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AJR 159:i309-13i3, December 1992 0361-803X/92/1596-1309 0
American Roentgen Ray Society
Pictorial Essay
L ..:,Normal Anatomy of the Hippocampus and AdjacentTemporal
Lobe: High-Resolution Fast Spin-Echo MRImages in Volunteers
Correlated with Cadaveric HistologicSectionsRobert 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-resolutionheavily T2-weighted fast spin-echo MR images and
correlatesthem with histologic sections. We found that this MR
examinationshowed the detailed anatomy of the normal hippocampus in
amuch shorter time than is possible with conventional
spin-echotechniques. The information provided in this essay can be
usedas a baseline for distinguishing between normal and
abnormalhippocampi in a variety of disease states.
The hippocampus is an important structure in the brain thatis
involved in numerous diseases. Visualization of the hippo-campus
with MR imaging has therefore been extremely usefulin detecting
such pathologic entities as hippocampal sclerosisor atrophy in
patients with temporal lobe epilepsy and Alz-heimers disease [1 ].
Although gross estimates of hippocam-pal size and signal
abnormality have clinical value [2], wethink that more precise
imaging can help to further delineatethe fine anatomic detail of
the hippocampus and thus providemore sensitive detection and
localization of lesions in thisstructure. Anatomic details of the
hippocampus shown on Ti -weighted images (5-mm-thick sections)
correlate closely withanatomic findings in cadaveric sections [3].
However, imagingcan be improved by using a recently described MR
pulsesequence, 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. Withthis
technique, anatomic detail is improved because thinsections (2 mm),
a high-resolution matrix (256 x 256), andfour excitations can be
used. In addition, it may be possibleto detect signal abnormalities
involving the hippocampus. Wecorrelated the fast spin-echo images
of the hippocampus andmedial temporal lobe structures in eight
healthy volunteerswith histologic sections from a normal cadaveric
brain.
Fast Spin-Echo MR Imaging in Healthy Volunteers
MR images of the brains of eight healthy young adultvolunteers
(mean age, 32 years) were obtained with a 1 .5-Tsuperconducting
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 imageswere prescribed to cover
the entire length of the hippocampus(Fig. 1 ). Each person was then
imaged by using a standardquadrature head coil and fast spin-echo
techniques with thefollowing image parameters: 2-mm-thick sections
with inter-leave (the minimal slice thickness in our current fast
spin-echosoftware), 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, 1992.1
Department of Radiology, Box 3808, Duke University Medical Center,
Durham,2 Department of Pathology. Duke University Medical Center,
Durham, NC 27710. NC 2771 0. Address reprint requests to A. D.
Tien.
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A 1
A B
1 3i 0 TIEN ET AL. AJR:159, December 1992
Fig. 1.-Drawing shows left lateral view of lim-bic system.
Hippocampus (green) is located inmedial temporal lobe and has an
arclike configu-ration ending in region of splenium of corpus
cal-losum. Fimbria of hippocampus (yellow), which isformed by
alveus, in turn becomes fornix (yellow)at level of hippocampal
tail. Amygdala (blue) isimmediately rostral to hippocampal
head.
Fig. 2.-A and B, Histologic section (A) through anterior
hippocampal head (Hh) and correspondingslightly anterior fast
spin-echo coronal MR image (B). Gray matter of hippocampal head is
inferior totemporal horn; gray matter of amygdala (A) is superior
and anterior to hippocampal head. Lateralaspect of hippocampal head
is limited by temporal horn; medially, entorhinal cortex (cc) can
beidentified within parahippocampal gyrus.
Fig. 3.-A and B, Histologic section (A) throughhippocampal head
(Hh) slightly posteriorto Fig. 2Aand 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 tohippocampus at this level. Hippocampal
head isseparated from gray matter of amygdala (A) (midto 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 beobtained
in i 2 mm so sec. The rationale for choosing an echotrain length of
i6 instead of eight was as follows: Althoughan echo train length of
eight may offer a better signal-to-noiseratio with lower resolution
matrices (256 x i 28), with a higherresolution matrix size such as
256 x 256, the gain in thesignal-to-noise ratio when an echo train
length of eight is usedrather than one of 1 6 is minimal and
results in a doubling ofimage time. Although not shown in this
essay, proton density-weighted fast spin-echo images can also be
obtained that inour experience are comparable to conventional
spin-echoimages. 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
byHennig et al. [4]. This fast spin-echo sequence consists of ai
6-echo Carr-Purcell-Meiboom-GiII train with an echo spacing
between iS and i8 msec. In this technique, a single RF pulseis
followed by an echo train in which each echo is individuallyphase
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 echocompared with i 37 mm 4 sec
for conventional spin-echotechnique with similar parameters).
Histologic Sections from a Cadaver
A brain from a person with no history of neurologic diseaseand
no neuropathologic findings at autopsy was selected forexamination.
After 2 weeks fixation in 20% formalin, thetemporal lobe was
removed and cut perpendicular to its longaxis in order to mimic the
angle used for MR imaging. Blocks3-4 mm thick were obtained
throughout the entire length of
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AJR:159, December 1992 FAST SPIN-ECHO MR OF NORMAL HIPPOCAMPUS 1
3i 1
the temporal lobe. These were embedded in paraffin andsectioned
at 8 m. Sections from each block were stainedwith either cresyl
violet or hematoxylin and eosin with a Luxolfast blue counterstain
for myelin. The stained sections werematched to the MR images, and
individual temporal lobestructures were then determined both on MR
images andcadaveric histologic sections according to anatomic
refer-ences [5].
MR-Histologic Correlation
Fast spin-echo MR images of the brain showed excellentanatomic
detail, with no significant variance in the shape of
Fig. 4.-A and B, Histologic section (A) throughjunction of
hippocampal head (H)and body slightlyposterior to Fig. 3A and
corresponding fast spin-echo coronal MR Image (B). At this level,
hippo-campus gradually loses characteristic waviness ofhippocampal
digitations that mark hippocampalhead. Posterior portion of
amygdala (A) Is sepa-rated from hippocampus by temporal horn.
Subi-culum (s) between entorhinal cortex and first fieldof
hippocampus (cornu Ammonis 1) can be easilyidentified, as can
subiculum in gyrus uncinatus(su) between hippocampal head and
amygdala.
the hippocampus among the eight persons examined. Figures2-7 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 TemporalLobe
Structures
The hippocampus consists of two major parts, the cornuAmmonis
(hippocampus proper) and the dentate gyrus, whichare separated by
the hippocampal sulcus (Fig. SC). Below thehippocampal 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 hippocampalbody, 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. MRImage shows
some persistence of hippocampal sulcus at lateral/inferior aspect
of body (arrow); this normal structure is commonly identified and
shouldnot 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 comuAmmonis 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
whitematter tract and appears at cranial limit of hippocampus;
fimbria ultimately forms fornix in region of hippocampal tail.
Dentate gyrus has two layers: thedensely packed granular layer (gD)
above the adjacent, loosely packed neuropil of the molecular layer
(mD). Hippocampal sulcus (Hs) representsembryonic fissure between
dentate gyrus and comu Ammonis; it is usually obliterated during
development, although commonly traces may remain (seeB).
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Fig. 6.-A and B, Histologic section (A) throughhippocampal body
(Hb) slightly posterior to Fig. 5Aand corresponding fast spin-echo
coronal MR im-age (B). Although temporal horn in region of
hip-pocampal head lacks choroid plexus, choroidplexus is commonly
identified in temporal horn atlevel of hippocampal body. Fimbria
attains itsgreatest size at this level before forming fornix attail
of hippocampus. s = subiculum.
Fig. 7.-A and B, Histologic section (A) throughhippocampal tail
(Ht) and corresponding fast spin-echo coronal MR image (B). Tail is
characterizedby alveus/fimbria forming fornix (Fo) covering
itscranial 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
orallocortex, is therefore separated from the temporal
neocortex(specifically, the entorhinal cortex and the rest of the
parahip-pocampal gyrus) by the transistional zone (periallocortex)
ofthe 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
thetemporal horn of the lateral ventricle and is the main
efferentpath 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. Theremaining four layers of
the hippocampus are gray matterconsisting primarily of pyramidal
neurons, dendrites, and col-lateral axons. Because of the different
appearances anddifferent connections of the pyramidal neurons, the
cornuAmmonis is usually divided into four fields, CAi , CA2,
CA3,and CA4, which are labeled in Figure SC. CAl is adjacent tothe
subiculum and is by far the largest of these areas. Itcontains
small, scattered neurons, which are roughly dividedinto two
sublayers. CA2 contains pyramidal cells packed intoa single dense
layer; it generally appears at or near thesuperior aspect of the
cornu Ammonis. CA3 is located at ornear the curve of the cornu
Ammonis as it enters the hilum
of the dentate gyrus. CA4 consists of a dispersed populationof
pyramidal cells scattered within this hilum.
The dentate gyrus envelops field CA4 of the cornu Ammonisand is
separated from CAl -CA3 and the subiculum by thehippocampal fissure
(Fig. SC). The hippocampal fissure isusually obliterated during
development, although a persistentcavity often remains (Fig. SB).
The two most prominent layerswithin the dentate gyrus are the
densely packed layer of cellbodies called the granular layer and
the adjacent neuropilcalled the molecular layer (Fig. SC).
Specific Anatomic Features of the Hippocampus andAdjacent
Temporal Lobe Structures Important forInterpretation of MR
Images
With continuing refinements in MR technology, finer ana-tomic
details of the hippocampus can be identified. While thecellular
structures of the hippocampus proper are currentlybeyond the
resolution of current techniques, some anatomicstructures can be
identified consistently. The hippocampus,like the caudate nucleus,
forms an arc running roughly rostralto caudal in the medial
temporal lobe with a head (also knownas the pes hippocampi), body,
and tail that are approximately4 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
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1993 ARRS RESIDENTS IN RADIOLOGY A WARDS
AJR:159, December 1992 FAST SPIN-ECHO MR OF NORMAL HIPPOCAMPUS
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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 isdirectly anterior to
the hippocampal head. Laterally, the headbulges into the temporal
horn; this region of the ventricle isfree of choroid plexus.
Medially, the pes hippocampi continuesinto the posterior portion of
the uncus. (The uncus is theanterior segment of the parahippocampal
gyrus. It includesthe entorhinal cortex, Brodmanns 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 alveusand the ependyma. Choroid
plexus in the temporal horncovers this surface, which is composed
primarily of fieldsCAl -CA3. The superficial aspect of the body is
adjacent tothe fimbria, which extends superiorly and medially over
thedentate gyrus.
The hippocampal tail (Fig. 7) forms an arc posteriorly
andoccupies a portion of the floor of the atrium and curves
alongthe inferior surface of the splenium. It is covered by the
whitematter of the alveus and by ependyma superolaterally.
Thealveus is continuous with the fimbria, which in turn forms
thethin crura of the fornices.
REFERENCES
1 . Bronen RA, Cheung G. Charies JT. et al. Imaging findings in
hippocampalsclerosis. 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 methodfor clinical MR. Magn Reson Med 1986:3:823-833
5. Duvernoy HM. The human hippocampus. Berlin: Springer-Verlag.
1988
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