for turtle cones, Gc ~" (tpeak) 4, that
is the gain of a cone decreased like the fourth power
of its time to peak for the response to a brief flash.
The total amount of "speeding up" of the cone
response is about a factor of two over a range of
backgrounds in which the gain drops by a factor
of two hundred. The speeding up of rod and cone
responses with the change in gain is illustrated in
Fig. 54 (Baylor and Hodgkin, 1974; Baylor e t al . ,
1980).
Steady illumination affects different parts of the
cone's response in different ways. This is illustrated
in Fig. 55 from Baylor and Hodgkin (1974). The
I I I
0
_o
--1
impulse response of the cone, i.e. the response to
a brief, weak flash of light in the linear range,
changes as the steady background increases. The
gain for later parts of the impulse response drops,
but the gain for the initial rising phase of the
response is relatively unaffected by steady
backgrounds. The peak of the response becomes
smaller at higher backgrounds and occurs at earlier
times after the flash, but the rising phases of
impulse responses at several levels of background
superimpose. Although this feature may not be
completely convincing in Fig. 55, it is true. Recent
preliminary experimental results involving the
measurements of temporal frequency responses in
turtle horizontal cells and cones are consistent with
the resistance of the rising phase of the impulse
I
1 . 6 2 . 2
- - 2
. . y-
O
-
, I I
1 . 8 2 . 0
l o g t m a x
E
E
O
O
f ~
100 -
5 0 -
2 0 -
1 0 -
5 . 0 -
2 . 0 -
1.0
0-5
0.2
0.1
0-1
I I I
0-2 0. 5 1.0 2.0
f'a~ak (see)
I I
5.0 10
FIG. 54. The speeding up of cone and rod responses in the turtle and toad retinas. As mean illumination increases, the
gain and the time to peak decrease. In the left panel, the log of the gain is plotted against the log of the time between
the peak response to a brief flash and the onset of the flash, for turtle cones (intracellular recording). The gain is plotted
against peak time for toad rods (suction electrode recording) in the right panel. For about two log units log tma x is
approximately proportional to log gain (here denoted SF). In the left panel, the different symbols are for different red
cones, eight in all. On the right are graphed data points from seven different rod outer segments. Note that the cone time
to peak stops decreasing when the gain drops below 0 log. The units of the left ordinate are log[#V (quanta gm-~)-l]; on
the right the units are picoamps (quanta ~m-2)-L On the left the units of the abscissa are log[ms]; on the right they are
simply s. From (left) Baylor and Hodgkin (1974), and (right) Baylor et al. (1980).
328
r e s p o n s e t o a d a p t a t i o n ( T r a n c h i n a , Go r d o n a n d
S h a p l e y , u n p u b l i s h e d ) .
m s e c
0 1 O 0 2 0 0 3 O 0
I I I
3 0 -
10
0 4"52 ~ ~ " " ";
2
I -
E
o 1
0
~. 0 - ~
>
0. 15
0- 10
0. 05
5.79
1 ~ I
I oo 200 300
msec
FIG. 55. Effect of increasing illumination of conditioning
step on the time course of the flash response in a turtle cone
(intracellular), The flash was I1 ms in duration, and was
applied 1.1 s after the onset of a conditioning step of
illumination. The horizontal axis is the time after flash onset.
The ver t i cal axes are all in uni t s of gai n:
/aV/photoisomerization, which is equivalent to taV/quantum
effectively absorbed. The numbers near each curve are the
illuminations of the conditioning steps, in units of
log[effective quanta(cone s)-q. These data are from a red
cone. The stimulus was a 150/am white spot. From Baylor
and Hodgkin (1974).
5 . 2 . P h o t o r e c e p t o r s w h i c h S a t u r a t e b u t d o n o t
A d a p t
T h e be s t s t u d i e d e x a mp l e s o f r e c e p t o r s wh i c h
s a t u r a t e wi t h o u t a d a p t a t i o n a r e t h e r o d s o f t h e
mu d p u p p y s t u d i e d b y No r ma n n a n d We r b l i n
( 1974) . F i g u r e 56 s h o ws t h e i r r e s ul t s . I t c a n be s e e n
t h a t t he r o d o p e r a t i n g c ur ve s s hi f t t o t he r i ght a ve r y
l i t t l e wi t h i n c r e a s i n g b a c k g r o u n d , b u t ma i n l y
c o l l a p s e d u e t o s a t u r a t i o n . S i mi l a r r e c e p t o r
b e h a v i o r is i mp l i e d b y t h e h o r i z o n t a l cel l r e s ul t s o f
Wi t k o v s k y ( 1967) i n c a r p a n d Na k a et al. ( 1979) i n
c a t f i s h . Re c e n t l y , Nu n n a n d Ba y l o r ( 1982) h a v e
r e p o r t e d t h a t r o d s i n t h e mo n k e y Macaca
fascicularis ma i n l y s a t u r a t e wi t h o u t a d a p t i n g . Th e r e
is s u p p o r t i v e e v i d e n c e f r o m ma s s r e c e p t o r p o t e n t i a l
r e c o r d i n g i n t h e r a t t h a t a t l e a s t s o me ma mma l i a n
r o d s s a t u r a t e wi t h o u t a d a p t i n g ( P e n n a n d Ha g i n s ,
1972; Gr e e n , 1973). Th i s is a l s o c o n s i s t e n t wi t h t h e
v e r y s ma l l a mo u n t o f a d a p t a t i o n i n t h e a - wa v e o f
t he r a t ' s E R G, t h o u g h t t o be d e t e r mi n e d b y r e c e p t o r
a n d h o r i z o n t a l cel l r e s p o n s e s ( Do wl i n g , 1967), a n d
b y ma s s r e c e p t o r p o t e n t i a l r e c o r d i n g i n t h e c a t e ye
i n wh i c h t h e i n n e r n u c l e a r l a y e r a n d t h e g a n g l i o n
cel l l a y e r we r e r e n d e r e d a n o x i c b y o c c l u d i n g t h e
o p h t h a l mi c a r t e r y ( S a k ma n n a n d F i l i o n , 1972).
S a k ma n n a n d F i l i o n a l s o s h o we d t h a t t h e g a i n o f
t h e i s o l a t e d r o d r e c e p t o r p o t e n t i a l wa s
E = 2
Q ~
0 - I , , I ' :
0 4
Fro. 56. Rod operating curves on backgrounds. Plotted is
the magnitude of the rod response (recorded intracellularly)
measured as the difference between the peak of the response
and the steady polarization just before the response. The
response to test flashes brighter than the background are
shown below the horizontal axis, and to test flashes dimmer
than the background above the axis. The stimuli were diffuse
2 s flashes. The background illuminations can be read as the
test stimuli which produced zero response, i.e. the intersection
of the curve with the horizontal axis. Circles are from a rod
in a normal retina, and squares are from a rod in a retina
treated with aspartate. The units of the horizontal axis, which
indicates the test flash illumination, are as follows: 6. l0 s
quanta(522 nm) (cm 2 s) -1 when log I = 0. From Normann and
Werblin (1974).
V I S U A L A D A P T A T I O N A N D R E T I N A L G A I N C O N T R O L S 329
I 0 '
" ~ 10 4
"0
i 0 I
"E I 0 '
I 0
Dotk
I 0 0
( a)
E
._E
MO)
f I I
I I 0 I 0 z IO s 104 I 0 " I 0 "
Adapt i nt ensi t y ( t r ol ands)
( b )
/ / / / / o~ ~3
/ / / / / ~5 02
, / / / . 4 .~o,,I.,.~
I I I I I I I
IO I 01 J O I IO* IO I IO e IO v
Test i nt ens i t y ( t r ol ands)
FIG. 57. Adaptation and saturation in the monkey cone receptor potential (extracellular recording of a mass response).
(a) The retinal illumination required to reach a criterion response in the monkey's late receptor potential is plotted against
background illumination. The criterion was 10/aV. Also shown are human psychophysical thresholds under the same stimulus
conditions. In both cases, the stimulus was a yellow (580 nm) light presented on a yellow background. The background
was on steadily for at least 5 min before test flashes were presented. The test stimuli were 150 ms in duration, presented
in the fovea. The axes are given in photopic td.
(b) Stimulus - response curves under dark adapted conditions and for five background levels for the monkey late receptor
potential. The adapting and test fields were both 1 mm spots, centered on the fovea. The adapting illuminations are indicated
in the figure in log td(photopic). The data are the mean values from six animals. They have been normalized for between
animal comparisons, as per cent of the maximum response for each animal. From Boynton and Whitten (1970).
a p p r o x i ma t e l y c o n s t a n t ove r s e ve r a l l og uni t s whe n
g a n g l i o n cel l g a i n was d r o p p i n g l i ke We b e r ' s La w.
Th u s , ma mma l i a n r o d s a n d t e l e os t c one s s e e m t o
s a t u r a t e wi t h o u t a d a p t i n g . Th e a n a t o mi c a l l y l a r ge r
r ods a n d cones o f a mp h i b i a n s a n d r ept i l es d o a d a p t
t o l i ght . F a i n (1976) ha s s ugge s t e d t he ne c e s s i t y f or
a d a p t a t i o n i n t he mo r p h o l o g i c a l l y l a r g e r r e c e p t o r s
be c a us e o f t hei r l a r ge r q u a n t u m c a t c hi ng ar eas , a n d
c o n s e q u e n t o v e r l o a d i n g at l owe r l evel s o f r e t i na l
i l l u mi n a t i o n .
We ha ve p u t o f f a d i s c u s s i o n o f ma mma l i a n
c one s t o l as t b e c a u s e t he e vi de nc e a b o u t t h e m is
i n d i r e c t a n d s o me wh a t e q u i v o c a l . Fi g u r e 57 f r o m
Bo y n t o n a n d Wh i t t e n (1970) s h o ws , i n t he r i ght -
h a n d p a n e l , r e s p o n s e - l og I c ur ve s o f t he i s o l a t e d
c o n e r e c e p t o r p o t e n t i a l r e c o r d e d wi t h g r o s s
e l e c t r o d e s i n t he f o v e a o f a mo n k e y ' s eye i n whi c h
t he o p h t h a l mi c a r t e r y h a d be e n b l o c k e d . The s e
cur ves ma y be a c c o u n t e d f or s ol el y i n t e r ms o f a
mo d i f i e d Na k a - Ru s h t o n r el at i on. On l y s a t ur a t i on,
c a l l e d b y B o y n t o n a n d Wh i t t e n " r e s p o n s e
c o mp r e s s i o n , " was us ed t o d r a w t he cur ves t h r o u g h
t he p o i n t s whi c h wer e a ve r a ge s f r o m r es ul t s o n si x
mo n k e y s . On t he l ef t , d a t a f r o m a n o t h e r mo n k e y
a r e seen t o f o l l o w We b e r ' s La w. As we k n o w f r o m
o u r p r e v i o u s d i s c u s s i o n , i n S e c t i o n 1 . 2 . 2 . ,
s a t u r a t i o n a n d We b e r ' s La w a r e i n c o mp a t i b l e , a n d
i n f act u p o n i ns pe c t i on, Fi g. 57(a) is n o t c ons i s t e nt
wi t h Fi g. 57( b) . I f one c o n s t r u c t s a n i n c r e me n t a l
g a i n vs b a c k g r o u n d c ur ve f r o m t he d a t a i n
Fi g. 57( b) , b y c h o o s i n g a c o n s t a n t r e s p o n s e
c r i t e r i o n , one o b t a i n s a c u r v e q u i t e u n l i k e
Fi g. 57( a) ; i t is mo r e s h a l l o w at l ow b a c k g r o u n d s
a n d s t e e pe r at hi gh b a c k g r o u n d s . I t is c o n s i s t e n t
wi t h a n e x p l a n a t i o n i n t e r ms o f s a t u r a t i o n . So we
d o n ' t k n o w whi c h c one r e c e p t o r p o t e n t i a l ( t hos e i n
Fi g. 57( a or b) is r e p r e s e n t a t i v e o f ma mma l i a n
c one s . Mo r e r e c e nt i n v e s t i g a t i o n o f t he s a me
p r e p a r a t i o n ( Va l e t o n a n d v a n No r r e n , 1983)
i ndi cat es t ha t a n a u t o ma t i c ga i n c o n t r o l r a t he r t h a n
s a t u r a t i o n is t he p r e d o mi n a n t f a c t o r i n c o n t r o l l i n g
ga i n i n p r i ma t e cones . But t hi s is a n i mp o r t a n t t opi c
whi c h wi l l u n d o u b t e d l y r ecei ve mo r e a t t e n t i o n .
6. T HE OR I E S OF R E T I NAL GAI N
C ONT R OL AND T HE DE T E R MI NANT S OF
VI S UAL S E NS I T I VI T Y
We ha ve d e v o t e d t hi s c h a p t e r up t o t hi s p o i n t t o
t he q u e s t i o n s " wh y " a n d " wh a t " c o n c e r n i n g t he
c o n t r o l o f r e t i n a l ga i n a n d vi s ua l s ens i t i vi t y.
Ho we v e r , t o d e a l wi t h t he q u e s t i o n " Ho w" i t is
d o n e , we wi l l at t hi s p o i n t r evi ew t he or i e s o f r e t i na l
330
and visual f unct i on. Theori es of light adapt at i on
can be divided i nt o t wo categories: (a) t heori es of
t he retinal gain cont r ol and (b) t heori es of how t he
gain cont rol and noise combi ne t o det ermi ne visual
sensitivity in psychophysi cal or behavi oral experi-
ment s. These will be discussed in t ur n.
6. 1. Theories of the Retinal Gai n Control
All t heori es of ret i nal gain cont r ol share t he
common f eat ur e t hat t hey at t empt t o account f or
a basic nonl i neari t y of vision, namel y t hat t he gain
and time course of responses t o time varying stimuli
are dependent on t he mean level of i l l umi nat i on,
or t he backgr ound i l l umi nat i on, t o which t he t i me
varyi ng stimuli are added. The nonl i neari t y of light
adapt at i on is a gentle one, allowing a linear range
of vision ar ound t he operat i ng poi nt of the mean
level. Anot her way of saying this is t hat t he mean
level must be changed a lot t o have a big effect on
gain and time course. For i nst ance, in t he Weber
Law range, in or der t o reduce t he gain t o hal f its
value at one mean level, the value of the mean must
be doubl ed. Thi s is a large change in mean level.
Thus for normal vision in the real world of (Weber)
cont rast s, which are in t he range 0 - 0 . 5 , t he
response of the visual system will not be t hrown into
a very nonl i near range by t he processes of retinal
light adapt at i on. In t he model s t o be consi dered,
adapt at i on acts like a nonl i near negative feedback:
a negative feedback because increasing t he out put
reduces the gain of earlier stages; nonl i near because
t he f eedback signal is not added or subt ract ed but
is used as a gain cont rol and a cont rol l er of the time
const ant s of response.
gain and time course of response in phot or ecept or s
of t he horseshoe crab, L i m u l u s p o l y p h e m u s . We
have excl uded the t opi c of light adapt at i on in
i nvert ebrat es f r om our review, f or obvi ous reasons
of length cont r ol . The phot or ecept or s of inverte-
brates are quite di fferent f r om those of vertebrates;
most of t hem depol ari ze in response t o increases in
i l l umi nat i on r at her t han hyper pol ar i ze as do verte-
brat e rods and cones. However , t he F u o r t e s -
Hodgki n ( FH) model has crossed phyl ogenet i c
boundar i es. Sui t abl y modi f i ed, it has been used by
Bayl or e t al . (1974a, b) and Bayl or e t al . (1980) t o
analyze t he gain and time course of turtle cones and
t oad rods, respectively. It is also rel at ed t o model s
devel oped f or t he cat ret i na by Enr ot h- Cugel l and
Shapley (1973a) and Shapley and Victor (1981), and
t o a model f or human vision pr oposed by Sperling
and Sondhi (1968), and t her ef or e is a useful starting
poi nt .
The FH model is composed of a sequence of
stages of t empor al i nt egrat i on connect ed in series,
as di agrammed in Fig. 58. Each stage is represented
as an RC circuit in t he original model . However ,
a t heor y with t he same f or mal st ruct ure can be
devised for stages which are chemical reaction states
reached by repeat ed catalytic react i ons (Borsellino
e t al . , 1965). The t i me course of t he response of
stage j in t he FH cascade is descri bed by a
di fferent i al equat i on which says t hat t he bui l dup of
response (or s u b s t a n c e ) j is pr opor t i onal t o a
react i on rat e const ant a~ times t he amount of
response (or substance) in stage j - I , minus the decay
f r om s t agej which is equal t o anot her rate const ant
a2 times t he amount of subst ance in state j .
6 . 1 . 1 . FUORTES AND HODGKIN' S MODEL FOR
PHOTORECEPTORS
Fuort es and Hodgki n (1964) originally developed
a t heoret i cal model t o account f or t he rel at i on of
d y j ( t ) / d t = a~v j _~( t ) - az yj ( t ) . (25)
In this scheme onl y t he first stage is driven by light,
d y ~ ( t ) / d t = Y . I ( t ) - az. vl(t) (26)
V o V 1 V , _ I Vr Vn
Inp Out put
C O 0 C - ' - ' - ~ I~ C R o
FIG. 58. Di agr am of t he Fuor t es - Hodgki n ( FH) model . The el ement s l abel ed/ a r epr esent i sol at i on st ages wi t h gai n g. Li ght
a da pt a t i on is a s s u me d t o af f ect onl y t he val ue o f R. Fr o m Fuor t es a nd Hodgki n (1964).
BuiLd up o f p a r t i c l e s
331
~ ( - t ) m , , , ~ l ~ - y ,
Li ght
Q u ( i (~
1 Y2 D Y3 l l l l l ] l ~ Y4 ]1 Y5 "
Removal of par t - i ct es
Y 6
( =Z, )
m ~ m d l l ~ Z ~
Open channels
ChanneLs
cl osed by Z ,
K 1 2 ~ " ~ K23 K34
Z2 . Z3
K21 K32
I Z 4
FIG. 59. This is a diagram of the Bayl or- Hodgki n- Lamb (BHL) model. The blocking substance is denoted y~ or z,. Y
is used for build-up, z for destruction of the blocking substance. Note that this scheme is fundamentally different from
the FH model (Fig. 58) in that the rate constant for production of each y stage is the same as for its decay, except for
the first and last stages. In the FH model, the rate constant for growth of each stage is different from the rate of decay,
and only the decay rate is subject to change by adaptation. Here adaptation only works by changing the rate constant of
decay from state z,. From Baylor e t al . (1974).
where Yis t he gai n of t he initial t r ansduct i on f r om
fight t o y and I(t) is the fight stimulus. The last stage,
t he t i me evol ut i on of whi ch is given by y, ( t ) , is
pr esumed in t he model t o cont r ol t he membr ane
conduct ance and t her eby t he el ect rophysi ol ogi cal
r esponse t o l i ght of t he phot or e c e pt or . In
compari ng equat i ons (25) and (26) with Fig. 58, one
shoul d make t he i dent i f i cat i on a , = ~ / C and
a2 = 1/ RC.
Thi s model was devel oped t o expl ai n first of all
t he many stages of t empor al i nt egr at i on in t he
process of visual t r ansduct i on, as refl ect ed in t he
slow rise t o t he peak of t he i mpul se response of
phot or ecept or s. It does this ver y well. In t urt l e
cones and t oad r ods t he model indicates t hat t he
number of stages is f r om f our t o six. Fr om t he
experi ment al evidence of the t oad r od phot ocur r ent
recordi ngs ( Bayl or et ai . , 1980) pr obabl y all of t he
t empor al i nt egr at i on is in t he out er segment of t he
phot or ecept or .
The FH model as r epr esent ed in equat i ons (25)
and (26) is a l i near model . That is, t he sum of t wo
i nput s L( t ) + 12(0 yields a response y. ~(t) + y. 2(t)
whi ch is t he sum of t he responses t o t he t wo i nput s
present ed al one - - t he pri nci pl e of Superposi t i on.
However , Fuor t es and Hodgki n (1964) descri bed a
modi fi cat i on of t he model which woul d help explain
observed depart ures f r om linearity, in particular t he
change of gain wi t h changes in mean level of
i l l umi nat i on which is t he basis of phot or ecept or
light adapt at i on. They suggested t hat t he rat e
const ant of decay, a2, was i ncreased by increase of
st eady level of t he out put stage y, but t hat t he rat e
const ant f or bui l dup al was i ndependent of
i l l umi nat i on. Thus, t he scheme t hey pr oposed was:
a2 = ao2(1 +f 0' . ) ) (27)
where t he f unct i on fLy.) is chosen t o fit t he
dependence of gain on mean level.
The poi nt of t he FH model f or adapt at i on is t hat
t he gain and t i me course of response are t her eby
l i nked, whi ch may be seen as follows. Say T2 =
1/a2. The i mpul se response (t hat is, t he response
t o a br i ef fl ash in t he linear range) of t he simple
n-stage FH model is, [cf. equat i on (7) of Fuor t es
and Hodgki n, 1964]
Q . A . T2"-'. (t l T2)"-' e -'IT2
(28)
where Q is t he amount of light in t he fl ash and A
is a const ant pr opor t i onal t o (al)". The time t o peak
of this i mpul se response is ( n - 1)T2 and t he gai n
is pr opor t i onal t o /'2 "-1. I f onl y T2 is r educed by
adapt at i on, as assumed by Fuor t es and Hodgki n,
t he t i me t o peak will short en and t he gain will drop,
much mor e steeply t han t he t i me t o peak.
332
Ther ef or e, in t he ori gi nal FH model , t he rel at i on
bet ween gai n and t i me t o peak of t he i mpul se
response is a power l aw where t he exponent is one
less t han t he numbe r of stages whi ch are af f ect ed
by adapt at i on.
di fferent i al equat i ons f or the BHL model , up to the
z~ stage is:
6. 1. 2. THE BAYLOR -- HODGKIN -- LAMB MODEL
I n the t r eat ment of t urt l e cone responses, Bayl or
et al . (1974b) modi f i ed t he ori gi nal FH model by
setting
dy, (t )
dt
dyj(t)
dt
- I ( t ) - a y, ( t )
- - - a [Yj_l(t) - y~(t)]
(31)
a, = as = a = 1 / T . (29) dy. (t ) dz, (t )
Several ot her kinetic schemes were f ound t o fit the
wavef or ms of cone responses bet t er (Bayl or et al . ,
1974a) but t he modi f i ed FH model was chosen
adequat e f or an expanded t heor y of adapt at i on and
responses t oo l arge t o be in t he l i near range. It al so
has a much si mpl er i nt er pr et at i on t han t he FH
model as a chai n of chemi cal react i ons ( compar e
Borsel l i no et al . , 1965, wi t h Bayl or et al . , 1974b).
Fi gure 59 illustrates the model used by Bayl or et al.
(1974b), which we will call t he BHL model .
There are i mpor t ant differences between the BHL
model and t he ori gi nal FH model . Since, in t he
BHL model , t he rat e const ant s f or bui l dup and
decay of t he y subst ance are t he same, t here is no
change in t he gai n when t he val ue of t he rat e
const ant s is changed, as t here is in t he FH model .
Thi s can be seen by consi deri ng t he i mpul se
r esponse of t he first n stages of t he BHL model :
y , (t ) = Q B ( t / T ) " - ' e t / T (30)
dt dt
- a Y n ~( t ) -
{K, 2 + v z , ( t ) } z , ( t ) +
K21
A
{1 + v Z2(t)} z2(t )
dz2(t)
- g , ~ {1 + v z 2 ( t ) } z , ( t ) -
dt
{K,2 [1 + vZ2(t)] + K23}Z~(t).
In t hese equat i ons v is t he aut ocat al yt i c const ant
implicitly defi ned by the equat i on K,2 = /(,2 + vz2.
A is t he equi l i br i um const ant of zx, z2 and is equal
t o K, 2 / K2 , . Thi s is a compl i cat ed set of di f f er ent i al
equat i ons and an i nt ui t i ve feeling of what is goi ng
on is di ffi cul t . Some insight may be gai ned by
exami ni ng a special case of interest: a weak,
si nusoi dal l y modul at ed i ncr ement which pr oduces
a r esponse in t he l i near range. In this case,
where T = 1 / a , and B is a const ant .
I n this case t he peak of Yn is at ( n- 1) T and t he
magni t ude of t he peak is i ndependent of T. Gai n
cont r ol cannot be achi eved in this model si mpl y by
an i ncrease of t he rat e, a. Ther ef or e, t he BHL
model has t o have a new f eat ur e, an ext r a pat hway
f or decay of t he fi nal st age of t he cascade where
t he decay rat e depends on t he level of i l l umi nat i on.
Thi s is shown in Fig. 59 as t he pat hway denot ed z, ,
z,, z3, z,. z, is equi val ent t o Yn and is assumed t o
be t he concent r at i on of " bl ocki ng par t i cl es" which
lead t o closing of t he sodi um channel s in t he
phot or e c e pt or ' s membr ane. The decay of z, t o the
next state, z2, is subj ect t o a u t o c a t a l y s i s by the level
of z2 present (see Fig. 59). Thus, t he syst em of
/ (t ) = Io + I, e i~t
yj ( t ) = Yjo + Yil ei~'
z~(t) = Z~o + z~le ~t.
(32)
We make t he a ppr oxi ma t i on t hat 0>>, and t hat
Io, t he mean level of i l l umi nat i on which ma y al so
be vi ewed as t he mean arri val r at e of light quant a,
is l arge c ompa r e d t o t he rat e const ant s of t he
cascade. Then we obt ai n [cf. equat i on (40) of
Bayl or et al. (1974b)] f or the cone' s f r equency
r esponse in t he light adapt ed range:
z , , ( c o ) y . l ( c o )
I , ( o ~ ) I , ( c o )
where T = l / a
(33
1
+ A
1 + io~B2
B, = [g,2 + K2,]/[K23"K,2]
Bz = 1/{J~2,[1 + vlo/(Kz3K,2)]}
A = K,2/K2,.
Thus, t he BHL model predi ct s no ef f ect of light
adapt at i on in t he limit of high f r equency. Thi s is
qual i t at i vel y in agr eement with t he measur ement s
of t he cone' s i mpul se response by Bayl or and
Hodgki n (1974). They f ound t hat t he rising phase
of t he i mpul se response was not af f ect ed by
backgr ound level. Thi s result is also qual i t at i vel y
in agr eement with Kel l y' s (1972) psychophysi cal
dat a on t he l i neari t y of high f r equency response in
h u ma n vi s i on. Re c e nt di r e c t i n t r a c e l l u l a r
measur ement s of t he f r equency responses of t urt l e
hor i zont al cells also conf i r m this pr edi ct i on of t he
BHL t heor y ( Tr anchi na, Gor don and Shapl ey
unpubl i shed).
Not i ce t hat t he f r equency response of t he cone
consists of t hr ee t erms, t he first t wo of which are
stages of t empor al i nt egr at i on whi ch are i ndepen-
dent of t he mean level, Io. The onl y place where io
enters in t he expressi on f or t he cone' s light adapt ed
frequency response is in the time const ant B~ in t hi rd
t er m of equat i on (33). Thi s t er m has t he f or m of
t he f r equency response of a negative feedback l oop
whi ch has a gai n A and t i me const ant B2. The t i me
const ant of the feedback is what is affect ed by mean
level in t he BHL model . As Bayl or et al. (1974b)
demonst r at ed, this coul d account qual i t at i vel y f or
t he ef f ect of backgr ounds on t he gai n and t i me
course of t he cone' s i mpul se response [the Four i er
t r ans f or m of t he f r equency response in equat i on
(33)]. However , as i ndi cat ed above in Fig. 53, t he
predi ct ed gain vs backgr ound curve is st eeper t han
t he real dat a, while t he dependence of t he t i me t o
peak of t he response on mean level is t oo shallow.
In a l at er paper , concer ni ng t oad rods, Bayl or et
al. (1980) pr oposed t hat f eedback t o earlier stages
of processi ng, r at her t han t o j ust t he last stage as
in t he BHL model , woul d pr ovi de a bet t er fit t o t he
dat a. However , t he t heor y of such a system has not
been anal yzed and woul d cert ai nl y be mor e
compl i cat ed t han t he BHL model .
A very i mpor t ant consequence of t he BHL model
is t hat t he amplitudes of responses t o high t empor al
frequenci es of modul at i on are unaf f ect ed by mean
level. This can be seen in equat i on (33) in t he limit
as co~oo. Then t he onl y t er m whi ch cont ai ns Io
appr oaches t he val ue uni t y, and it does so at l ower
values of co t han t he ot her t er ms appr oach zero.
6.1.3. ENROTH-CUGELL AND SHAPLEY'S MODEL OF
ADAPTATION IN GANGLION CELLS
Anot her scheme f or obt ai ni ng Weber ' s Law
behavi or linked t o dynami c changes is di agr ammed
in Fig. 60 ( Enr ot h- Cugel l and Shapl ey, 1973a). In
this model f or t he rod-dri ven retinal net wor k of t he
cat , t he r od signal is subj ect ed t o a mul t i pl i cat i ve
gai n cont r ol at t he level of t he r o d - b i p o l a r
synapse. In t he original model it was pr oposed t hat
t he f eedback signal which mul t i pl i ed t he r od signal
was pr oduced by t he hor i zont al cell. Lat er wor k
reviewed above indicates r at her t hat t he f eedback
signal may arise in bi pol ar cells. In any case t he
f or mal expressi on of t he model is:
r(t ) = P(t)/exp{H(t)/Htrig}
P( t ) = f ~ ( t - t ' ) p ( t ' ) dt '
p ( t ' ) = g - ( t ' / r , ) 3 exp { - t ' / x p }
H( t ) = f ~ r ( t - t ' ) h ( t ' ) dt '
h ( t ' ) = exp ( - - t ' / TH) .
(34)
Wher e r(t ) is t he r od signal t o t he bi pol ars, H( t )
is t he hor i zont al cell pot ent i al (now t hought of as
t he bi pol ar cell' s pot ent i al ) and T. is t he t i me
const ant of t he f eedback neur on. Htri, is a critical
level this signal must exceed, Tp is t he t i me const ant
of t he r od, I ( t ) is t he light stimulus, P( t ) is t he
phot ocur r ent of t he r od, ~ is t he gai n in t he dark.
The f r equency response of this model has been
wor ked out and it is (Enrot h-Cugel l and Shapl ey,
1973a):
3 3 4 R . M . SHAPLEY AND C. ENROTH- CUGELL
r,(o)
- g-exp { - r o / H t r i g }
l,((o)
(35)
n
: E p j ( t )
j = o
f l T t 4 ~ 1 t
+ i o) + l ' n t rig
1 + i m ' r n . ~
where ro is the st eady state value of r ( t ) . In t he
model , ro appr oxi mat el y increases like log Io f or
g-Io>>H~r~g. Two feat ures are not ewor t hy. The
general " s h a p e " of t he f r equency r esponse
resembles t hat of the BHL model ' s f r equency
response, equat i on (33). However , t he effect of
mean level on dynami cs is on t he gain of t he
feedback t er m r o H t r i g , rat her t han on the t i me
const ant r,,. Mor eover , t he gain of high f r equency
responses in this model does dr op at high
backgr ounds by t he f act or e x p { - r o / H, ng}, t hat is
appr oxi mat el y r eci pr ocal t o Io in t he hi gh
backgr ound limit. This predi ct i on is not correct f or
single cone responses, but it has not been tested in
t he system for which this model was designed, t he
cat ret i na in t he scot opi c range. Measur ement of
t he t empor al f r equency response of cat retinal
gangl i on cells at several di f f er ent backgr ound or
mean levels woul d be a crucial test of t he di fferent
predi ct i ons of t he BHL model and t he E n r o t h -
Cugell - Shapley model. Prel i mi nary experiments of
this t ype appear t o conf i r m a model of t he BHL
t ype and t o excl ude mul t i pl i cat i ve model s like t he
E n r o t h - Cu g e l l - Shapl ey model (Shapl ey e t a l . ,
1983).
6.1.4. THE CONTRAST GAINCONTROL MODEL
The cont r ast gai ncont r ol adj ust s t he t i me course
of response cont i ngent on t he average level of
cont rast rat her t han simply cont i ngent on t he mean
flux. Shapl ey and Vi ct or (1981) pr oposed a t heor y
f or t he way in whi ch t he t i me course of response
was changed by cont rast , a t heor y which resembles
the BHL model . Thei r model is di agrammed in Fig.
61. Ther e are n stages of t empor al i nt egr at i on and
one negative f eedback stage. The t empor al fre-
quency response of this system is:
n
( t ) = ~ r j ( l )
( t l ~ "-I
r(~ ;; r
e l l ( t )
I
e x
H o t c e l t J
FIG. 60. A model for adaptation in the cat retina. The p(t)s
are the photocurrents in individual rods. The amount of signal
transmission from rods to bipolar and horizontal cells is called
r(t), with subscripts for each rod. H ( t ) is the horizontal cell
potential due to the sum of its inputs. An exponential function
of the horizontal cell's potential is what controls the sensitivity
of receptor transmission. Thus, r(t) =p(t )/exp{H(t )}. From
Enroth-Cugell and Shapley (1973a).
f 1
r~(o)) A 1
- +
11(o) + io 1 +- iwT
(36)
Shapl ey and Vi ct or (1981) f ound t hat increase of
cont rast affect ed onl y the rat i o K / t H and had onl y
negligible affects on A , x~ or n. Formal l y, equat i on
(36) resembles equat i on (33) f or t he BHL model .
The ef f ect of cont r ast is exert ed on t he same t erm,
t he f eedback t erm, and in a r oughl y similar way.
Whet her this similarity of the consequences of these
model s f or i ncrement al responses has any deep
meani ng about mechani sms, it does reveal t hat
functionally t he t wo processes seem t o af f ect t i me
cour se of responses in similar ways.
Not e t hat in none of t hese model s is response
simply a gai n f act or times an unadapt ed signal.
Rat her , in each case, adj ust ment of gai n and
adj ust ment of t i me const ant s, a n d / o r st rengt h of
negative feedback, appear t o be necessary, in or der
t o expl ai n t he associ at i on of gai n and t i me cour se
in t he dat a f r om visual neur ons. The response of
retinal neur ons is t hus a functional of t he light now
and t he past hi st or y of i l l umi nat i on. The ret i nal
f unct i onal is under t he cont r ol of mean level and
mean cont r ast .
FI o. 61. A di a gr a m o f a mode l f or t he way t he c ont r a s t
ga i nc ont r ol modi f i es fi rst or der r e s pons e s o f ga ngl i on cells.
I c is t he c ont r a s t si gnal . The mode l cons i s t s o f a ga i n s t age
A, una f f e c t e d by c ont r a s t , N L st ages o f l ow pa s s f i l t er i ng,
and one stage of high pass filtering. Each low pass stage has
a time constant "r,. The high pass stage is a feedback loop
with one stage with a time constant TH, and with feedback
gain K. Contrast mainly affects K and T H. From Shapley
and Victor (1981).
6. 2. Ret i nal Gai n and Vi sual Sensi t i vi t y
The psychophysi cal consequences of retinal gain
cont r ol , and t he i mpl i cat i ons of psychophysi cal
results about ret i nal gain cont rol s, requi re f or t hei r
i nt er pr et at i on a t heor y linking t he psychophysi cs
and neur ophysi ol ogy of vision. In a previ ous
publ i cat i on (Enrot h-Cugel l and Shapley, 1973b) we
suggested a sket ch of such a t heor y and here will
make it explicit.
The aims of t he t heor y are: (i) t o show how gain
and noise i nt eract in det ermi ni ng sensitivity in r od
vision; (ii) t o show how t he dependence of gain
setting on receptive field size can be used t o explain
t he observed spatial effect s on t he psychophysi cal
laws of light adapt at i on (Barl ow, 1957, 1965; van
Nes and Bouman, 1967; Koender i nk et al. 1978).
In our proposed model , psychophysical t hreshol d
is pr esumed t o be gover ned by a signal-to-noise
rat i o. The signal is pr esumed t o be t he neural
response of a population of ret i nal gangl i on cells;
t he noise is t he vari abi l i t y of firing in t hose cells.
The signal is subj ect t o gain cont r ol which is
supposed, in t he t heor y, t o behave in t he way t hat
t he retinal gain cont rol has been observed t o behave
in cat ret i nal gangl i on cells. We pr esume t hat t here
are a few (at least) ret i nal spatial channel s at any
par t i cul ar ret i nal locus. We post ul at e t hat r od and
cone signals are i ndependent , in t hei r noise
gener at i on and in t hei r gain cont r ol , unt i l late in
the retinal stages of signal processing. Rod and cone
pat hways must have i ndependent dar k noises, and
di f f er ent dar k adapt ed gains. Ther e are t wo mai n
f act or s which det er mi ne t he sensitivity of gangl i on
cells: gain and noi se (Barl ow and Levi ck, 1969;
Rose, 1948). Fr om wor k cited above, t he gai n of
a gangl i on cell' s response t o a step of light on a
backgr ound in t he scot opi c range, G R is:
G R = GRO/(1 + FB/FRo) P (37)
where GR0 is t he dar k adapt ed gain, FB is t he
backgr ound fl ux effect i vel y absor bed, FRO is t he
cri t eri on amount of flux which must be exceeded
t o t ur n on t he gain cont r ol of t he r od pat hway, and
P is an exponent , usually measured t o be 0.9, which
we will appr oxi mat e t o 1 (Cl el and and Enr ot h-
Cugell, 1970; Enr ot h- Cugel l and Shapl ey, 1973a).
The noise will be t he dar k noise summed t oget her
with t he backgr ound fl ux over t he recept i ve field.
Thus the variance o 2 of the noise f r om the r od pat h-
way in a gangl i on cell' s act i vi t y will be
oR 2 -- [ a d "(FB + FRo)]
FRD = IRD fl l t
FB = IB " A,
(38)
Wher e IB is t he backgr ound ret i nal i l l umi nat i on,
A, is t he summi ng area of t he gangl i on cell cent er,
FRD is t he dar k noise in t he r od pat hway (in
equi val ent quant a s-X). It is assumed t hat t he
psychophysical threshold will be reached when the
cell's si gnal - noi se ratio reaches 4. Thus, if Is is
the retinal illumination of a light stimulus and As
is its area in squared degrees, then:
In the scotopic range we can make the approxima-
tion that
FB < < FCD < Fc0 ( 44)
4 = I s " A s " ( GR) / OR (39)
Solving for the threshold stimulus illumination, one
obtains:
Thus,
Gc ~ Gco
and, oc 2 ~ Gco 2 F c o .
(45)
1 s = 4 OR/ [ A s GR]
= 4 . [GR = ( F . + F R D ) ] ' / 2 / [ A s I GR o / ( 1 +
F B I F . o ) } ] . (40)
In order to obtain the correct value for the (Weber)
scotopic contrast sensitivity, which approximately
equals 10, one can calculate that
Oc = Gco FCD ' ' 2 = 0.02 FRO (46)
When FB, the background flux, is small, the
threshold is approximately constant depending only
on the values of the dark adapted gain GR0 and the
dark noise FRD. However, as FB becomes large
compar ed to FRD, the t hreshol d becomes
proportional to Fa 1/2. That is, it follows the square
root law. This happens even though the retinal gain
is dropping like 1/(1 + FB/ FRo ) , because the
variance of the noise is dropping also, being
proport i onal to FB-' when FB becomes large
compared to FRO. In order to obtain Weber' s Law
one must put a clamp on the noise; it cannot keep
declining in variance as the retinal gain declines.
Indeed, as Barlow and Levick (1969) and
Derrington and Lennie (1982) have found, the noise
at the ganglion cell does not decline as the gain
declines. How can this be so? One idea is that noise
from the c o n e p a t h w a y is added into the ganglion
cell, and is more or less unaffected by changes of
gain in the rod pathway. Thus, if we change
equation (39) to include cone pathway noise with
variance Oc 2 we obtain
4 = I s A s " GR/ ( OR 2 + OC2) ' / 2 (41)
where
OC 2 = Gc2[FB + FCD ] ( 42)
and in analogy with the rod pathway:
Gc = Gc0 (1 + F B / F c o ) . (43)
Since we found FRO tO be equivalent to 3000
phot on absorptions s-' , this would mean the cone
dark noise would have to produce a variance of
about 60 phot on events s-' at the ganglion cell, a
106 / ~ t
0 I deg .
J . / /
1 0 4 0 5
o
k - 1 0 3
2 x l O -5 2 x l O -4 2 x i O 3 2 x l O -2 2 x l O -I 2 2 0 Tr ol onds
I 0 I 02 103 I 04 105 106 107
I B G ( q / d e g 2 s e c )
FXG. 6 2 . T h e p r e d i c t i o n s o f a t h e o r y o f l i g h t a d a p t a t i o n
concerning the effects of stimulus area on the slope of the
increment threshold curve. The curves are the predicted
increment threshold behaviour for retinal ganglion cells which
have the areas indicated in the figure. The psychophysical
data plotted for comparison are: empty circles from Barlow's
(1957) data for a 19 deg 2 target, filled circles for Barlow's
(1957) 0.0077 deg 2 target, and crosses for Aguilar and Stiles'
(1954) 64 deg z target. See text.
not - unr easonabl e number whi ch must be checked
experi ment al l y in t he f ut ur e.
Not i ce t hat , in this model , t he dar k noises and
t he cri t eri on fluxes f or t he t ur ni ng on of t he gain
cont r ol are distinctly di f f er ent . Thi s is in accor d
with actual measurement s on ganglion cells (Enrot h-
Cugell and Shapl ey, 1973a; Barl ow, 1977) whi ch
show cl earl y t hat t he dar k light is t oo small t o
account f or the behavi or of t he gain vs backgr ound
relationship. A di fferent f undament al const ant , t en
t o one hundr ed times l arger t han t he dar k noise
must be hypot hesi zed.
The poi nt of t he model is reveal ed in Fig. 62
whi ch shows predi ct i ons of t he model f or t he
i ncrement t hreshol d curves of t wo types of cell, one
with a small cent er and one with a l arger cent er.
The cells' sensitivities are pl ot t ed on t he same
coor di nat es as psychophysi cal dat a f r om Agui l ar
and Stiles (1954) and Barl ow (1957) whi ch exhi bi t
characteristic steep and shallow slopes, respectively.
Cl earl y, t he model account s adequat el y f or t he
t ransi t i on f r om square r oot t o Weber behavi or
cont i ngent on t arget size. It provi des a way t o
under st and why this t r ansi t i on is a f unct i on of t he
square of the spatial frequency of a sinusoidal target
(van Nes and Bouman, 1967). It also provi des a
f r amewor k with whi ch t o under st and why noise
sometimes controls sensitivity and why, under ot her
ci rcumst ances, t he gain det ermi nes sensitivity.
7. RETROSPECTI VE AND CONCLUSI ON
We have considered t he " wh y " , the " wh a t " , and
t he " h o w" of visual adapt at i on, and even at t emp-
t ed t o say " wh e r e " and " wh e n " it t akes place. At
t he out set we demons t r at ed how aut omat i c
adj ust ment of ret i nal gain woul d cause bri ght ness
c o n s t a n c y u n d e r d i f f e r e n t c o n d i t i o n s o f
illumination, by maki ng retinal responses dependent
on cqnt rast . Then we exami ned what happens t o
t he visual per f or mance of humans under di f f er ent
condi t i ons of backgr ound or mean level of
i l l umi nat i on. In this section, we poi nt ed out t hat
" n o i s e " f r om t he stimulus may somet i mes limit
per f or mance, and t hat at ot her times ret i nal
adapt at i on det ermi nes t he limits of sensitivity. The
vi sual r es pons es o f r et i nal ga ngl i on cel l s,
particularly cat ganglion cells, as a funct i on of mean
337
or backgr ound level, were consi dered next. In these
cells, gain cont r ol seems t he domi nant f act or in
limiting t hei r capaci t y t o detect stimuli as t he mean
level of i l l umi nat i on varies. The rel at i on of this
wor k t o human vision, where bot h gain and
" n o i s e " seem significant, is an open quest i on f or
f ut ur e research. In seeking t o answer t he quest i on,
" wh e r e " t he gain cont r ol is l ocat ed, we next
consi dered what is known about adapt at i on in
retinal i nt erneurons. Then we reviewed the t opi c of
adapt at i on in phot orecept ors. Finally, we discussed
some t heori es of how t he gain of ret i nal neur ons
is cont r ol l ed, and how such a gain cont r ol mi ght
cont r i but e t o visual per f or mance.
Ther e are several neural gain cont rol s in t he
ret i na. Surpri si ngl y, what evidence we have about
t he t i me course of gain r educt i on af t er an increase
in mean i l l umi nat i on, t oget her with t he change in
response t i me cour se with change in gain, suggests
t hat all these gain cont r ol s share t he pr oper t y of
at t enuat i ng t he component s of response t o slow
var i at i on of t he st i mul us, and spar i ng t he
component s of t he response t o rapi d vari at i ons of
t he stimulus light. However , t he di f f er ent gain
cont r ol s do seem t o have di f f er ent spat i al
i nt egrat i on areas, and this allows one t o distinguish
t hem.
Fut ur e wor k is requi red t o establish t he answer
t o " wh e r e " in t he ret i na some of t he gain cont r ol s
live. However , it will be even mor e i mpor t ant t o
di scover or i nvent model s f or " h o w" t he gain
cont rol s manage t o make t he ret i na except i onal l y
sensitive t o cont r ast and yet insensitive t o large
swings in t he mean level.
A P P E N D I X 1 - - R E T I N A L N E U R O N S
The details of ret i nal ci rcui t ry var y f r om species
t o species al t hough many of t he general principles,
at least in hi gher mammal s, are t he same. Much of
what we have wri t t en about t he physi ol ogi cal
mechani sms of ret i nal adapt at i on stems f r om
experi ment s on t he cat ret i na and any f r ui t f ul
consi der at i on of these mechani sms requi res some
familiarity with retinal funct i onal connectivity. The
bri ef comment s about retinal circuitry which follow
draw heavily on t he detailed studies of the cat retina
under t aken over t he past t en years or so ( f or
338
summar y see Sterling, 1983).
I nf or mat i on in the vert ebrat e retina flows mainly
in a r adi al di rect i on f r om the receptors, in the out er
ret i na, t he r od and cone cells, t hr ough bi pol ars
t owar ds gangl i on cells in t he i nner ret i na, with
lateral interaction in bot h pl exi form layers, and with
feedback within and bet ween layers.
Increasing t he amount of light t hat falls on
vertebrate receptors causes the inside of the receptor
cell t o become mor e negative. That is, ver t ebr at e
receptors respond t o light by h y p e r p o l a r i z i n g . Since
t ransmi t t ers are released in response t o neur on
depol ari zat i on it must be concl uded t hat vert ebrat e
recept ors release t he maxi mum amount of t hei r as
yet uni dent i fi ed t r ansmi t t er or t ransmi t t ers in
complete darkness. Direct evidence for this has been
obt ai ned by Schacher e t al. (1974) in the frog retina,
and by Ripps e t al. (1976) in t he skate ret i na, using
horseradi sh peroxi dase ( HRP) upt ake as a measure
of synapt i c vesicle t ur nover .
Rod signals leave t he r od cell' s di st ri but i ng end
f or one t ype of bi pol ar cell while cone signals leave
t he di st ri but i ng end of t he cone cells f or ot her
bi pol ar cells. The st at ement t hat t he cat has r od
bi pol ars and cone bi pol ars means onl y t hat at
present t here is no a n a t o mi c a l evi dence t hat bot h
rods and cones cont act t he same bi pol ar cell (Kolb
e t al. 1981). This does not necessarily mean t hat rod
and cone signals are strictly separated in the bi pol ar
layer. For example, Nelson (1977) f ound t hat mixed
rod - cone signals t ravel in some cone bi pol ars (see
also Nel son, 1980).
Structurally, t here is onl y one kind of r o d bi pol ar
in the cat, one t hat receives signals in invaginations
of the proxi mal surface of t he r od spherules. Ther e
are two structurally different kinds of cone bipolars:
the invaginating ones which cont act cones in pits
in the proxi mal surface of cone pedicles while ot her
cone bi pol ars onl y f or m superficial cont act s with
the pedicle bases. These are t he " f l a t " cone
bi pol ars. It seems t hat all r ecept or cells in t he cat
do not " t a l k " to bi pol ars in exact l y t he same
language because t he ul t rast ruct ural synaptic
specializations are not t he same in the r od and cone
pits as in t he cont act s bet ween t he base of t he cone
pedicles and t he flat cone bi pol ar dendri t es
(Sterling, 1983), suggesting t hat t he mode of signal
transmission is di fferent in the t wo types of synapse.
This is also consistent with the recent physiological
wor k of Saito e t al. (1979) in t he carp ret i na which
suggests t hat rods and cones af f ect f undament al l y
di fferent ionic channels in their respective bipolars.
Al t hough, as far as is known, all vert ebrat e
recept ors r espond t o light by hyperpol ari zi ng, t he
same does not hol d t rue f or all bi pol ar cells. This
has been known since 1969 when Werbl i n and
Dowl i ng showed t hat some mudpuppy bi pol ars
hyper pol ar i ze whi l e ot her s depol ar i ze when
i l l umi nat ed. Nel son and co-workers (Nelson and
Kol b, 1982) have r ecor ded i nt racel l ul arl y f r om
anatomically identified bipolars in the cat retina and
t hey f ound t hat in t he cat ret i na t oo some bipolars
hyperpolarize while others depolarize when the light
level is increased.
It is in t he i nner pl exi f or m l ayer ( I PL) t hat t he
t hi rd or der neur ons, t he gangl i on cells, communi -
cate with ot her ret i nal cells. Two feat ures of this
connect i vi t y are of special interest. First, some
ganglion cells' dendri t i c trees are l ocat ed within t he
a-l ami na of t he I PL where t hey receive i nf or mat i on
f r om t hose bipolars whi ch ext end onl y as far as t he
a-lamina. Ot her ganglion cell dendritic trees branch
out in t he b-l ami na of t he I PL and are fed by
bi pol ars whose di st ri but i ng end ext ends t o t he b-
l ami na. One of t he maj or recent achi evement s
wi t hi n r et i nal a n a t o my - p h y s i o l o g y is t he
demonst r at i on by Fami gl i et t i and co-workers
(Famiglietti e t al . , 1977; Nelson e t al . , 1978) t hat
when bi pol ars and gangl i on cells talk t o each ot her
in l ami na-a of t he i nner pl exi f or m layer, t he
gangl i on cell is of t he of f - cent er t ype, i.e. an
i ncrement of i l l umi nat i on within t he cent er of the
gangl i on recept i ve field (see Appendi x 2) causes it
to become hyperpol ari zed. But when t he t wo talk
to each ot her in l ami na-b t he gangl i on cell is of t he
on-cent er t ype, i.e. it depol ari zes in response to
increased illumination of the receptive field center.
Sterling (1983) and his colleagues have f ound t hat
at least t wo di fferent types of bi pol ar cells converge
on each retinal gangl i on cell of t he mor phol ogi cal
class called bet a (Boycot t and W~issle, 1974), which
is equi val ent t o t he funct i onal class, X. Thus each
of f - cent er X gangl i on cell receives direct synaptic
i nput f r om one kind of flat cone bi pol ar and an
i nvagi nat i ng cone bi pol ar, as well as indirect i nput
f r om r od bipolars. A similar state of affai rs applies
t o on-cent er X cells: t wo cone bi pol ar direct inputs,
and an indirect r od bi pol ar i nput . Ther e are thus
several cone bi pol ar t ypes, since on- and of f - X cells
each recei ve i nput f r om t hei r own speci al
invaginating bi pol ars, and t hei r own special t ype of
fl at bi pol ar (Sterling, 1983).
Lat er al spread of signals wi t hi n t he ret i na is
i mpor t ant f or adapt i ve mechani sms. Lat er al
i nt er act i on is possible al r eady at t he r ecept or cell
level. In t he cat t here are gap j unct i ons bet ween
pedicles of i ndi vi dual cone cells and also bet ween
rod-spherul es and processes ext endi ng f r om cone-
pedicles (see e.g. Nel son e t al . , 1981). Nel son (1977)
has demonst r at ed t hat i ndi vi dual cat cones receive
r od signals whi ch pr esumabl y ent er vi a t he
r o d - c o n e gap j unct i ons. To what ext ent t he
c o n e - c o n e j unct i ons also represent f unct i onal
cont act s in t he cat is not known at present and we
are not aware t hat anybody has shown t hat t he cat
ret i na has any f unct i onal or anat omi cal r o d - r od
cont act s, but , in some col d- bl ooded vert ebrat es,
funct i onal coupl i ng bet ween rods via gap j unct i ons
is a pr omi nent f eat ur e (e.g. Det wi l er e t al . , 1980).
The mor e distal of t he t wo l at eral l y spreadi ng
neur on t ypes is t he h o r i z o n t a l cel l of whi ch t he cat
has t wo kinds ( Boycot t , 1974; Boycot t e t al . , 1978).
The t ype A and t ype B cell bot h have a soma and
a dendri t i c ar bor i zat i on in whi ch all synapt i c
cont act s are with c o n e s . The t ype B cell in addi t i on
has a l ong, ver y t hi n ( pr obabl y non-i mpul se
carryi ng) axon whi ch leaves t he soma- dendr i t e
compl ex and at a distance of about hal f a millimeter
" e xpl ode s " i nt o an el abor at e ar bor i zat i on whi ch
cont act s onl y r o d s . In t he cat, hor i zont al cells onl y
hyperpol ari ze t o increases in illumination, and most
receive bot h cone and r od signals f r om phot o-
r ecept or s (St ei nberg, 1971; Ni emeyer and Gour as,
1973; Nel son e t a L, 1975).
The ot her i nt er neur ons whi ch medi at e lateral
i nt eract i on are t he amacri ne cells which spread their
processes in t he inner pl exi form layer. The amacrine
cell f ami l y is made up of at least t went y- t wo
di f f er ent types in t he cat ret i na, as distinguished by
dendritic branchi ng pat t erns in t he I PL (Kolb e t aL,
1981). The most well studied of these cells is t he Al l
amacr i ne cell whi ch receives di rect synapt i c i nput
f r om r od bi pol ars in l ami na-b of t he I PL, and gap-
j unct i on cont act s f r om cone-bi pol ars in l ami na-b
also. It also receives cone bi pol ar i nput f r om
synapses in lamina-a. So far onl y r od bipolars which
hyper pol ar i ze t o i ncrement s of light have been
descri bed (Nelson, 1980) and yet AI I amacri nes
depol ari ze t o i ncrement s, suggesting t hat t he
r o d - b i p o l a r t o AI I amacr i ne synapse is sign-
i nvert i ng. AI I amacri nes make synapt i c cont act
ont o pr es umed of f - c e nt e r (i . e. d e c r e me n t -
exci t at ory) gangl i on cells, whi ch suggests t hat t he
synapse between t he AI I and the off-cent er ganglion
cell is sign-inverting also. None of t he ot her
amacri ne cells' connect i vi t y is as well charact eri zed
as t hat of t he AI I cell, yet cert ai n feat ures of t hei r
st ruct ure are not ewor t hy. As in ot her species, t here
are numer ous amacr i ne ~ amacr i ne synapt i c
cont act s in t he I PL of t he cat ret i na. Fur t her mor e,
t here is a preferent i al i nput of amacri ne cells t o Y
gangl i on cells, while t her e is much mor e di rect
bi pol ar i nput t o t he X cells (Kol b, 1979; Sterling,
1983). Since most is known about t he processes of
ret i nal adapt at i on in t he X and Y gangl i on cells in
t he cat, t he similarities and di fferences in t hei r
anat omi cal connect i ons are i mpor t ant f or under -
st andi ng t he site in t he ret i na where ret i nal
adapt at i on t akes place.
One of the curious features of retinal mor phol ogy
is t hat t here appears t o be onl y one r od bi pol ar t ype
compar ed t o several cone bi pol ar types (Sterling,
1983). Since recept i ve field or gani zat i on is j ust as
rich in t he scot opi c range as in t he phot opi c, one
mi ght have expect ed as much anat omi cal el abor-
at i on of t he r od bi pol ar f ami l y as of t he cone
bi pol ars. Because of t he great degree of r od - cone
i ndependence, we guess t hat r o d - c o n e coupl i ng
(Nel son, 1977) is of s econdar y i mpor t ance.
However , Sterling (1983) believes t hat r o d - cone
coupl i ng is t he mai n pat hway f or r od i nput t o
gangl i on cells over most of t he scot opi c range. This
is not really a cont r over sy, since bot h our view and
Sterling' s are equally speculative at present. The AII
amacri ne, whi ch gets its pr edomi nant i nput f r om
r od bi pol ar cells, couples into the phot opi c circuitry
when it makes gap j unct i ons with t he cone bi pol ar
cells in l ami na-b of t he I PL. The AI I amacr i ne
seems t o be a crucial link in scotopic receptive fields.
One of t he most i nt erest i ng i nt er neur ons in t he
retina is t he i nt erpl exi form cell (Boycot t et al . , 1975;
Kol b and West, 1977; Nakamur a e t al . , 1980). This
neur on is per haps t he most likely candi dat e t o be
i nvol ved in gain cont r ol in t he ret i na. It has
dendri t i c arbori zat i ons in t he I PL, where it receives
synapses f r om amacr i ne cells of so-far i ndet er-
340 R . M. SHAPLEY AND C. ENROTH- CUGELL
I P L
b
C B o 1
~ a 2
~ ~ All
~ F ~ G ON-Beta G
I l l , o N
FIG. 63. Di a gr a m o f connect i ons i n t he i nner pl exi f or m l ayer o f t he cat r et i na f r om serial EM r econs t r uct i ons . Chemi cal
s ynaps es ar e i ndi cat ed by t he ar r ows : gap j unc t i ons ar e i ndi cat ed by t he s ymbol -I . CB i ndi cat es a cone bi pol ar cell; f our
subt ypes are labeled. RBP s t ands f or r od bi pol ar cell. Al l is a subcl ass of amacr i ne cells. The Bet a gangl i on cells are pr es umed
t o be t he anat omi cal equi val ent of t he X cells. The i nner pl exi f or m l ayer is subdi vi ded i nt o s ubl ami nae- a a nd -b, as i ndi cat ed
i n t he f i gur e. On gangl i on cells recei ve i nput in s ubl a mi na - b, whi l e o f f gangl i on cells recei ve i nput in s ubl a mi na - a . Fr o m
St erl i ng (1983).
mi nat e t ype. Then t he i nt er pl exi f or m cell makes
synapses on all t ypes of bi pol ar cells at t he level of
t he I PL but mor e especially at the level of t he out er
pl exi f or m layer ( OPL) . It is t he perfect exampl e of
a f eedback neur on. Mor eover , it coul d af f ect all
bi pol ars which is a pr oper t y one woul d want f r om
a gain cont r ol since on- and of f - pat hways must be
adapt ed in t he same way in or der t o keep cont r ast
sensitivity const ant . However , t he wide t ermi nal
br anchi ng of t he i nt er pl exi f or m cell in t he OPL is
a pr obl em i f this cell is t o pl ay a role in regulating
gain on st eady backgr ounds, because, at least f or
X cells, t he area of t he ret i na over which adapt i ve
signals are summed for the center is less t han 1 deg 2,
i.e. less t han 200 /a by 200/ a. However , t here is
evidence f or a di f f er ent kind of gain cont r ol which
depends on stimulus cont r ast r at her t han average
flux (see Sect i on 3.8; Shapl ey and Vi ct or, 1978; cf.
Werbl i n and Copenhagen, 1974) and perhaps the
i nt erpl exi form cell' s propert i es may mat ch t hose of
this ot her gain cont r ol .
A schematic di agram of the neur onal circuitry in
t he cat ' s I PL, where gangl i on cells receive t hei r
i nput s, is of f er ed in Fig. 63, f r om a recent review
article (Sterling, 1983).
APPENDI X 2 - - RECEPTI VE FI ELDS
The neural signal which leaves the ret i na consists
of trains of impulses carri ed by t he axons of retinal
ganglion cells. The response of these cells t o a visual
stimulus may be defi ned as a change in the rat e of
firing of impulses. An adequat e stimulus t o cause
such a change in firing is some change in the
i l l umi nat i on on t he ret i na. The wor k of Har t l i ne
(1940), Barl ow (1953), and Kuf f l er (1952, 1953)
showed t hat each retinal gangl i on cell generat ed
responses, as defi ned above, t o st i mul at i on over a
limited area of t he retina, and this area was defi ned
as the receptive field of t hat ganglion cell. Wor ki ng
in t he cat retina, Kuffl er (1953) f ound t hat ganglion
cell recept i ve fields consisted of t wo concent ri c
zones which he called t he center and surround. The
cent er and sur r ound were mut ual l y antagonistic. In
on-cent er cells in which the center caused excitatory
VISUAL ADAPTATION AND RETINAL GAIN CONTROLS 3 4 1
ON-CENTER
RECEPTIVE FIELD
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r f f ~- ]
F- - - ' q
III1 IIIIIIIII I I
I l l l I l l l l l l l l I I
~ l - - - - " q
I I I I I I IIIIIII I l l l l
I I I I I I IIIIIII IIIII
FIG. 64. Schemat i c r epr es ent at i on o f t he mu t u a l a nt a goni s m
bet ween cent er a n d s u r r o u n d i n on a n d of f - cent er cells. I n
on- cent er cells ( a, b, c) , a n i nc r e me nt i n t he cent er i ncr eases
t he cell' s fi ri ng rat e while an i ncr ement o f l i ght i n t he s ur r ound
decreases t he firing rate. Wh e n t he t wo i ncr ement s are appl i ed
t oge t he r in s ync hr ony, as i n (c), t he r e s pons e t o l i ght " o n "
is l ess t h a n i n (a) a n d t he r e s pons e t o l i ght " o f f " is l ess t h a n
i n (b). Thi s me a n s t he t wo r egi ons ar e mut ua l l y ant agoni s t i c.
I n of f - cent er cells ( d, e, f ) , t he cel l s' r e s pons e pa t t e r n at l i ght
" o n " i n t he cent er a nd i n t he per i pher y ar e r ever sed, but t he
mu t u a l a n t a g o n i s m is t he s a me .
responses t o increments of light, the sur r ound
woul d cause i nhi bi t ory responses t o increments. In
off-cent er cells in which the central region was
inhibitory during an increment, the surround would
be excitatory during an increment. The on- and off-
center cells and their cent er-surround organi zat i on
are illustrated in Fig. 64.
Rodi eck (1965) made a maj or advance by
developing a model for the cat gangl i on cell
receptive field in terms of overlapping center and
sur r ound mechani sms. Each mechani sm may be
conceived of as the receptors and i nt erneurons, the
signals of which are pool ed t oget her to influence
the firing of the gangl i on cell. Wi t hi n the center
mechanism all light evoked signals generated within
the pool of these receptors and i nt erneurons are
summed, according t o the model , and similarly for
the surround. Then center and surround signals are
summed at the gangl i on cell. The signals f r om
di fferent positions within each pool are weighted
by what Rodi eck called the "sensi t i vi t y pr of i l e",
and which we will refer t o as the "spat i al
distribution of gai n". The center has its own narrow
spatial di st ri but i on of gain, and the surround has
a rat her broader spatial di st ri but i on. Rodi eck
proposed t hat these t wo spatial di st ri but i ons could
be appr oxi mat ed by Gaussi an surfaces wi t h
di fferent extents of spread. The spatial resol ut i on
and opt i mal spatial t uni ng of retinal gangl i on cells
can be rat i onal i zed in terms of Rodi eck' s model
(Enrot h-Cugel l and Robson, 1966). The spatial
resol ut i on of the cell is due t o the finite size of the
center, and in fact can be predicted from knowledge
of the magni t ude of the spread of the cent er' s
Gaussian spatial distribution of gain (Cleland et eL,
1979; So and Shapley, 1979; Linsenmeier et el. ,
1982). Figure 65 shows the Rodi eck model for the
receptive field of cat retinal gangl i on cells.
~
R-MECHANISM
__ ~ D - M E C H A N I S M
C ~ " E N ' I - - - I 1 " - - ~ I ' , ~
SURROUND
j _ L
RESPONS~ ~
CENTER TYPE NO RESPONSE ON-OFF TYPE
RESPONSE RESPONSE
FIG. 65. The t wo spat i al l y over l appi ng me c h a n i s ms i n t he
Rodi eck mode l o f r et i nal ga ngl i on cell r ecept i ve fi el ds. I n
t he s ket ch at t he t op, t he hor i zont al axi s r epr es ent s di s t ance
on t he r et i na. The hei ght s o f t he t wo cur ves r epr es ent t he
ga i n o f t he cent er a n d o f t he s u r r o u n d , as l abel ed, as a
f unc t i on o f pos i t i on on r et i na. Bot h ar e Ga us s i a n f unc t i ons
o f posi t i on; t he cent er ' s Ga us s i a n has a nar r ower spr ead t ha n
t he s u r r o u n d ' s . The cent er a nd s u r r o u n d ha ve oppos i t e si gn
i n t hi s model . Thi s r esul t s i n mu t u a l a n t a g o n i s m. I n t hi s
mode l t he cent er a nd s u r r o u n d c o mp o n e n t s c ombi ne by
s i mpl e addi t i on, i . e. l i near l y. Th u s , r e s pons e t o s t i mul a t i on
a nywhe r e wi t hi n t he fi el d i s, accor di ng t o t he model , s i mpl y
a s u m o f t he cent er a n d s u r r o u n d c o mp o n e n t s i n r e s pons e
t o t he s t i mul us , as is i l l ust r at ed i n t he f i gur e. Fr o m Rodi eck
(1973).
SURROUNO TYP~
RESPONSE
342
There are several ganglion cell classes in each
vertebrate retina (see Rodieck, 1979). This is a
significant complication, because not all of these
cell types conform to the simple elegance of the
Rodieck model. As far as we know, the ganglion
cell classes in the cat retina which have the highest
contrast gain are the X and Y cells discovered by
Enroth-Cugell and Robson (1966). While X cells do
behave in a way approximately predictable from the
Rodieck model, Y cells exhibit nonlinear summation
of visual signals (Enroth-Cugell and Robson, 1966;
Hochstein and Shapley, 1976a, b). It seems that
while X cells have two pools or mechanisms as in
Rodieck's model, Y cells have at least three different
types of neuronal mechanism. The new type of
mechanism is what Hochstein and Shapley have
dubbed the "nonlinear subunits", small spatial
pools within which neural signals are summed in
a linear manner, but between which a nonlinearity
is interposed before signal summation. There have
been several excellent reviews of the physiology and
anatomy of cat ganglion cells (Robson, 1975;
Rodieck, 1979; Lennie, 1980; Wfissle, 1982; Levick
and Thibos, 1983, among others).
Ac k n o wl e d g e me n t - - We t ha nk our col l eagues in New Yor k a nd
Eva ns t on for hel pf ul c omme nt s a nd cri t i ci sm dur i ng t he wri t i ng
of t hi s review paper . We t h a n k Dr . E. N. Pu g h for hi s hel pf ul
advi ce. For per mi s s i on t o cite unpubl i s he d wor k we t ha nk Dr s.
J. Gor don, T. Har di ng, E. Kapl an, P. Lenni e, and D. Tr anchi na.
Pr epar at i on of this chapt er has been partially suppor t ed by gr ant s
f r om t he Nat i onal I nst i t ut es of Heal t h: RO1 EY 01472, and ROI
EY00206.
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