Normal anatomy of the hippocampus and adjacent temporal lobe: high-resolution fast spin-echo MR Images in volunteers correlated with cadaveric histologic sections

Abstract

This essay illustrates the appearances of sections of the normal hippocampus and adjacent temporal lobe 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.

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1309
AJR 159:i309-13i3, December 1992 0361-803X/92/1596-1309 0American Roentgen Ray Society
Pictorial Essay
L..“:‘,‘
Normal Anatomy of the Hippocampus and Adjacent
Temporal Lobe: High-Resolution Fast Spin-Echo MR
Images in Volunteers Correlated with Cadaveric Histologic
Sections
Robert D. Tien,1 Gary J. Felsberg,1 and Barbara Cram2
This essay illustrates the appearances of sections of the nor-
mel hippocampus and adjacent temporal lobe 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 hippo-
campus 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 Alz-
heimer’s disease [1 ]. Although gross estimates of hippocam-
pal 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
heavily T2-weighted (long TR/long TE) images and large-
matrix 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 gener-
ated parasagittal images through the long axis of the hippo-
campus, 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 inter-
leave (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
Received March 20, 1992; accepted after revision June 24, 1992.
1Department of Radiology, Box 3808, Duke University Medical Center, Durham,
2Department of Pathology. Duke University Medical Center, Durham, NC 27710. NC 2771 0. Address reprint requests to A. D. Tien.

A 1
A B
13i 0 TIEN ET AL. AJR:159, December 1992
Fig. 1.-Drawing shows left lateral view of lim-
bic system. Hippocampus (green) is located in
medial temporal lobe and has an arclike configu-
ration ending in region of splenium of corpus cal-
losum. 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.
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 and B, Histologic section (A) through
hippocampal head (Hh) slightly posteriorto Fig. 2A
and corresponding fast spin-echo coronal MR im-
age (B). Hippocampal head can be seen consist-
ently on MR by identification of hippocampal digi-
tations, 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 sub-
iculum (5), which is lateral continuation of ento-
rhinal 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 16 is minimal and results in a doubling of
image time. Although not shown in this essay, proton density-
weighted 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 proton-
density images are to be obtained.
The fast spin-echo technique is a hybrid based on a rapid-
acquisition 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 frequency-
encoding gradient. T2-weighted images are acquired in sub-
stantially less time than when conventional spin-echo tech-
niques are used (in our case, 12 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

AJR:159, December 1992 FAST SPIN-ECHO MR OF NORMAL HIPPOCAMPUS 13i 1
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 refer-
ences [5].
MR-Histologic Correlation
Fast spin-echo MR images of the brain showed excellent
anatomic detail, with no significant variance in the shape of
Fig. 4.-A and B, Histologic section (A) through
junction of hippocampal head (H)and body slightly
posterior to Fig. 3A and corresponding fast spin-
echo coronal MR Image (B). At this level, hippo-
campus gradually loses characteristic waviness of
hippocampal digitations that mark hippocampal
head. Posterior portion of amygdala (A) Is sepa-
rated from hippocampus by temporal horn. Subi-
culum (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.
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 his-
tologic sections.
Anatomy of the Hippocampus and Adjacent Temporal
Lobe Structures
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 occu-
pies the medial/superior curvature of the parahippocampal
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
body, 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.
C, Higher magnification of area of hippocampal body in A. The four regions of the cornu Ammonis (CAl, CA2, CA3, CA4), comprising pyramidal neurons,
are well seen. CAl field is the largest cellular field and represents lateral continuation of subiculum (5). CA2 field appears at cranial aspect of comu
Ammonis before curving 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 sulcus (Hs) represents
embryonic fissure between dentate gyrus and comu Ammonis; it is usually obliterated during development, although commonly traces may remain (see
B).

i 3i 2 TIEN ET AL. AJR:159, December 1992
Fig. 6.-A and B, Histologic section (A) through
hippocampal body (Hb) slightly posterior to Fig. 5A
and corresponding fast spin-echo coronal MR im-
age (B). Although temporal horn in region of hip-
pocampal 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 and B, Histologic section (A) through
hippocampal 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 cho-
roid plexus containing atrium of lateral ventricle.
gyrus and runs superolaterally to its border with the hippo-
campus. The hippocampus, which represents primitive or
allocortex, is therefore separated from the temporal neocortex
(specifically, the entorhinal cortex and the rest of the parahip-
pocampal gyrus) by the transistional zone (periallocortex) of
the subiculum.
The hippocampus proper consists of six layers: the alveus,
stratum oriens, stratum pyramidale, stratum radiatum, stra-
tum 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 al-
veus continues medially to form the fimbna of the hippocam-
pus, which in turn joins the fomix. Stratum lacunosum con-
tains 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 col-
lateral 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 Anatomic Features of the Hippocampus and
Adjacent Temporal Lobe Structures Important for
Interpretation of MR Images
With continuing refinements in MR technology, finer ana-
tomic 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

1993 ARRS RESIDENTS IN RADIOLOGY AWARDS
AJR:159, December 1992 FAST SPIN-ECHO MR OF NORMAL HIPPOCAMPUS 1313
of the hippocampus proper, each surrounding a digital exten-
sion of the dentate gyrus. 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, Brodmann’s area 28.)
The hippocampal body lacks the digitations of the hippo-
campal head (Figs. S and 6). The deep aspect of the hippo-
campal 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.
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.
REFERENCES
1.Bronen RA, Cheung G. Charies JT. et al. Imaging findings in hippocampal
sclerosis. A.JNR 1991:12:933-940
2. Jack CR, Sharbrough FW, Twomey CK. et al. Temporal lobe seizures:
lateralization with MR volume measurements of the hsppocampal forma-
tion. 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: anatomic-
MR correlation. Radiology 1987; 1 62 : 747-754
4. Hennig J, Naureth A, Friedburg H. RARE imaging: a fast imaging method
for clinical MR. Magn Reson Med 1986:3:823-833
5. Duvernoy HM. The human hippocampus. Berlin: Springer-Verlag. 1988
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