Exp Brain Res (2008) 186:131–141
DOI 10.1007/s00221-007-1216-5
R ES EA R C H A R TI CLE
Auditory-motor and cognitive aspects in area 8B of macaque
monkey’s frontal cortex: a premotor ear–eye Weld (PEEF)
C. Lucchetti · M. Lanzilotto · L. Bon
Received: 15 June 2007 / Accepted: 6 November 2007 / Published online: 24 November 2007
© Springer-Verlag 2007
Abstract In previous reports, we showed the involvement
of area 8B neurons in both spontaneous ear and eye move-
ment and in auditory information processing. Audition-
related cells responded to complex environmental stimuli,
but not to pure tones, and their activity changed during
visual Wxation as a possible inhibitory expression of the
engagement of attention. We observed auditory, auditory-
motor and motor cells for both eye and ear movements.
This Wnding suggests that area 8B may be involved in the
integration of auditory input with ear and eye motor output.
In this paper, we extended these previous studies by exam-
ining area 8B activity in relation to auditive orienting
behaviour, as well as the ocular orientation (i.e., visual Wxa-
tion) studied previously. Visual Wxation led to inhibition of
activity in auditory and auditory-motor cells, which sug-
gests that attention may be involved in both, maintaining
the eye position and reducing the response of these cell
types. Accordingly, during a given task or natural behav-
iour, spatial attention seems to aVect more than one sensori-
motor channel simultaneously. These data add to our
understanding of how the neural network, through a two-
channel attentive process, accomplishes to switch between
two eVectors, namely eyes and ears. Considering the func-
tional, anatomical and cytoarchitectonic diVerences among
the frontal eye Weld (FEF), the supplementary eye Weld
(SEF) and area 8B, we propose to consider area 8B as a
separate premotor ear–eye Weld (PEEF).
C. Lucchetti · M. Lanzilotto · L. Bon (&)
Department of Biomedical Sciences Section of Physiology
and Animal Facilities Centre Section of Policlinic,
University of Modena and Reggio Emilia,
Via Campi 287, 41100 Modena, Italy
e-mail: bon.leopoldo@unimore.it; bonleo@unimo.it
Keywords Premotor cortex · 8B Auditory · Attention ·
Eye movement · Ear movement · Monkey
Introduction
In macaque monkeys, area 8B is located anterior to the ros-
tral part of the dorsal agranular area six(Walker 1940).
Anatomical investigations showed the presence of complex
connections between dorsal prefrontal areas, including area
8B, and other cortical areas (Barbas and Mesulam 1981;
Barbas and Pandya 1989; Barbas et al. 1999; Luppino et al.
2003). Moreover, area 8B sends projections to the deep lay-
ers of the superior colliculus, pretectum and nucleus reticu-
laris tegmentum ponti (NRTP) (Schmahmann and Pandya
1997; Fries 1984; Tanila et al. 1993). Quantitative studies
have established the basis of inhibitory interactions
between prefrontal areas nine and ten and inhibitory neu-
rons in superior temporal cortices involved in auditory per-
ception (Barbas et al. 2005), and these principles are likely
to apply to areas 8B as well.
Evidence of evoked eye and ear movements has been
found in the frontal cortex, particularly in the frontal eye Weld
(FEF area 8A), the supplementary eye Weld (SEF) and area
8B (Bruce et al. 1985; Schlag and Schlag-Rey 1987; Mitz
and Godschalk 1989; Bon and Lucchetti 1992; Tehovnik and
Lee 1993; Stepniewska et al. 1993; Bon and Lucchetti 1994;
Schall 1991; Preuss et al. 1996; Tehovnik and Sommer
1997). Unit activity has been studied in areas 9, 8A, and 8B
and in SEF in relation to both auditory stimuli and eye/ear
motor control (Vaadia et al. 1986; Schlag and Schlag-Rey
1987; Bon and Lucchetti 1994; Russo and Bruce 1994;
Schall 1991; Fuster et al. 2000; Bon and Lucchetti 2006).
In this paper, we show the presence of auditory-motor
and motor neurons in area 8B, and the eVect of the
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132
engagement of attention in visual Wxation task on neurons
showing auditory-motor characteristics.
Methods
Behavioural methods
Three macaque monkeys (Macaca fascicularis) were con-
ditioned for two visuomotor tasks: (1) a visual Wxation task
and (2) a visually guided saccade task. Preliminary training
was performed with the apparatus mounted on the mon-
key’s home cage. Each monkey learned to press a bar to
illuminate a bicolored (red/green), light-emitting diode
(LED, SIEMENS LS110). The LEDs, with a diameter of
0.05°, were placed 114 cm in front of the monkey. After a
random time period (0.5–5.0 s), the LED turned from red to
green for a Wxed period of time (0.5 s). Because the animal
then had to release the bar during the green period to
receive a liquid reward, the task required Wxation of the red
LED. After the monkey learned to perform the Wxation task
in the cage, it was taught to sit in a primate chair inside a
Faraday cage and to perform the same task in this new con-
dition. When its performance reached a very good level
(80–90% correct responses), it was trained in the saccade
task. In this task, several LEDs could become red sequen-
tially before the last one turned green. Each LED switched
on simultaneously with the oVset of the previous LED. As
in the Wxation task, the animal had to release the bar during
the green period to receive a liquid reward, so the monkey
needed to Wxate each red LED as it illuminated. An audi-
tory white-noise stimulus marked the start and the end of
the task, between which the animal was free to begin the
trials at will. The trial was aborted if the animal made an
extra saccade.
After the monkeys learned to perform the saccade task,
they were prepared for the eye position measurement and
painless head restraint. After a week, the monkeys were
trained with their head Wxed in place until they performed
85–95% of the saccade-task trials successfully.
The unit activity was recorded under two experimental
conditions: (a) auditory stimuli in spontaneous conditions
and (b) auditory stimuli during visual Wxation.
The saccade task was only used to test the presence of
visually guided saccade cells.
With the animal sitting in the primate chair, diVerent
auditory stimuli were presented: (1) single tones generated
by an electronic piano; (2) a single tone followed by
delivery of a liquid reward after a delay of 150 m s (tone-
reward); and (3) environmental stimuli, such as the experi-
menters’ voices shouting a single word, opening and
closing of doors, scraping of feet, scraping of the laboratory
chairs, footsteps towards and away from the animal, Wnger
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Exp Brain Res (2008) 186:131–141
or pen drumming. We also generated unusual auditory
stimuli such as hammering, the pulling suspenders sound,
knocking of glass, voice of an unknown human and animal
vocalizations. All auditory stimuli were recorded previ-
ously and reproduced by four loudspeakers, positioned
100 cm to the right and to the left of the animal, two in front
and two behind the animal at 45° angles versus the inter-
hemispheric line. The auditory stimulation was produced
on the left or right side or on both sides. The environmental
and unusual stimuli were produced during the experiments
with or without loudspeaker ampliWcation. The volume of
auditory stimuli was measured with a sound level meter
(Larson Davis 824): the white-noise ranged between 40 and
50 dB while the environmental stimuli ranged between 65
and 85 dB. We could modulate the volume of the white-
noise in relation to the intensity of auditory stimuli.
The Wnal test involved generation of the same auditory
stimuli while the animal performed the Wxation task and
only during Wxation of the LED. The auditory stimulus was
produced while the LED was red, after the eye reached the
target. This test enabled us to verify whether engaging the
animal’s attention on the red LED, as it awaited the change
to green, modiWed the activity of audition-related neurons.
The white-noise was only present when we tested the Wxa-
tion eVect and not in the spontaneous condition.
At the end of the training the animals were prepared for
unit activity recording.
Surgical methods
Using aseptic techniques and under general anaesthesia
(ketamine 10 mg/kg i.m. with 0.1 mg/kg Xylazine, i.m. or
only Zoletil 10 mg/kg i.m.), one hollow stainless steel cyl-
inder was attached to the skull of the animal with four
screws. It was cemented in place to permit a painless Wxa-
tion of the head. A search coil was implanted subconjuncti-
vally (Judge et al. 1980), and two stainless steel wires were
inserted into the neck muscles to monitor the electromyo-
gram (EMG). Finally, a stainless steel chamber for the elec-
trophysiological investigation was implanted over one
hemisphere using stereotaxic coordinates.
Physiological methods and data analysis
Eye movement was recorded by the search coil technique
using the phase detection method (Remmel 1984). The
same technique was used for ear movement, taping a search
coil to the ears of the animal at the start of every experi-
mental session (Jay and Sparks 1987; Bon and Lucchetti
1994). This system allowed us to deWne the beginning and
the end of an ear movement. The noise of the ear signal was
grater than that of the eye signal since the coil was not
Exp Brain Res (2008) 186:131–141
permanently attached to the ear (Populin and Yin 1998). At
the same time, we used a TV infrared system to observe the
movements and behaviour online, and recorded it by a
computer for oVline analysis. The unit activity, the EMG
and experimenters’ voices, were also recorded on video
with an audio mixer. We could thereby measure the timing
between the ear movement and the unit discharge and com-
pare the X and Y signals with the signal observed by both
experimenters both online and oVline with the infrared TV
system. The auditory stimuli were recorded with an ampli-
Wed microphone and the output signals were then used as
markers to study the timing between unit activity and
stimuli. The animals’ attempts to rotate their heads was
monitored by EMG of the neck muscles.
Single neurons were isolated with epoxylite-coated tung-
sten electrodes passed through the dura with a hydraulic
microdrive (Narishige MO-95B). The microelectrode
signal was ampliWed (Bak MDA-4) and passed through a
custom-built band-pass Wlter (500–7,500 Hz) to eliminate
artefacts from the 50 and 75-KHz coil drivers. A SPS
8701E Waveform Discriminator System selected the unit
activity. The eye and ear movements, auditory stimulus, the
bar and LED level, and unit activity were sampled at 1 KHz
and stored by a Macintosh system for oVline analysis, and
we utilized SuperScope II (GWI) software for data acquisi-
tion and analysis.
Two tests were used for the statistical analysis: (1) the
Wilcoxon test to identify diVerences between activity histo-
grams, (2) Student’s t-test to identify diVerences in peak
discharge for a population of neurons, in diVerent experi-
mental conditions.
In addition, to estimate the maximum rate of discharge
better, we generated unit activity density (UAD) by a
Gaussian Wlter (
= 50 m s) (Kass et al. 2005), using Rpad
(http://www.Rpad.org).
Electrolytic marking lesions were made by DC current
(10
A for 15 s) at some of the recording sites for histo-
logical reconstruction. At the end of the experiments, under
deep anaesthesia, the animals were perfused with a 0.9%
NaCl solution followed by 5% formalin. Subsequently, the
brain was sectioned at 60
m and stained with thionine.
All phases of the experimental procedure followed the
standards established by the European Community and Ital-
ian law (D.L. 116/92). The project was approved by the
Italian National Superior Institute of Health and received
the authorization of the Italian National Ministry of Health.
Results
Previous data showed the involvement of area 8B in eye
and ear motor control and in auditory functions. SpeciW-
cally, one previous report pointed out that area 8B is
133
involved in ear and eye motor control (Bon and Lucchetti
1994), and a second report showed that its auditory neurons
discharge for environmental auditory stimuli, but not for
pure tones (Bon and Lucchetti 2006). The results presented
here follow up the second paper, based on cells recorded in
the same experimental sessions.
As described previously, our approach was ecological.
The auditory stimuli were those habitually produced in a
laboratory and were not linked with an operantly condi-
tioned auditory task. The animal produced the ear and eye
movements spontaneously or in response to an environ-
mental auditory stimulus. The purpose of the additional
analysis presented here was to verify two issues: (a) is this
area involved in orienting movements of both ears and eyes
and not only in spontaneous motor behaviour? (b) Does the
engagement of attention, during visual Wxation task, modu-
late the discharge of auditory-motor neurons as in auditory
neurons?
We recorded the activity of 139 neurons in three male
macaque monkeys (Macaca fascicularis) in three hemi-
spheres. Thirty-two neurons of 139 were described in a pre-
vious paper (Bon and Lucchetti 2006). The remaining
neurons (107) were studied in relation to environmental
auditory stimuli and to eye and ear movement. In this study,
we did not Wnd neurons discharging strictly in relation to
visual Wxation or to visually guided saccades. We did not
Wnd any systematic diVerences in the response as a function
of the type of auditory stimulus.
Fig. 1 Reconstructed map of auditory-motor and motor cells. Top left
representation of the stimulation studies of Levinsohn (1909). Top
centre cytoarchitectonic map of Walker (1940). Top right representation
of the stimulation and recording study of Bon and Lucchetti (1994)
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134 Exp Brain Res (2008) 186:131–141

Fig. 2 Example of sensory dis-

charge of an auditory-motor cell.
The auditory discharge is
evoked by voice and drumming
but is very weak with scraping.
Raster: each dot is one spike.
HIS unit activity histogram.
UAD unit activity density. Bin
width: 50 m s

Fig. 3 Example of auditory-

motor cell. a These cells are
active for auditory environmental
stimuli, for orienting saccades,
and orienting ear movement.
b In spontaneous condition the
discharge is synchronized nei-
ther with saccades nor with ear
movement. Raster: each dot is
one spike. HIS unit activity
histogram. UAD unit activity
density. Bin width: 50 m s

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Exp Brain Res (2008) 186:131–141
Fig. 4 Example of auditory-motor cell. These cells are active for audi-
tory environmental stimuli and for orienting saccades Raster: each dot
is one spike. HIS unit activity histogram. UAD unit activity density.
Bin width: 50 m s
Fig. 5 Example of auditory-motor cell. These cells are active for audi-
tory environmental stimuli and for orienting ear movement. Raster:
each dot is one spike. HIS unit activity histogram. UAD unit activity
density. Bin width: 50 m s
Additionally, the discharge of these neurons showed a
rapid adaptation.
We identiWed the following cell types: auditory-motor
cells (39%, 42/107), motor cells (28%, 30/107), complex
behaviour cells (5%, 5/107) and indeWnable cells (28% 30/
107). The diVerent cell types were intermingled in the pen-
etrations and recording locations (Fig. 1).
135
Fig. 6 Example of motor cell. These cells are correlated to ear move-
ment. In this example, we can see a relationship to ear movement and
a diVerent tonic discharge in relation to the ear position. PX horizontal
ear component, PY vertical ear component, U unit activity, each bar is
one spike. Raster: each dot is one spike. HIS unit activity histogram.
UAD unit activity density. Bin width: 50 m s
Cells that showed activity synchronized with the onset of
auditory stimuli and with the onset of an orienting saccade
and/or orienting ear movement were deWned as “auditory-
motor”. For the sensory aspects of neural activity, the unit’s
discharge rates could modulate in relation to one or more
types of environmental stimuli (Fig. 2). With some stimuli,
this activity was very weak and showed rapid adaptation.
Most cells were active for contralateral auditory stimuli.
For the motor aspects of neural activity, we found three
diVerent types of neuronal behaviour. The discharge of 10
of 42 auditory-motor cells was synchronized with the onset
of orienting movements of both the eye and the ear (Fig. 3).
Three of these 42 cells showed activity correlated only with
the onset of orienting eye movement, and 29, activity corre-
lated only with the onset of orienting ear movement
(Figs. 4, 5). Of these 42 cells, none showed activity correla-
tion with spontaneous as opposed to orienting eye and ear
movement (Fig. 3).
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136 Exp Brain Res (2008) 186:131–141

Fig. 7 Example of complex

cell. The auditory stimulus
inhibits the cell discharge in
relation to ear position.
PX horizontal ear component,
PY vertical ear component,
U unit activity, each bar is one
spike, AS auditory stimulus.
Raster: each dot is one spike.
HIS unit activity histogram,
UAD unit activity density.
Bin width: 50 m s

Fig. 8 Example of auditory-

motor cell in spontaneous condi-
tion and during visual Wxation.
In spontaneous condition, the
activity is brisk for both auditory
stimulus and ear movement,
while during visual Wxation task
the discharge is weak for both
auditory stimulus and ear move-
ment. Raster: each dot is one
spike. HIS unit activity histo-
gram, UAD unit activity density.
Bin width: 50 m s

The cells that did not show activity synchronized with
the onset of auditory stimulus, but only with orienting ear
movements, were deWned as motor cells. The motor cells
showed phasic, tonic and phasic-tonic activity. An example
of phasic-tonic activity is presented in Fig. 6, where we can
see a phasic discharge related to orienting ear movement
and a tonic discharge in relation to ear position. These cells
sometimes showed a directional selectivity, forward and
backward, and only a few cells discharged for oblique,
upward and downward movements.
In the Wve “complex behaviour” cells, the discharge was
inhibited by an auditory stimulus only when the ear was in
a posterior position (Fig. 7).
Of the remaining 30 “indeWnable” cells, 8 cells showed
activity related to eye movement that was self-initiated dur-
ing the interval between 2 auditory stimuli. These cells

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Exp Brain Res (2008) 186:131–141
Fig. 9 Population analysis of 11 auditory-motor cells inXuenced by visual Wxation. Top auditory component, bottom motor component
might be considered “checking-saccade” neurons as previ-
ously described by us (Bon and Lucchetti 1992; Bon and
Lucchetti 1994). Of these 30 cells, ten cells responded only
once to novel visual stimuli (mirror, diVerent cans, objects
in general) and 12 cells discharged for an experimenter’s
body or for a white coat presented on a stick. Tanila et al.
(1992) found visual neurons with similar characteristics in
the prefrontal cortex.
These data answer positively to our Wrst issue.
To answer our second issue, 20 auditory ear-motor cells
were tested while the animal performed a visual Wxation in
primary position in which their attention was engaged.
Eleven auditory-motor cells, related only to orienting ear
movement, showed a signiWcantly lower activity level, in
both their auditory and motor components, when auditory
stimuli were presented during the execution of visual Wxation
task, as opposed to when the same stimuli were presented in
spontaneous conditions (Fig. 8) (Wilcoxon test P < 0.001).
For this population of 11 cells, this property is illustrated by
the bipolar chart plot and t-test, showing the statistically sig-
niWcant diVerence between the two experimental conditions
for both auditory (t = 7.93, P = 0.0001) and motor (t = 10.35,
P = 0.0001) components. The scatter plot shows that a linear
regression for both auditory (r = 0.80) and motor (r = 0.84)
components describes the neuronal activity (Fig. 9).
The remaining nine cells tested did not show a signiWcant
decrease or increase in activity, for either auditory stimuli
and orienting ear movements, when visual Wxation task activ-
ity was compared to spontaneous conditions (Fig. 10)
(Wilcoxon test P < 0.1). The diVerence between the two
experimental conditions was not statistically signiWcant for
137
both auditory (t = ¡0.20, P = 0.8367) and motor (t = 0.04,
P = 0.9679) components. The scatter plot shows that a linear
regression for both auditory (r = 0.70) and motor (r = 0.97)
components describes the neuronal activity well (Fig. 11), as
was the case for the 11 cells with signiWcant diVerences
between the visual Wxation task and the spontaneous condi-
tions (Fig. 9). In this set of experiments, we tested these
eVects while the monkey maintained active Wxation at the
primary central location, considering it a neutral eye position,
and did not test the role of eccentric eye position on auditory-
motor cells (GiVord and Cohen 2004).
These second parts of the results show how the engage-
ment of attention during visual Wxation task aVects the
behaviour of auditory-motor neurons in area 8B.
Discussion
If we observe the natural behaviour of a cat pointing to a rat
and at the same time we produce a sound by scraping our
feet, we can see two diVerent reactions: the animal main-
tains gaze towards the rat and orients its ears towards the
auditory stimulus, or the animal orients both gaze and ears
towards the auditory stimulus. Our previous reports indi-
cated that area 8B is involved in ear–eye motor control and
in the auditory perception of environmental auditory stim-
uli. Other studies, carried out in the lateral belt area and in
the core of the auditory cortex, showed neurons with dis-
charge that was related to complex stimuli, vocalizations,
and to faces and conspeciWc vocalizations (Rauschecker
et al. 1995; Recanzone 2000; Ghanzanfar et al. 2005).
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Fig. 10 Example of auditory-motor cell in spontaneous condition and
during visual Wxation. In spontaneous condition, the activity is brisk
for both auditory stimulus and ear movement, and during visual Wxa-
tion task the discharge is always sustained for both auditory stimulus
and ear movement. Raster: each dot is one spike. HIS unit activity
histogram, UAD unit activity density. Bin width: 50 m s
As in our previous studies (Bon and Lucchetti 1994,
2006), in this study our approach was ecological. The
auditory stimuli were those habitually produced in a lab-
oratory. The animal produced ear and eye movements
spontaneously or in response to an auditory stimulus. The
animals were trained for only two tasks: visual Wxation
and visually guided saccade. Two issues are relevant in
the present report, to build on our previous ones: the
presence of auditory-motor and motor cells types, and the
inhibitory eVect of visual Wxation on auditory-motor
cells.
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Exp Brain Res (2008) 186:131–141
Auditory-motor neurons are both sensory and motor
neurons in nature. These neurons discharge in response to
environmental auditory stimuli, and also show a repertoire
of motor integration with two eVectors: ear and/or eye.
Motor cells are unresponsive to auditory stimuli and dis-
charge only in relation to ear movement. With the current
approach, the animal was neither instructed to recognise an
auditory stimulus nor to locate its source with its ear or eye
in order to receive a reward. Consequently, we could not
test if the recorded cells were able to discriminate between
two diVerent auditory stimuli or if they were spatially
tuned. However, without any behavioural constraints
imposed by operant conditioning, these auditory-motor
cells were speciWc for environmental auditory stimuli and
the animals oriented their gaze, in a natural behaviour, turn-
ing their ears towards a stimulus presented in front of them
or behind them. Accordingly, the neural activity could reX-
ect a general aspect of orienting that involves the spatial
localization of an acoustic stimulus.
According to present results, and results in non-human
and human primates, area 8B may be involved in the recog-
nition of auditory stimuli and in the orienting processes
(Romanski et al. 1999; Rao et al. 1997; Alain et al. 2001).
In addition, the activation of speciWc environmental audi-
tory stimuli and the presence of auditory-motor and com-
plex cells suggest that area 8B has an important place in the
hierarchical organisation of the auditory system (Kaas and
Hackett 2000; Wessinger et al. 2001).
The second issue of importance in the present results is
the inhibitory eVect of visual Wxation on the activity of
auditory-motor cells, as well as on the activity of the audi-
tory cells, as previously described (Bon and Lucchetti
2006). Some considerations are necessary to explain the
prevalent inhibitory eVect that the visual Wxation task has
on auditory-motor neurons. Consonant results were found
in the superior colliculus of the cat, when two visual stim-
uli were presented at the same time (Rizzolatti et al. 1974)
and when visual Wxation inhibited the auditory response
(Populin and Yin 2002). Moreover, a similar eVect has
been found in the superior colliculus and in the posterior
parietal cortex of the macaque monkey for visual and audi-
tory peripheral stimuli (Bell et al. 2003; GiVord and Cohen
2004; Cohen et al. 2005). In the experiments of Rizzolatti
et al. (1974), carried out with curare, both stimuli were
visual. The authors explained the inhibitory eVect as a con-
sequence of orienting attention. Our experimental
approach is similar to that of Bell et al. (2003), since one
stimulus is visual and the other is auditory. The inhibitory
eVect on neural discharge of auditory-motor cells might be
a consequence of the engagement of attention during
visual Wxation. This issue may be the expression of a com-
bination of a covert orienting of attention relative to eye
position (i.e., nonfoveal locations), similar to the classic
Exp Brain Res (2008) 186:131–141
Fig. 11 Population analysis of nine auditory-motor cells uninXuenced by visual Wxation. Top auditory component during visual Wxation, bottom
motor component during visual Wxation
consideration of Cherry (1953), and an overt orienting of
attention relative to ear orientation. Accordingly, it seems
that attention may aVect more than one channel at the same
time during a conditioned task or during natural behaviour
(Turatto et al. 2004). The involvement of attention in the
gaze and ear motor control is also in agreement with the
premotor theory of attention (Rizzolatti and Craighero
1998).
All together, its functional characteristics and anatomi-
cal connections suggest that area 8B is part of the inhibitory
network for the gaze shift and ear orienting. Therefore, we
propose to call area 8B the “premotor ear–eye Weld”
(PEEF). In our previous report (Bon and Lucchetti 1994),
we said that this area “may be considered a rostral exten-
sion of supplementary eye Weld (SEF) or a diVerent region”.
Cytoarchitectonic, anatomical and functional consider-
ations now make it more reasonable to consider area 8B as
a separate Weld: PEEF.
There is a debate about whether area 8 (area 8A plus 8B)
should be treated as a premotor or a prefrontal area. In
macaque monkeys the cytoarchitecture of area 8B may be
considered a transitional area between the granular area 9,
rostrally, and the rostral part of the dorsal agranular area 6
caudally (Walker, 1940; Von Bonin and Bailey 1947;
Matelli et al. 1991). Pandya and Yeterian (1985) used the
term “premotor” to include both, areas 8 and 6. Subse-
quently, other authors also treated area 6 and 8 as premotor
cortex (Mann et al. 1988; Passingham 1993; Bon and
Lucchetti 1994; Lucchetti et al. 1998). In addition, the cyto-
architecture of area 8B diVers from the granular area 8A
139
(FEF), located latero-caudally to it in the prearcuate region
(Barbas and Mesulam 1981; Petrides and Pandya 1994).
Transneuronal transfer of rabies virus and a functional
imaging study clearly show that area 8B is involved with
SEF in eye motor control (Moschovakis et al. 2004).
Area 8B is reciprocally connected with the auditory cor-
tex (Barbas and Mesulam 1981; Barbas and Pandya 1989),
receives projections from the dentate nucleus of cerebellum
via the thalamus, much like FEF (Lynch et al. 1994;
Middleton and Strick 2001), and projects to the superior
colliculus, also like FEF (Fries 1984). Recent anatomical
studies show that area 8B sends robust projections to (SEF)
(Luppino et al. 2003; Wang et al. 2005), to an even greater
extent than those from area 8A (FEF).
The neural activity of area 8B is prevalently related to
ear or to ear–eye movement and to auditory environmental
stimuli (Bon and Lucchetti 1994, 2006). In contrast, the
neural activity of SEF is related to eye movement, eye Wxa-
tion, ear and neck movements (Schlag and Schlag-Rey
1987; Bon and Lucchetti 1991; Bon and Lucchetti 1992;
Tehovnik et al. 2000; Chen and Walton 2005), auditory
stimuli (Schall 1991) and attentional processes (Bon and
Lucchetti 1997). Neural activity in the FEF is related to eye
movement, neck movement, auditory and visual stimuli and
attentional processes (Schall 1997).
The microstimulation of area 8B predominantly evoked
small Wxed-vector saccades and ear movement, as well as
ear–eye movement (Levinsohn 1909; Bon and Lucchetti
1994). The microstimulation of SEF predominantly evoked
goal-directed saccades and, in a few penetrations, also ear
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140
movements (Tehovnik et al. 2000). In contrast, microstimu-
lation of FEF evoked small Wxed-vector saccades in the
inferior part, and large Wxed-vector saccades in the superior
part (Bruce et al. 1985).
Taking these results together, the principal diVerence
between area 8B and SEF/FEF is that the neurons in area
8B are rarely related to saccades and visual Wxation, and
they are more related to ear movement. Moreover, microsti-
mulation of area 8B predominantly evokes an activation of
ear muscles or a coactivation of ear and eye muscles.
Accordingly, considering the functional diVerences
between area 8B and both the SEF and FEF (area 8A), as
well as the diVerences in cytoarchitecture and anatomical
projections, we propose to call the area 8B: PEEF.
Acknowledgments We wish to thank Dr. Steven Wise for English
revision, Dr. Marcello Manfredi for volume measurements,
Prof. Rodolfo Cecchi prorector University of Modena and Reggio-
Emilia for his support for this type of research and for improvements
in animal housing, Dr. Vasco Lolli and Mr. Vincenzo Molino for ani-
mal care. Grants were provided by University of Modena and Reggio
Emilia, Foundation Cassa di Risparmio of Modena and PRIN 2005.
References
Alain C, Arnott SR, Hevenor S, Graham S, Grady CL (2001) “What”
and “Where” in the human auditory system. Proc Natl Acad Sci
USA 98:12301–12306
Barbas H, Mesulam MM (1981) Organization of aVerent input to sub-
divisions of area 8 in the rhesus monkey. J Comp Neurol
200:407–431
Barbas H, Pandya DN (1989) Architecture and intrinsic connections of
the prefrontal cortex in the rhesus monkey. J Comp Neurol
286:353–375
Barbas H, Ghashghaei H, Dombrowski SM, Rempel-Clower NL
(1999) Medial prefrontal cortices are uniWed by common connec-
tions with superior temporal cortices and distinguished by input
from memory-related areas in the rhesus monkey. J Comp Neurol
410:343–367
Barbas H, Medalla M, Alade O, Suski J, Zikopoulos B, Lera P (2005)
Relationship of prefrontal connections to inhibitory systems in
superior temporal areas in the rhesus monkey. Cereb Cortex
15:1356–1370
Bell AH, Corneil BD, Munoz DP, Meredith MA (2003) Engagement
of visual Wxation suppresses sensory responsiveness and multi-
sensory integration in the primate superior colliculus. Eur J Neu-
rosci 18:2867–2873
Bon L, Lucchetti C (1991) Behavioural and motor mechanisms of
dorsomedial frontal cortex of macaca monkey. Int J Neurosci
60:187–193
Bon L, Lucchetti C (1992) The dorsomedial frontal cortex of the
macaca monkey: Wxation and saccade-related activity. Exp Brain
Res 89:571–580
Bon L, Lucchetti C (1994) Ear and eye representation in the frontal
cortex, area 8b, of the macaque monkey: an electrophysiological
study. Exp Brain Res 102:259–271
Bon L, Lucchetti C (1997) Attentional-related neurons in the supplemen-
tary eye Weld of the macaque monkey. Exp Brain Res 113:180–185
Bon L, Lucchetti C (2006) Auditory environmental cells and visual Wx-
ation eVect in area 8B of macaque monkey. Exp Brain Res
168:441–449
123
Exp Brain Res (2008) 186:131–141
Bruce CJ, Goldberg ME, Bushnell MC, Stanton GB (1985) Primate
frontal eye Welds: II. Physiological and anatomic correlates of
electrically evoked eye movements. J Neurophysiol 54:714–734
Chen LL, Walton MMG (2005) Head movement evoked by electric
stimulation in the supplementary eye Weld of the rhesus monkey.
J Neurophysiol 94:4502–4519
Cherry EC (1953) Some experiments on the recognition of speech with
one and with two ears. J Acust Soc Am 25:975–979
Cohen YE, Russ BE, GiVord III GW (2005) Auditory processing in the
posterior parietal cortex. Behav Cogn Neurosci Rev 4:218–231
Fries W (1984) Cortical projections to the superior colliculus in the
macaque monkey: a retrograde study using horseradish peroxi-
dase. J Comp Neurol 230:55–76
Fuster JM, Bodner M, Kroger JK (2000) Cross-modal and cross-tem-
poral association in neurons of frontal cortex. Nature 405:347–
351
Ghazanfar AA, Maier JX, HoVman KL, Logothetis NK (2005) Multi-
sensory integration of dynamic faces and voices in rhesus monkey
auditory cortex. J Neurosci 18:5004–5012
GiVord III GW, Cohen YE (2004) The eVect of a central Wxation light
on auditory spatial responses in area LIP. J Neurophysiol
91:2929–2933
Jay MF, Sparks DL (1987) Sensorimotor integration in the superior
colliculus. II. Coordinates of auditory signals. J Neurophysiol
57:35–55
Judge SJ, Richmond BJ, Chu FC (1980) Implantation of magnetic
search coil for measurement of eye position: an improved method.
Vision Res 20:535–538
Kaas JH, Hackett TA (2000) Subdivision of auditory cortex and pro-
cessing streams in primates. Proc Natl Acad Sci USA 97:11793–
11799
Kass RE, Ventura V, Brown EN (2005) Statistical Issue in the analysis
of neuronal data. J Neurophysiol 94:8–25
Levinsohn G (1909) Uber die beziehungen der grosshirnrinde beim
aVen zu den bewegungen des auges. Graefes Arch Clin Exp Oph-
thalmol 71:313–378
Lucchetti C, Lui F, Bon L (1998) Neglect syndrome for aversive stim-
uli in a macaque monkey with dorsomedial frontal cortex lesion.
Neuropsychologia 36:251–257
Luppino G, Rozzi S, Calzavara R, Matelli M (2003) Prefrontal and
agranular cingulate projections to the dorsal premotor areas F2
and F7 in the macaque monkey. Eur J Neurosci 17:559–578
Lynch JC, Hoover JE, Strick PL (1994) Input to the primate frontal eye
Weld from the substantia nigra, superior colliculus, and dentate nu-
cleus demonstrated by transneuronal transport. Exp Brain Res
100:181–186
Mann SE, Thau R, Schiller PH (1988) Conditional task-related re-
sponses in monkey dorsomedial frontal cortex. Exp Brain Res
69:460–468
Matelli M, Luppino G, Rizzolatti G (1991) Architecture of superior
and mesial area 6 and adjacent cingulate cortex in the macaque
monkey. J Comp Neurol 311:445–462
Middleton FA, Strick PL (2001) Cerebellar projections to the prefron-
tal cortex of the primate. J Neurosci 21:700–712
Mitz AR, Godschalk M (1989) Eye-movement representation in the
frontal lobe of rhesus monkeys. Neurosci Lett 106:157–162
Moschovakis AK, Gregoriou GG, Ugolini G, Doldan M, Graf W,
Guldin W, Hadjidimitrakis K, Savaki HE (2004) Oculomotor
areas of the primate frontal lobes: a transneuronal transfer of
rabies virus and [14 C]-2-deoxyglucose functional imaging study.
J Neurosci 24:5726–5740
Pandya DN, Yeterian EH (1985) Architecture and connections of cor-
tical association areas. In: Peters A, Jones EG (eds) Association
and auditory cortices. Plenum, New York, pp 3–61
Passingham R (1993) In: The frontal lobes and voluntary action.
Oxford Psychology Series NO 21
Exp Brain Res (2008) 186:131–141
Petrides M, Pandya DN (1994) Comparative architectonic analysis of
the human and the macaque frontal cortex. In: Boller F, Grafman
J (eds) Handbook of neuropsychology, vol 9. Elsevier, Amster-
dam, pp 17–57
Populin LC, Yin TCT (1998) Pinna movements of the cat during sound
localization. J Neuroscience 18:4233–4243
Populin LC, Yin TCT (2002) Bimodal interactions in the superior col-
liculus of the behaving cat. J Neurosci 22:2826–2834
Preuss TM, Stepniewska I, Kaas JH (1996) Movement representation
in the dorsal and ventral premotor areas of Owl monkeys: a micr-
ostimulation study. J Comp Neurol 371:649–676
Rao SC, Rainer G, Miller EK (1997) Integration of what and where in
the primate prefrontal cortex. Science 276:821–824
Rauschecker JP, Tian B, Hauser M (1995) Processing of complex sounds
in the macaque non primary auditory cortex. Science 268:111–114
Recanzone GH (2000) Spatial processing in the auditory cortex of the
macaque monkey. Proc Natl Acad Sci USA 97:11829–11835
Remmel RS (1984) An inexpensive eye movement monitor using the
scleral coil technique. IEEE Trans Biomed Engin BME
31(4):388–390
Rizzolatti G, Craighero L (1998) Spatial attention: mechanisms and
theories. In: Sabourin M, Craik F, Robert M (eds) Advances in
psychological science: biological and cognitive aspects, vol 2.
Psychological Press, Francis & Taylor, pp 171–198
Rizzolatti G, Camarda R, Grupp LA, Pisa M (1974) Inhibitory eVect of
remote visual stimuli on visual responses of cat superior collicu-
lus: spatial and temporal factors. J Neurophysiol 37:1262–1275
Romanski LM, Bates JF, Goldman-Rakic PS (1999) Auditory belt and
parabelt projections to the prefrontal cortex in the rhesus monkey.
J Comp Neurol 403:141–157
Russo GS, Bruce CJ (1994) Frontal eye Weld activity preceding aurally
guided saccades. J Neurophysiol 71:1250–1253
Schall JD (1991) Neuronal activity related to visually guided saccadic
eye-movements in the supplementary motor area of Rhesus mon-
keys J. Neurophysiology 66:530–558
Schall JD (1997) Visuomotor areas of the frontal lobe in cerebral cor-
tex. In: Rockland KS, Kaas JH, Peters A (eds) Extrastriate cortex
in primates, vol 12. Plenum Press, New York, pp. 527–616
Schlag J, Schlag-Rey M (1987) Evidence for a supplementary eye
Weld. J Neurophysiol 57:179–200
141
Schmahmann JD, Pandya DN (1997) Anatomic organization of the
basilar pontine projections from prefrontal cortices in rhesus
monkey. J Neurosci 17:438–458
Stepniewska I, Preuss TM, Kaas JH (1993) Architectonics, somato-
topic organization, and ipsilateral cortical connections of the
primary motor area (M1) of owl monkeys. J Comp Neurol
330:238–271
Tanila H, Carlson S, Linnankoski I, Lindros F, Kahila H (1992) Func-
tional properties of dorsolateral prefrontal cortical neurons in
awake monkey. Behav Brain Res 47:169–180
Tanila H, Carlson S, Linnankoski I, Kahila H (1993) Regional distri-
bution of functions in dorsolateral prefrontal cortex of the mon-
key. Behav Brain Res 53:63–71
Tehovnik EJ, Lee KM (1993) The dorsomedial frontal cortex of the
rhesus monkey. Topographic representation of saccades evoked
by electric stimulation. Exp Brain Res 96:430–442
Tehovnik EJ, Sommer MS (1997) Electrically evoked saccades from
the dorsomedial frontal cortex and frontal eye Weld: a parametric
evaluation reveals diVerences between areas. Exp Brain Res
117:369–378
Tehovnik EJ, Sommer MA, Chou IH, Slocum WM, Schiller PH (2000)
Eye Welds in the frontal lobes of primates. Brain Res Rev 32:413–
448
Turatto M, Galfano G, Bridgeman B, Umiltà C (2004) Space-indepen-
dent modality-driven attentional capture in auditory, tactile and
visual systems. Exp Brain Res 155:301–310
Vaadia E, Benson DA, Hienz RD, Goldstein MH (1986) Unit study of
monkey frontal cortex: active localization of auditory and of visu-
al stimuli. J Neurophysiol 56:934–952
Von Bonin G, Bailey P (1947) The neocortex of macaca mulatta. Uni-
versity of Illinois Press, Urbana
Walker AE (1940) A cytoarchitectural study of frontal area of the
macaque monkey. J Comp Neurol 73:59–86
Wang YW, Isoda M, Matsuzaka Y, Shima K, Tanji J (2005) Prefrontal
cortical cells projecting to the supplementary eye Weld and pre-
supplementary motor area in the monkey. Neurosci Res 53:1–7
Wessinger CM, Van Meter J, Tian B, Van Lare J, Pekar J, Rauschecker
JP (2001) Hierarchical organization of the human auditory cortex
revealed by functional magnetic resonance imaging. J Cogn
Neurosci 13:1–7
123