Downloaded from www.ajronline.org by 202.69.105.142 on 05/28/13 from IP address 202.69.105.142. Copyright ARRS.

For personal use only; all rights reserved

1309

Pictorial

Essay

..:,

Normal Anatomy of the Hippocampus

and Adjacent
Temporal Lobe: High-Resolution
Fast Spin-Echo MR
Images in Volunteers
Correlated
with Cadaveric
Histologic
Sections
Robert

This
mel

D. Tien,1

essay

Gary

illustrates

hippocampus

and

J. Felsberg,1

the

appearances

adjacent

temporal

and

Barbara

of sections
lobe

Cram2

of the

nor-

on high-resolution

heavily T2-weighted
fast spin-echo
MR images and correlates
them with histologic sections. We found that this MR examination
showed
the detailed
anatomy
of the normal hippocampus
in a
much

shorter

time

than

is possible

with

conventional

spin-echo

techniques.
The information
provided
in this essay can be used
as a baseline
for distinguishing
between
normal and abnormal
hippocampi
in a variety of disease states.

The hippocampus
is an important
structure
in the brain that
is involved
in numerous
diseases.
Visualization
of the hippocampus with MR imaging has therefore
been extremely
useful
in detecting
such pathologic
entities as hippocampal
sclerosis
or atrophy
in patients
with temporal
lobe epilepsy
and Alzheimers disease [1 ]. Although
gross estimates
of hippocampal size and signal abnormality
have clinical value [2], we
think that more precise imaging can help to further delineate
the fine anatomic
detail of the hippocampus
and thus provide
more sensitive
detection
and localization
of lesions in this
structure.
Anatomic
details of the hippocampus
shown on Ti weighted
images (5-mm-thick
sections)
correlate
closely with
anatomic
findings in cadaveric
sections [3]. However,
imaging
can be improved
by using a recently
described
MR pulse
sequence,
fast spin echo, a method that allows acquisition
of

Received March 20, 1992; accepted

after revision June 24, 1992.
1 Department
of Radiology,
Box 3808, Duke University
Medical Center,
2

Department

Durham,

of Pathology. Duke University Medical Center, Durham, NC 27710.

AJR 159:i309-13i3,

December

1992 0361-803X/92/1596-1309

heavily T2-weighted
(long TR/long
TE) images
and largematrix examinations
in clinically acceptable
time periods. With
this technique,
anatomic
detail is improved
because
thin
sections
(2 mm), a high-resolution
matrix (256 x 256), and
four excitations
can be used. In addition,
it may be possible
to detect signal abnormalities
involving
the hippocampus.
We
correlated
the fast spin-echo
images of the hippocampus
and
medial temporal
lobe structures
in eight healthy
volunteers
with histologic
sections
from a normal cadaveric
brain.

Fast Spin-Echo

MR Imaging

in Healthy

Volunteers

MR images
of the brains of eight healthy
young
adult
volunteers
(mean age, 32 years) were obtained
with a 1 .5-T
superconducting
magnet (Signa, General Electric, Milwaukee,
WI). A sagittal localizer sequence
was used first. This generated parasagittal
images through
the long axis of the hippocampus, from which orthogonal
coronal fast spin-echo
images
were prescribed
to cover the entire length of the hippocampus
(Fig. 1 ). Each person was then imaged by using a standard
quadrature
head coil and fast spin-echo
techniques
with the
following
image parameters:
2-mm-thick
sections
with interleave (the minimal slice thickness
in our current fast spin-echo
software),
256 x 256 matrix, 1 8-cm field of view, 4000/i 00/
4 (TR/TE/excitations)
sequences,
echo train length of 16, and

NC 2771 0. Address reprint requests to A. D. Tien.

American Roentgen Ray Society

Downloaded from www.ajronline.org by 202.69.105.142 on 05/28/13 from IP address 202.69.105.142. Copyright ARRS. For personal use only; all rights reserved

1 3i 0

TIEN

Fig. 1.-Drawing

bic system.

shows

Hippocampus

left lateral

(green)

view

of lim-

is located

in

medial temporal
lobe and has an arclike configuration ending in region of splenium
of corpus callosum. Fimbria of hippocampus
(yellow),
which is
formed
by alveus,
in turn becomes
fornix (yellow)
at level of hippocampal
tail. Amygdala
(blue)
is
immediately
rostral to hippocampal
head.

ET AL.

AJR:159,

December

1992

Fig. 2.-A and B, Histologic

section
(A) through anterior hippocampal
head (Hh) and corresponding
slightly anterior fast spin-echo coronal MR image (B). Gray matter of hippocampal
head is inferior to
temporal horn; gray matter of amygdala
(A) is superior
and anterior to hippocampal
head. Lateral
aspect of hippocampal
head is limited by temporal
horn; medially,
entorhinal
cortex (cc) can be
identified within parahippocampal
gyrus.

Fig. 3.-A
hippocampal

and B, Histologic
section (A) through
head (Hh) slightly posteriorto
Fig. 2A
and corresponding fast spin-echo coronal MR image (B). Hippocampal
head can be seen consistently on MR by identification
of hippocampal
digitations,
which give a characteristic
waviness
to
hippocampus
at this level. Hippocampal
head is
separated from gray matter of amygdala
(A) (mid
to posterior portions) by temporal
horn. Note subiculum (5), which is lateral continuation
of entorhinal cortex (ec). Subiculum
in gyrus uncinatus
(su)joins
hippocampal
head to amygdala.

i6-kHz
bandwidth.
With this method,
30 sections
can be
obtained
in i 2 mm so sec. The rationale for choosing
an echo
train length of i6 instead of eight was as follows:
Although
an echo train length of eight may offer a better signal-to-noise
ratio with lower resolution
matrices (256 x i 28), with a higher
resolution
matrix size such as 256 x 256, the gain in the
signal-to-noise
ratio when an echo train length of eight is used
rather than one of 1 6 is minimal and results in a doubling
of
image time. Although
not shown in this essay, proton densityweighted
fast spin-echo
images can also be obtained
that in
our experience
are comparable
to conventional
spin-echo
images. However,
there is an additional
time penalty if protondensity images are to be obtained.
The fast spin-echo
technique
is a hybrid based on a rapidacquisition
relaxation-enhanced
method initially described
by
Hennig et al. [4]. This fast spin-echo
sequence
consists
of a
i 6-echo Carr-Purcell-Meiboom-GiII
train with an echo spacing

between
iS and i8 msec. In this technique,
a single RF pulse
is followed
by an echo train in which each echo is individually
phase encoded
and then read in the presence
of a frequencyencoding
gradient.
T2-weighted
images are acquired
in substantially
less time than when conventional
spin-echo
techniques are used (in our case, 1 2 mm so sec for fast spin echo
compared
with i 37 mm 4 sec for conventional
spin-echo
technique
with similar parameters).
Histologic

Sections

from a Cadaver

A brain from a person with no history of neurologic

disease
and no neuropathologic
findings at autopsy
was selected for
examination.
After 2 weeks
fixation
in 20% formalin,
the
temporal
lobe was removed
and cut perpendicular
to its long
axis in order to mimic the angle used for MR imaging.
Blocks
3-4 mm thick were obtained
throughout
the entire length of

Downloaded from www.ajronline.org by 202.69.105.142 on 05/28/13 from IP address 202.69.105.142. Copyright ARRS. For personal use only; all rights reserved

AJR:159,

December

FAST

1992

SPIN-ECHO

MR

OF

the temporal
lobe. These were embedded
in paraffin
and
sectioned
at 8 m. Sections
from each block were stained
with either cresyl violet or hematoxylin
and eosin with a Luxol
fast blue counterstain
for myelin. The stained sections
were
matched
to the MR images,
and individual
temporal
lobe
structures
were then determined
both on MR images and
cadaveric
histologic
sections
according
to anatomic
references [5].

MR-Histologic

Correlation

Fast spin-echo
anatomic
detail,

MR images of the brain showed

excellent
with no significant
variance
in the shape of

NORMAL

1 3i 1

HIPPOCAMPUS

the hippocampus
among the eight persons examined.
Figures
2-7 are a representative
anterior to posterior
series of images,
matched
as closely as possible
with the corresponding
histologic sections.

Anatomy
of the Hippocampus
Lobe Structures

and Adjacent

Temporal

The hippocampus
consists
of two major parts, the cornu
Ammonis
(hippocampus
proper) and the dentate gyrus, which
are separated
by the hippocampal
sulcus (Fig. SC). Below the
hippocampal
sulcus or fissure is the subiculum,
which occupies the medial/superior
curvature
of the parahippocampal

Fig. 4.-A and B, Histologic

section
(A) through
junction of hippocampal
head (H)and body slightly
posterior
to Fig. 3A and corresponding
fast spinecho coronal MR Image (B). At this level, hippocampus gradually loses characteristic
waviness of
hippocampal

digitations

that mark

hippocampal

head. Posterior
portion of amygdala
(A) Is separated from hippocampus
by temporal
horn. Subiculum (s) between
entorhinal
cortex and first field
of hippocampus
(cornu Ammonis
1) can be easily
identified,
as can subiculum
in gyrus uncinatus
(su) between
hippocampal
head and amygdala.

Fig. 5.-A and B, Histologic section (A) through hippocampal

body (Hb) and corresponding
fast spin-echo
coronal MR image (B). At level of hippocampal
waviness characteristic of hippocampal head is completely absent. Temporal horn can be identified defining lateral aspect of hippocampal
body,
whereas choroidal fissure defines cranial aspect of hippocampal
body. Also note absence
of gray matter of amygdala
at level of hippocampal
body. MR
Image shows some persistence
of hippocampal
sulcus at lateral/inferior
aspect of body (arrow); this normal structure is commonly identified and should
not be mistaken for pathologic change. S = subiculum, cc = entorhinal
cortex.
body,

C, Higher magnification
are well seen. CAl field
Ammonis
before curving

of area of hippocampal
body in A. The four regions of the cornu Ammonis (CAl, CA2, CA3, CA4), comprising
pyramidal
neurons,
is the largest cellular field and represents
lateral continuation
of subiculum
(5). CA2 field appears
at cranial aspect of comu
into region of dentate
gyrus. CA3 field is transitional
portion of comu Ammonis,
with CA4 field surrounded by dentate gyrus.
Alveus (a) is a compact white matter tract of efferent axons separating
hippocampus
from temporal
horn. Fimbna (Fl) represents
free edge of this white
matter tract and appears at cranial limit of hippocampus;
fimbria ultimately forms fornix in region of hippocampal
tail. Dentate
gyrus has two layers: the

densely packed granular layer (gD) above the adjacent, loosely packed neuropil of the molecular layer (mD). Hippocampal
embryonic fissure between dentate gyrus and comu Ammonis; it is usually obliterated during development,
although commonly
B).

sulcus (Hs) represents

traces may remain (see

TIEN

i 3i 2

ET AL.

AJR:159,

December

1992

Downloaded from www.ajronline.org by 202.69.105.142 on 05/28/13 from IP address 202.69.105.142. Copyright ARRS. For personal use only; all rights reserved

Fig. 6.-A and B, Histologic section (A) through

hippocampal
body (Hb) slightly posterior to Fig. 5A
and corresponding
fast spin-echo
coronal MR image (B). Although temporal horn in region of hippocampal
head
lacks choroid
plexus,
choroid
plexus is commonly identified in temporal horn at
level of hippocampal
body. Fimbria
attains
its
greatest size at this level before forming fornix at
tail of hippocampus.
s = subiculum.

Fig. 7.-A

hippocampal

and B, Histologic

section (A) through

tail (Ht) and corresponding
fast spin-

echo coronal MR image (B). Tail is characterized

by alveus/fimbria
forming fornix (Fo) covering
its
cranial aspect.
Hippocampal
tail bulges into choroid plexus containing
atrium of lateral ventricle.

gyrus and runs superolaterally

to its border with the hippocampus.
The hippocampus,
which
represents
primitive
or
allocortex,
is therefore
separated
from the temporal neocortex
(specifically,
the entorhinal
cortex and the rest of the parahippocampal
gyrus) by the transistional
zone (periallocortex)
of
the subiculum.
The hippocampus
proper consists
of six layers: the alveus,
stratum
oriens, stratum
pyramidale,
stratum
radiatum,
stratum lacunosum,
and stratum moleculare.
The alveus (Fig. SC)
covers the portion of the hippocampus
that protrudes
into the
temporal
horn of the lateral ventricle
and is the main efferent
path followed
by hippocampal
and subicular
axons. The alveus continues
medially to form the fimbna of the hippocampus, which in turn joins the fomix. Stratum
lacunosum
contains some of the efferent
fibers to the hippocampus.
The
remaining
four layers of the hippocampus
are gray matter
consisting
primarily of pyramidal
neurons,
dendrites,
and collateral axons.
Because
of the different
appearances
and
different
connections
of the pyramidal
neurons,
the cornu
Ammonis
is usually divided into four fields, CAi
CA2, CA3,
and CA4, which are labeled in Figure SC. CAl is adjacent
to
the subiculum
and is by far the largest of these areas. It
contains
small, scattered
neurons,
which are roughly divided
into two sublayers.
CA2 contains
pyramidal
cells packed into
a single dense layer; it generally
appears
at or near the
superior
aspect of the cornu Ammonis.
CA3 is located at or
near the curve of the cornu Ammonis
as it enters the hilum
,

of the dentate gyrus. CA4 consists

of a dispersed
population
of pyramidal
cells scattered
within this hilum.
The dentate gyrus envelops field CA4 of the cornu Ammonis
and is separated
from CAl -CA3 and the subiculum
by the
hippocampal
fissure
(Fig. SC). The hippocampal
fissure
is
usually obliterated
during development,
although
a persistent
cavity often remains (Fig. SB). The two most prominent
layers
within the dentate gyrus are the densely packed layer of cell
bodies called the granular
layer and the adjacent
neuropil
called the molecular
layer (Fig. SC).

Specific
Adjacent

Anatomic
Temporal

Interpretation

Features
of the Hippocampus
and
Lobe Structures
Important
for

of MR

Images

With continuing
refinements
in MR technology,
finer anatomic details of the hippocampus
can be identified.
While the
cellular structures
of the hippocampus
proper are currently
beyond the resolution
of current techniques,
some anatomic
structures
can be identified
consistently.
The hippocampus,
like the caudate
nucleus, forms an arc running roughly rostral
to caudal in the medial temporal
lobe with a head (also known
as the pes hippocampi),
body, and tail that are approximately
4 cm long [5] (Fig. i). The hippocampal
head (pes hippocampi)
(Figs. 2 and 3) is marked
by the hippocampal
digitations,
which are sagittally
oriented
enfoldings
of the various layers

AJR:159,

December

of the hippocampus
sion of the dentate

Downloaded from www.ajronline.org by 202.69.105.142 on 05/28/13 from IP address 202.69.105.142. Copyright ARRS. For personal use only; all rights reserved

FAST

1992

SPIN-ECHO

MR

OF

proper, each surrounding

a digital extengyrus. The amygdala
is directly anterior/

superior
to the hippocampal
head and the uncal recess is
directly anterior to the hippocampal
head. Laterally,
the head
bulges into the temporal
horn; this region of the ventricle
is
free of choroid plexus. Medially, the pes hippocampi
continues
into the posterior
portion
of the uncus. (The uncus is the
anterior
segment
of the parahippocampal
gyrus. It includes
the entorhinal
cortex, Brodmanns
area 28.)
The hippocampal
body lacks the digitations
of the hippocampal head (Figs. S and 6). The deep aspect of the hippocampal body forms a portion of the floor of the temporal
horn;
it protrudes
into the ventricle
and is covered
by the alveus
and the ependyma.
Choroid
plexus
in the temporal
horn
covers
this surface,
which is composed
primarily
of fields
CAl -CA3. The superficial
aspect of the body is adjacent
to
the fimbria, which extends
superiorly
and medially
over the
dentate gyrus.

1993

ARRS

RESIDENTS

Presidents
U

The

viniwr

senteci

of the
certilicate

(1

and

Award

receive

an

REFERENCES
1 . Bronen

be

JT. et al. Imaging

findings

CK. et al. Temporal

5. Duvernoy

HM. The human

hippocampus.

RADIOLOGY

The

two

will

each

of

AND

Council

winners

of the

receive

Berlin:

Springer-Verlag.

WARDS

Awards

Executive

a certifk-ate

Council

an

and

Award

honorarium

REGULATIONS

clinical
applk-aand
radiological

U
U

S(iCIl(C.

is eii
to residents
sciences.
If not the

llie event
radiological
expected
majority

that
the resident
of the work
and

radiology

in

sole
author.
will have
performed
be the senior
author.

Manuscripts
10 illustrations.

EOOr

should

not

exceed

5,000

wOrdS

Winners

will

Papers

will

be
be

announced
presented

by
at

March

the

American

and
it is
the

and

Manuscripts
receiving

will

be

returned

to candidates

awards.

DEADUNE
copies
.

of the paper
ail
four
.
should
be subnitted
12,
1993,
to:

packages
no later

of the
than

1 6.

1 993.

Roent-

gen Ray Society

93u1
Annual
Scientific
Meeting
at
the
San
Francisco
Marriott,
San
Francisco.
CA.
April
25-30.
1993.
and
be submitted
for pul)lication
to the American
Journal
o/Roen(geriologtj.
U

lobe seizures:

of $1,000.

Papers
must
l)C sul)mitte(I
on the
tion
of I he discipline
of radiology

illustrations
February

in hippocampal

4. Hennig J, Naureth A, Friedburg H. RARE imaging: a fast imaging method

for clinical MR. Magn Reson Med 1986:3:823-833

pre-

honorariun

RULES

G. Charies

lateralization
with MR volume measurements
of the hsppocampal
formation. Radiology
1990;175:423-429
3. Naidich TP, Daniels DL, Haughton
VM, Williams A, Pojunas K, Palacios E.
Hippocampal
formation
and related structures
of the limbic lobe: anatomicMR correlation. Radiology
1987; 1 62 : 747-754

$2,000.

RA, Cheung

sclerosis. A.JNR 1991:12:933-940

2. Jack CR, Sharbrough FW, Twomey

Executive
will

1313

HIPPOCAMPUS

The hippocampal
tail (Fig. 7) forms an arc posteriorly
and
occupies
a portion of the floor of the atrium and curves along
the inferior surface of the splenium.
It is covered by the white
matter of the alveus and by ependyma
superolaterally.
The
alveus is continuous
with the fimbria, which in turn forms the
thin crura of the fornices.

IN

Award
Presidents

NORMAL

NaIuYO.

Wllitl(Y.

MI).

CIlatnI1an. C onhIlutU(Roentgen

Ai-riii

1891
Rtsloii,

Preston
Virginia

White
2209

on

Ra

l)rive
1

L(lt1C(At1ol
Soeietv

&.

R(s(-arch

not

1988