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MRI of the temporal lobe: Normal variations, with special reference toward epilepsy
Magnerrc Resonance Printed in the USA.
Imaging. Vol. 9. pp. 501-507, All rights reserved.
1991 Copyright
0730-725X/91 $3.00 + .OO 0 1991 Pergamon Press plc
l Original Contribution
MRI OF THE TEMPORAL LOBE: NORMAL WITH SPECIAL REFERENCE TOWARD RICHARD Department
A. BRONEN AND GORDON
VARIATIONS, EPILEPSY
CHEUNG*
of Diagnostic Radiology, Yale University School of Medicine, New Haven, CT
Recent investigations of epilepsy, Alzheimer’s disease, amnesia, and schizophrenia have used magnetic resonance imaging (MRI) to evaluate changes in temporal lobe structures. Normal variations in these structures need to be defined before one can use these structures to describe abnormal conditions. Twenty-nine normal volunteers were studied by coronal MRI. Frequent findings include notching of the uncus by the tentorium or adjacent vessels (22/29) and asymmetry of the temporal horns (20/29). This finding of uncal notching strengthens the evidence against “incisural sclerosis” as the basis for hippocampal sclerosis. Temporal horn dilatation occurred in four. However, mild asymmetry of the temporal horn was seen frequently at its anterior tip (16/29) and may be related to head rotation. Asymmetry of the choroidal fissure was never marked. Mild asymmetry was common at the hippocampal head (pes). Mild enlargement of the right temporal lobe by visual inspection is not uncommon. Subtle asymmetry of the white matter between the hippocampus and the collateral sulcus occurred in six. The collateral sulcus does not always point to the temporal horn. The occipitotemporal sulcus may point to the temporal horn. Asymmetric uncal protrusion (O/29) and Sylvian fissure dilatation (4/29) occur rarely.
Keywords: Choroidal fissure; Magnetic resonance; Sylvian fissure; Temporal horn; Temporal lobe; Uncus.
INTRODUCTION
pocampal sclerosis has been associated with a small hyperintense hippocampus, a small temporal lobe, uncal protrusion and associated notching, collateral white matter atrophy, choroidal fissure abnormalities, temporal horn enlargement, and Sylvian fissure dilatation.4s’2-23 MR of the normal hippocampus has already been described. 24-26This report focuses on asymmetry of temporal lobe, uncus, collateral white matter, choroidal fissure, temporal horn, and Sylvian fissure.
Temporal lobe structures have been the focus of attention because of their association with memory, language, and seizure propagation. l-6 Anatomic detail of the temporal lobe by magnetic resonance imaging (MRI) is clearly superior to other imaging modalities.7*8Thus, recent investigations of epilepsy, Alzheimer’s disease, amnesia, and schizophrenia have all used MRI to qualitatively or quantitatively analyze temporal lobe structures. 3,4.9-‘5Before one can analyze pathologic processes by MRI, variations occurring in normal populations should be considered. The purpose of this communication is to establish normative data for temporal lobe structures. Due to our interest in temporal lobe epilepsy and hippocampal sclerosis, we focused our attention on structures which have been reported to be altered in these entities. Although the literature can be conflicting at times, hip-
METHODS Description of subjects and MR technique has been previously reported. 27 Symmetry of six anatomic regions were investigated by visual inspection by two neuroradiologists: temporal lobe, uncus, collateral white matter, choroidal fissure, temporal horn (along with body of lateral ventricle), and Sylvian fissure
RECEIVED12/S/90; ACCEPTED2/25/91. *Present address: Sunnybrook Health Science Centre, University of Toronto, Department of Diagnostic Radiology, 2075 Bayview Avenue, New York, Ontario, Canada M4N 3M5.
Address ail correspondence to Richard A. Bronen, M.D., Yale University School of Medicine, Department of Diagnostic Radiology, 333 Cedar Street, New Haven, CT 06510, USA. 501
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Magnetic Resonance Imaging 0 Volume 9, Number 4, 1991
(Fig. 1). Head rotation was evaluated by assessing symmetry of internal auditory canals* and the anterior aspects of the atria (of the lateral ventricles). Temporal lobe was assessed by comparing the left and right temporal lobes from the anterior temporal tip back through the level of the brainstem. Boundaries of the temporal lobes were defined according to established precedent. ‘~4 Natural margins are formed by the Sylvian fissure, circummesencephalic cistern, choroidal fissure/temporal horn complex and the bony cranium. Completing the medial border of the temporal lobe is a line through the temporal stem connecting the inferior fork of the Sylvian fissure to the superiolateral aspect of the choroidal fissure/temporal horn complex. Rating criteria consisted of (i) no asymmetry, (ii) subtle or questionable asymmetry, and (iii) definite asymmetry. Asymmetric protrusion or herniation of uncus was assessed, as compared to a sag&al plane bisecting the third ventricle. Notching of the uncus was also studied. Grading consisted of the following categories: (i) no notching or questionable notching; (ii) left-sided notching, (iii) right-sided notching, or (iv) bilateral notching. The collateral white matter (CWM) is defined as the white matter situated between the collateral sulcus gray matter and the hippocampus just medial to the collateral eminence (Fig. 1). The “choroidal fissure” refers to the cerebrospinal fluid (CSF) space superior
Fig. 1. Coronal diagram of the right medial temporal lobe. The collateral white matter (CWM) is defined as the white matter situated between the hippocampus and the cortex overlying the collateral sulcus. The choroidal fissure (Ch) height is evaluated at the midpoint of the hippocampus. The choroidal fissure communicates with the transverse fissure (TF) and the ambient or circummesencephalic cistern (AC). LOTG = lateral occipitotemporal gyrus, PHG = parahippocampal gyrus, TH = temporal horn.
the hippocampal formation.28 The degree of enlargement of the Sylvian fissures was assessed. Specifically, the degree of fissure dilatation on the left was compared to the right (Fig. 2). The length and height of the fissure were not evaluated. Temporal horn was investigated by first assessing for dilatation. This is distinct from mild asymmetry which was also studied. The bodies of the lateral ventricles were also assessed for asymmetry. to
RESULTS
Temporal Lobe Both observers agreed that the anterior temporal lobes were symmetric in size in 16 subjects. In another 8 subjects, at least one observer felt the left temporal lobe was smaller (Fig. 3). Disparate findings by the observers occurred in three additional subjects. Temporal lobe asymmetry could not be reliably assessed in two studies due to the degree of rotation.
uncus Asymmetric uncal protrusion/herniation was not observed. Uncal notching was seen in 22 subjects, 18 bilateral (Fig. 2). Unilateral notching was left-sided in three and right-sided in one. Variations in the degree
Fig. 2. Coronal short TR image at the junction of amygdala with hippocampai head. The amygdala (a) and uncus (u) appear as one continuous mass of gray. Bilateral notching (white arrow) of the uncus by the tentorium (or vasculature) is a normal finding. Bilateral symmetric bulging of the uncus medially into the suprasellar cistern is also a normal finding. Asymmetry of the anterior temporal horn (t) is frequently found in normal subjects as the ventricle insinuates itself between the amygdala and hippocampus. Sylvian fissure dilatation is measured between the large black arrows and is usually symmetric. CWM (small black arrow) height is symmetric. The collateral sulcus (small curved arrow) points toward the temporal horn.
MR of the temporal lobe 0 R.A. BRONEN AND G. CHEUNG
503
Table 1.
Symmetry Temporal lobe* Uncus CMW*** Choroidal fissure Temporal horn Sylvian fissure
16 29 23 18 9 25
Mild asymmetry 1** 0 5 II 16 4
*3 cases-disparate findings; 2 cases-not marked head rotation. **By at least one observer. ***Collateral white matter. Fig. 3. Coronal short TR images through the anterior temporal lobe. The left anterior temporal lobe is smaller than the right. Figure 4, illustrating a more posterior image in the same study, confirms that this is not due to head rotation.
of the uncus was common. Often, it could not be determined whether the notch was due to the tentorium or an associated vessel.
of notching
Collateral White Matter Definite asymmetry of CWM was seen in one subject, subtle or questionable asymmetry in 5, while no asymmetry was seen in 23 (Figs. 2, 4). The collateral sulcus was not always the dominant sulcus pointing to
Fig. 4. Coronal short TR image, posterior to Fig. 3 in the same subject. This plane sections the hippocampus just posterior to the transition of head to body. The left and right choroidal fissure (large arrow), CWM (small arrow), and temporal horns (curved arrow) are symmetric. The temporal horns are usually symmetric posterior to the amygdala/ hippocampal junction. The right collateral sulcus (C) points toward the hippocampus while the occipitotemporal sulcus (0) is directed toward but not at the temporal horn.
Marked asymmetry 1** 0 1 0 4 0 evaluated due to
temporal horn. Not infrequently, the occipitotemporal sulcus with its cortical cap was the largest sulcus pointing to the temporal horn. The collateral sulcus is sometimes directed toward the hippocampal formation rather than the collateral eminence, the floor of the temporal horn. Choroidal Fissure The choroidal fissure height was symmetric in 18/29 subjects (Fig. 4). There was mild asymmetry of the fissure at the level of the hippocampal head in 9/29, with prominence of the right side in 8 of these 9. In only 2/29 was there mild asymmetry of the choroidal fissure posterior to the hippocampal head. The more prominent fissure was on the right in both subjects. Marked asymmetry or dilatation of choroidal fissure was never observed. No choroidal fissure cysts were seen in this group. Temporal Horn There was definite dilatation of the temporal horn in two patients, one left- and one right-sided. In the patient with the right temporal horn dilatation, there was concomitant right lateral body ventricle enlargement. In two patients, there was subtle or questionable temporal horn dilatation on the right side. In one of these, there was ipsilateral enlargement of the body of the lateral ventricle. In 25 subjects there was no significant temporal horn dilatation, but a mild asymmetry occurred in 16. The right side was mildly larger in 15 of these 16. This mild asymmetry often occurred anteriorly, as the temporal horn sweeps medially separating the amygdala from the hippocampal head (Figs. 2, 4). The body of the lateral ventricle was slightly enlarged on the right side in four subjects. In was definitely enlarged on the right in four others, and in two on the left.
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Sylvian Fissure Mild asymmetric dilatation of the Sylvian fissure occurred in 4 of the 29, 3 on the left and 1 on the right (Fig. 2). DISCUSSION Lateralization of brain function is well described. 5*6Certain mo r p hologic differences of the cerebral hemispheres appear to be closely related to the lateralization of brain function.29-33 Other asymmetries which may be related in some manner to handedness are more difficult to link to specific functions, yet are remarkedly consistent.34-37 Inherent cerebral asymmetries in normals can lead to gross miscalculations in the evaluation of disease states if one does not factor in these normal variations. The purpose of this study is to investigate the normal variations of the temporal lobe, particularly the medial portion, with MRI. MRI assessment of temporal lobe structures has recently been used to evaluate amnesia, Alzheimer’s disease, schizophrenia, and epilepsy.3,4,9-‘5 Since our eventual objective is to acquire normative data in order to evaluate imaging of epileptics, we focused our attention on the structures which have been reported to be abnormal in epilepsy, and in particular hippocampal sclerosis. These structures include the hippocampus, temporal lobe, uncus, CWM, choroidal fissure, temporal horn, and Sylvian fissure.4,12-23 Temporal Lobe Indirect support for temporal lobe asymmetry is available from studies of Sylvian fissure position. The vertical height of the temporal lobe, and thus its size on coronal slices, is dependent on Sylvian fissure position. As one proceeds posteriorly, the right Sylvian fissure is usually shorter and higher than the left.32,38-4’ The longer length of the Sylvian fissure on the left appears to be related to the larger planum temporale, which is speculated to be the morphologic substrate of language. 29-33Recent quantitative MRI studies have confirmed temporal lobe asymmetry.8~24*25In righthanded subjects, the anterior portion of the right temporal lobe is larger than the left by a small but statistically significant amount. The mean difference of 2.3 cm3 (4Oro)is probably difficult to appreciate visually. However, the range of differences approaches 20% of the temporal lobe volume, an amount which may be detected visually. 24Our study confirms these findings. The temporal lobes were visually symmetric in most. When asymmetry was visualized, the right temporal lobe was usually Iarger. In patients with temporal lobe epilepsy, asymmetry
of the temporal lobe and middle cranial fossa has been used to lateralize the seizure focus. 13-17*24*25 One must be aware of the inherent differences in normals to interpret these findings correctly. Since the right temporal lobe is frequently larger than the left, a smaller right temporal lobe is a much more significant finding than a smaller left lobe in the evaluation of epilepsy. Uncus It was theorized by Earle et al. that hippocampal sclerosis, or “incisural sclerosis” as they called it, is produced by hippocampal herniation at birth.42 This supposedly transient herniation was thought to cause anoxia to the medial temporal lobe via compression of the anterior choroidal and posterior cerebral arteries. Protrusion of the uncus medial to the tentorial edge, and grooving of the uncus by the tentorium have been used as signs of pathologic uncal herniation.43 Turner and Wyler found herniation of the medial temporal lobe structures in 12 of 16 with hippocampal sclerosis. I8 Although Bolender and Wyler reported CT evidence of medial temporal lobe herniation posteriorly in these same patients, quantitative separation of the “non-herniated” from the “herniated” group could only be obtained by mathematical manipulation of the data. I9320Other studies of epilepsy reported no herniation by either CT or MRI.‘4,44 Our data may help resolve this issue. Asymmetric protrusion of an uncus medially was not seen in any of our 29 volunteers. Notching of the uncus either by the tentorium or an adjacent vessel was seen frequently (76%) in our normal group. Variations exist in the degree of notching. The notching was frequently bilateral. In fact, uncal extension medial to the tentorial edge by 3 to 4 mm and mild grooving of the uncus are normal findings. ‘*45Thus, the uncal notching seen during epilepsy surgery may be unrelated to epilepsy. Since hippocampal sclerosis is an atrophic process, it seems unreasonable that it should be associated with the mass effect implied by uncal herniation. The “incisural sclerosis” theory falters for other reasons, as discussed by Falconer et al., and is not currently in vogue.46 Collateral White Matter Collateral white matter was visually symmetrical in 21 (72%) subjects, questionably asymmetric in 6 (21%) and definitely asymmetric in 2 (70/o). Since CWM asymmetry seen in hippocampal sclerosis may often be subtle,4 the normal population variation should lead one to use this finding as a secondary confirmatory rather than primary sign of hippocampal sclerosis.
MR of the temporal lobe 0 R.A.
The collateral eminence has been described as a bulge in the floor of the temporal horn due to the protrusion of the white and gray matter capping the collateral SU~CUS.‘*~~ Our findings suggest a moderate amount of variation. The collateral sulcus may point to the hippocampal formation rather than the temporal horn, while the occipitotemporal sulcus may point to the temporal horn. Choroidal Fissure Terminology surrounding the choroidal fissure is complex. We will use terms Duvernoy and Naidich et al. have used to describe the CSF spaces associated with the temporal lobe. 1,28The ambient cistern is located between the midbrain and the temporal lobe. Laterally, this cistern is renamed the “transverse fissure” or the “wing of the ambient cistern.” The floor of the transverse fissure is composed of the subiculum, while the roof is formed by the lateral geniculate body and thalamic pulvinar. The choroidal fissure is situated between the transverse fissure and the temporal horn of the lateral ventricle. Two pial layers (tenae) originating from the fimbria and stria semicircularis unite to form the choroid plexus. By strict definition, the choroidal fissure refers only to the region between these two tenae. In common usage and radiologic literature, the choroid fissure refers to the entire CSF space space forming the roof of the hippocampal formation.28 Visually, the choroidal fissure is rarely asymmetric posterior to the hippocampal head. Mild asymmetry at the hippocampal head is not uncommon (strictly speaking, this is the temporal horn, since the choroida1 plexus is not present at the level of the head). ’ This asymmetry was encountered in nine (31%) subjects, almost exclusively on the right side. Silver et al. noted a low association of choroid fissure cysts with epilepsy. 21We did not find any cysts among our normal subjects. CT (and MR) detection of choroidal fissure enlargement has been shown to be highly sensitive for diagnosing Alzheimer’s disease.47 Fissure enlargement appears related to atrophic changes occurring focally in the hippocampus. Sylvian Fissure While reproducible asymmetries of Sylvian fissure length have been reported30~38~39.4’*48 little has been published regarding fissure dilatation. Subtle asymmetric dilatation of the Sylvian fissures occurred in 4 (14%) of our subjects. Sylvian fissure enlargement has not been a particularly useful finding in evaluation of temporal lobe epilepsy. Theodore et a1.22 found unilateral Sylvian fissure enlargement in 2 of 36 epilep-
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tics, while McLachlan et al. l4 noted that this occurred with equal frequency in both epileptics and controls. Temporal Horn Asymmetry of the lateral ventricles and temporal horns in normals has been studied by a variety of methods. The body of lateral ventricle has been found to be larger on the left in 32%-72% of cases studied by pathology,4’*49 pneumoencephalography,41 CT 735so-52and ultrasound.53 During pneumoencephalography, the temporal horn was found to be larger on the left in 6890, and on the right in 11070.~’In our series, unilateral temporal horn dilatation occurred infrequently, in four patients. However, mild asymmetry at the level of the amygdala-hippocampal junction occurs commonly on coronal MR and can often be attributed to head rotation. The temporal horn has its greatest transverse diameter at this location and is known as the uncal recess. With head rotation, the larger uncal recess of one temporal horn may be imaged on the same slice as a smaller, more posterior portion of the contralateral temporal horn. Since mild temporal horn asymmetry appears to be common in normal subjects, one must temper reliance on it for detecting abnormal conditions. With regards to epilepsy and hippocampal sclerosis, the literature has been divided as to the usefulness of temporal horn asymmetry. 4.14,16,17,23.S4.55 REFERENCES 1. Duvernoy, H.M. The Human Hippocampus. An Atlas of Applied Anatomy. Munchen: J.D. Berman Verlag; 1988:~~. l-45. 2. Dam, A.M. Hippocampal neuron loss in epilepsy and after experimental seizures. Actu Neural. Scandinav. 66: 601-642; 1982. 3. Press, G.A.; Amaral, D.G.; Squire, L.R. Hippocampal abnormalities in amnesic patients revealed by high-resolution magnetic resonance imaging. Nature 341:54-57; 1989. 4. Bronen, R.A.; Cheung, G.; Charles, J.T.; et al. Pathologic study of mesial temporal sclerosis: Comparison of scalp EEG, MR, CT and angiography. American Society of Neuroradiology, Orlando, March 19-24, 1989. 5. Geschwind, N. The organization of language and the brain. Science 170:940-944; 1970. 6. Geschwind, N.; Galaburda, A.M. Cerebral Dominance. The Biological Foundations. Cambridge: Harvard University Press; 1984. I. Zhu, X.P.; Checkley, D.R.; Hickey, D.S.; Isherwood, I. Accuracy of area measurements made from MR images compared with computed tomography. J. Comput. Assist. Tomogr. 10:96-102; 1986. F.W.; et al. 8. Jack, C.R.; Gehring, D.G.; Sharbrough,
506
10.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
Magnetic Resonance Imaging 0 Volume 9, Number 4, 1991 Temporal lobe volume measurements from MR images: Accuracy and left-right asymmetry in normal persons. J. Comput. Assist. 12:21-29; 1988. Suddath, R.L.; G.W.; Torrey, Casanova, Weinberger, D.R. abnormalities in brains of twins discordant schizophrenia. New J Med. 1990. M.M. Schizophrenia the brain. Engi. J. 322:842-845; 1990. Fazekas, F., J.B.; Alavi, Hurtia, H.I.; R.A. MR abnormalities at ST in dementia and aging. AJNR 426; 1987 AJR 149:351-356; Bronen, Kim, H.; G.; Spencer, Sze, G. temporal sclerosis: of hipposize at with neuronal density. Preat the meeting of Society of America, Chicago, 1989. R.; de Sayette, V.; R.; et Magnetic imaging in lobe epilepsy: correlations. Ann. 22:341-347; 1987. McLachlan, R.S.; Nicholson, R.L.; Black, S.; Carr, T.; Blume, W.T. Nuclear magnetic resonance imaging, a new approach to the investigation of refractory temporal lobe epilepsy. Epilepsia 26:555-562; 1985. Jack, C.R.; Sharbrough, F.W.; Twomey, C.K.; et al. Temporal lobe seizures: Lateralization with MR volume measurements of the hippocampal formation. Radiofogy 175:423-429; 1990. Newcombe, R.L.; Shah, S.H. Radiological abnormalities in temporal lobe epilepsy with clinicopathological correlations. J. Neurol. Neurosurg. Psychiatr. 38:279287; 1975. McRae, D.L. Focal epilepsy: Correlation of the pathological and radiological findings. RadioZogy 50:439-457; 1948. Turner, D.W.; Wyler, A.R. Temporal lobectomy for epilepsy: Mesial temporal herniation as an operative and prognostic finding. Epilepsia 22:623-629; 1981. Bolender, N.F.; Wyler, A.R. CT measurements of mesial temporal lobe herniation in epileptics. Epilepsia 23: 409-416; 1982. Wyler, A.R.; Bolender, N.F. Preoperative CT diagnosis of mesial temporal sclerosis for surgical treatment of epilepsy. Ann. Neurol. 13:59-64; 1983. Silver, A.J.; Cross, D.T.; Friedman, D.P.; Belle, J.A.; Hilal, S.K. Medial temporal lobe: Choroid fissure cysts and hippocampal sclerosis. Presented at 75th annual meeting of Radiological Society of North America, Chicago, November 1989, p. 287. Theodore, W.H.; Dorwart, R.; Homes, M.; Porter, R.J.; DiChiro, G. Neuroimaging in refractory partial seizures: Comparison of PET, CT, and MRI. Neurology 36:750-759; 1986. Brooks, B.S.; King, D.W.; El Gammal, T.; et al. MR imaging in patients with intractable complex partial epileptic seizures. AJNR 11:93-99; 1990. Jack, C.R.; Twomey, C.K.; Zinmeister, A.R.; Shar-
26. 27.
28.
29.
30.
31.
32.
33.
34.
35.
36. 37.
38.
39.
40. 41.
F.W.; Petersen, Cascino, G.D. temporal lobes hippocampal formations: volumetric measurements MR images young adults. 1721549-554; 1989. Lencz, T.; G. ; Bronen, R.; Inserni, J.; Kim, J.H.; Spencer, D.D. The hippocampus in temporal lobe epilepsy: Correlation of pre-surgical MRI volumetrics with post-surgical cell counts. EpiZepsia31667-668; 1990. Bronen, R.A.; Cheung, G. MRI of the normal hippocampus. Magn. Resort. Imaging 9(4):497-500; 1991. Bronen, R.A.; Cheung, G. Relationship of the hippocampus and amygdala to coronal MRI landmarks. Magn. Resort. Imaging 9(3):449-457; 1991. Naidich, T.P.; Daniels, D.L.; Haughton, F.M.; et al. Hippocampal formation and related structures of the limbic lobe: Anatomic-MR correlation. Part I. Surface features and coronal sections. Radiology 162:747-754; 1987. Geschwind, N.; Levitsky, W. Human brain: Left-right asymmetries in temporal speech region. Science 161: 186-187; 1968. Galaburda, A.M.; LeMay, M.; Kemper, T.L.; Geschwind, N. Right-left asymmetries in the brain. Structural differences between the hemispheres may underlie cerebral dominance. Science 199:852-856; 1978. Galaburda, A.M.; Sanides, F.; Geschwind, N. Human brain. Cytoarchitectonic left-right asymmetries in the temporal speech region. Arch. Neural. 35:812-817; 1978. Wada, J.A.; Clarke, R.; Hamm, A. Cerebral hemispheric asymmetry in humans. Cortical speech zones in 100 adult and 100 infant brains. Arch. Nemo/. 32:239246; 1975. Ratcliff, G.; Dila, C.; Laughlin, T.; Milner, B. The morphological asymmetry of the hemispheres and cerebral dominance for speech: A possible relationship. Brain and Language 11:87-98; 1980. LeMay, M.; Kido, D.K. Asymmetries of the cerebral hemispheres on computed tomograms. J. Comput. Assist. Tomogr. 2:471-476; 1978. Shapiro, R.; Galloway, S.J.; Shapiro, M.D. Minimal asymmetry of the brain: A normal variant. AJR 147: 753-756; 1986. Hadziselimovic, H. Asymmetry of the human brain. J. Mrnforsch 2 1:265-270; 1980. Weinberger, D.R.; Luchins, D.J.; Morihisa, J.; Wyatt, R.J. Asymmetrical volumes of the right and left frontal and occipital regions of the human brain. Neurol. 11: 97-100; 1982. LeMay, M.; Culebras, A. Human brain: Morphologic differences in the hemispheres demonstrable by carotid arteriography. New Engl. J. Med. 287:168-170; 1972. Rubens, A.L.; Mahowalk, M.W.; Hutton, J.T. Asymmetry of the lateral (Sylvian) fissures in man. Neurology 26:620-624; 1976. Hochberg, F.H.; LeMay, M. Arteriographic correlates of handedness. Neurology 25:218-222; 1974. LeMay, M. Radiological, developmental, and fossil asymmetries. In: Geschwind, N.; Galaburda, A.M.
MR of the temporal lobe 0 R.A. BRONEN AND G. CHEUNG (Eds.), Cerebral Dominance. The Biological Foundations. Cambridge: Harvard University Press; 1984:~~. 26-42. 42. Earle, KM.; Baldwin, M.; Penfield, W. Incisural sclerosis and temporal lobe seizures produced by hippocampal herniation at birth. Arch. Neural. Psych. (AMA) 69~21-42; 1953. 43. Schwarz, G.A.; Rosner, A.A. Displacement and herni-
ation of the hippocampal gyrus through the incisura tentorii. A clinicopathologic study. Arch. Neurol. Psych. 46:297-321; 1941. 44. El Gammal, T.; Adams, R.J.; King, D.W.; So, E.L.; Gallagher, B.B. Modified CT techniques in the evaluation of temporal lobe epilepsy prior to lobectomy. AJNR 8:131-134;
507
48. Habib, M.; Renucci, R.L.; Vanier, M.; Corbaz, J.M.; Salamon, G. CT assessment of right-left asymmetries in the human cortex. J. Comput. Assist. Tomogr. 8:922927; 1984. 49. Last, R.J.; Thompsett, D.H. Casts of cerebral ventricles. Brit. J. Surg. 40~525-542; 1953. 50. Gyldensted, C. Measurements of the normal ventricu-
51.
52.
1987.
45. Quest, D.O. Increased intracranial pressure, brain herni-
lar system and hemispheric sulci of 100 adults with computed tomography. Neuroradiology 14:183-192; 1977. Schwartz, M.; Creasey, H.; Grady, C.L.; et al. Computed tomographic analysis of brain morphometrics in 30 healthy men, aged 21-81 years. Ann. Neurol. 17:146157; 1985. Zatz, L.M.; Jernigan, T.L.; Ahumada, A.J. Changes on computed cranial tomography with aging: Intracranial fluid volume. AJNR 3:1-11; 1982. Hobar, J.D.; Leahy, K.A.; Lucey, J.F. Ultrasound identification of lateral ventricular asymmetry in the human neonate. J. Clin. Ultrasound 11:67-69; 1983. Castorina, G.; McRae, D.L. Radiology findings in temporal lobe epilepsy of non-tumoral origin. Acta Radiol.
ation, and their control. In: Wilkins, R.H.; Rengachary, S.S. (Eds.), Neurosurgery. New York: McGraw-Hill; 1985:~~. 332-342. 46. Falconer, M.A.; Serafetinides, E.A.; Corsellis, J.A.N. Etiology and pathogenesis of temporal lobe epilepsy.
53.
Arch. Neurol. 10:238-248; 1964. 47. George, A.E. ; de Leon, M. J.; Stylopoulos,
[DiagnJ (Stand.) 1:541-557; 1963. 55. Duncan, R.; Patterson, J.; Hadley, D.M.; et al. CT,
L.A.; et al. CT diagnostic features of Alzheimer’s disease: Importance of choroidal/hippocampal fissure complex. AJNR 1 l:lOl-107:
1990.
54.
MR, and SPECT imaging in temporal lobe epilepsy. J. Psychiatr. 53: 11-15; 1990.
Neuroi. Neurosurg.
Imaging. Vol. 9. pp. 501-507, All rights reserved.
1991 Copyright
0730-725X/91 $3.00 + .OO 0 1991 Pergamon Press plc
l Original Contribution
MRI OF THE TEMPORAL LOBE: NORMAL WITH SPECIAL REFERENCE TOWARD RICHARD Department
A. BRONEN AND GORDON
VARIATIONS, EPILEPSY
CHEUNG*
of Diagnostic Radiology, Yale University School of Medicine, New Haven, CT
Recent investigations of epilepsy, Alzheimer’s disease, amnesia, and schizophrenia have used magnetic resonance imaging (MRI) to evaluate changes in temporal lobe structures. Normal variations in these structures need to be defined before one can use these structures to describe abnormal conditions. Twenty-nine normal volunteers were studied by coronal MRI. Frequent findings include notching of the uncus by the tentorium or adjacent vessels (22/29) and asymmetry of the temporal horns (20/29). This finding of uncal notching strengthens the evidence against “incisural sclerosis” as the basis for hippocampal sclerosis. Temporal horn dilatation occurred in four. However, mild asymmetry of the temporal horn was seen frequently at its anterior tip (16/29) and may be related to head rotation. Asymmetry of the choroidal fissure was never marked. Mild asymmetry was common at the hippocampal head (pes). Mild enlargement of the right temporal lobe by visual inspection is not uncommon. Subtle asymmetry of the white matter between the hippocampus and the collateral sulcus occurred in six. The collateral sulcus does not always point to the temporal horn. The occipitotemporal sulcus may point to the temporal horn. Asymmetric uncal protrusion (O/29) and Sylvian fissure dilatation (4/29) occur rarely.
Keywords: Choroidal fissure; Magnetic resonance; Sylvian fissure; Temporal horn; Temporal lobe; Uncus.
INTRODUCTION
pocampal sclerosis has been associated with a small hyperintense hippocampus, a small temporal lobe, uncal protrusion and associated notching, collateral white matter atrophy, choroidal fissure abnormalities, temporal horn enlargement, and Sylvian fissure dilatation.4s’2-23 MR of the normal hippocampus has already been described. 24-26This report focuses on asymmetry of temporal lobe, uncus, collateral white matter, choroidal fissure, temporal horn, and Sylvian fissure.
Temporal lobe structures have been the focus of attention because of their association with memory, language, and seizure propagation. l-6 Anatomic detail of the temporal lobe by magnetic resonance imaging (MRI) is clearly superior to other imaging modalities.7*8Thus, recent investigations of epilepsy, Alzheimer’s disease, amnesia, and schizophrenia have all used MRI to qualitatively or quantitatively analyze temporal lobe structures. 3,4.9-‘5Before one can analyze pathologic processes by MRI, variations occurring in normal populations should be considered. The purpose of this communication is to establish normative data for temporal lobe structures. Due to our interest in temporal lobe epilepsy and hippocampal sclerosis, we focused our attention on structures which have been reported to be altered in these entities. Although the literature can be conflicting at times, hip-
METHODS Description of subjects and MR technique has been previously reported. 27 Symmetry of six anatomic regions were investigated by visual inspection by two neuroradiologists: temporal lobe, uncus, collateral white matter, choroidal fissure, temporal horn (along with body of lateral ventricle), and Sylvian fissure
RECEIVED12/S/90; ACCEPTED2/25/91. *Present address: Sunnybrook Health Science Centre, University of Toronto, Department of Diagnostic Radiology, 2075 Bayview Avenue, New York, Ontario, Canada M4N 3M5.
Address ail correspondence to Richard A. Bronen, M.D., Yale University School of Medicine, Department of Diagnostic Radiology, 333 Cedar Street, New Haven, CT 06510, USA. 501
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(Fig. 1). Head rotation was evaluated by assessing symmetry of internal auditory canals* and the anterior aspects of the atria (of the lateral ventricles). Temporal lobe was assessed by comparing the left and right temporal lobes from the anterior temporal tip back through the level of the brainstem. Boundaries of the temporal lobes were defined according to established precedent. ‘~4 Natural margins are formed by the Sylvian fissure, circummesencephalic cistern, choroidal fissure/temporal horn complex and the bony cranium. Completing the medial border of the temporal lobe is a line through the temporal stem connecting the inferior fork of the Sylvian fissure to the superiolateral aspect of the choroidal fissure/temporal horn complex. Rating criteria consisted of (i) no asymmetry, (ii) subtle or questionable asymmetry, and (iii) definite asymmetry. Asymmetric protrusion or herniation of uncus was assessed, as compared to a sag&al plane bisecting the third ventricle. Notching of the uncus was also studied. Grading consisted of the following categories: (i) no notching or questionable notching; (ii) left-sided notching, (iii) right-sided notching, or (iv) bilateral notching. The collateral white matter (CWM) is defined as the white matter situated between the collateral sulcus gray matter and the hippocampus just medial to the collateral eminence (Fig. 1). The “choroidal fissure” refers to the cerebrospinal fluid (CSF) space superior
Fig. 1. Coronal diagram of the right medial temporal lobe. The collateral white matter (CWM) is defined as the white matter situated between the hippocampus and the cortex overlying the collateral sulcus. The choroidal fissure (Ch) height is evaluated at the midpoint of the hippocampus. The choroidal fissure communicates with the transverse fissure (TF) and the ambient or circummesencephalic cistern (AC). LOTG = lateral occipitotemporal gyrus, PHG = parahippocampal gyrus, TH = temporal horn.
the hippocampal formation.28 The degree of enlargement of the Sylvian fissures was assessed. Specifically, the degree of fissure dilatation on the left was compared to the right (Fig. 2). The length and height of the fissure were not evaluated. Temporal horn was investigated by first assessing for dilatation. This is distinct from mild asymmetry which was also studied. The bodies of the lateral ventricles were also assessed for asymmetry. to
RESULTS
Temporal Lobe Both observers agreed that the anterior temporal lobes were symmetric in size in 16 subjects. In another 8 subjects, at least one observer felt the left temporal lobe was smaller (Fig. 3). Disparate findings by the observers occurred in three additional subjects. Temporal lobe asymmetry could not be reliably assessed in two studies due to the degree of rotation.
uncus Asymmetric uncal protrusion/herniation was not observed. Uncal notching was seen in 22 subjects, 18 bilateral (Fig. 2). Unilateral notching was left-sided in three and right-sided in one. Variations in the degree
Fig. 2. Coronal short TR image at the junction of amygdala with hippocampai head. The amygdala (a) and uncus (u) appear as one continuous mass of gray. Bilateral notching (white arrow) of the uncus by the tentorium (or vasculature) is a normal finding. Bilateral symmetric bulging of the uncus medially into the suprasellar cistern is also a normal finding. Asymmetry of the anterior temporal horn (t) is frequently found in normal subjects as the ventricle insinuates itself between the amygdala and hippocampus. Sylvian fissure dilatation is measured between the large black arrows and is usually symmetric. CWM (small black arrow) height is symmetric. The collateral sulcus (small curved arrow) points toward the temporal horn.
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Table 1.
Symmetry Temporal lobe* Uncus CMW*** Choroidal fissure Temporal horn Sylvian fissure
16 29 23 18 9 25
Mild asymmetry 1** 0 5 II 16 4
*3 cases-disparate findings; 2 cases-not marked head rotation. **By at least one observer. ***Collateral white matter. Fig. 3. Coronal short TR images through the anterior temporal lobe. The left anterior temporal lobe is smaller than the right. Figure 4, illustrating a more posterior image in the same study, confirms that this is not due to head rotation.
of the uncus was common. Often, it could not be determined whether the notch was due to the tentorium or an associated vessel.
of notching
Collateral White Matter Definite asymmetry of CWM was seen in one subject, subtle or questionable asymmetry in 5, while no asymmetry was seen in 23 (Figs. 2, 4). The collateral sulcus was not always the dominant sulcus pointing to
Fig. 4. Coronal short TR image, posterior to Fig. 3 in the same subject. This plane sections the hippocampus just posterior to the transition of head to body. The left and right choroidal fissure (large arrow), CWM (small arrow), and temporal horns (curved arrow) are symmetric. The temporal horns are usually symmetric posterior to the amygdala/ hippocampal junction. The right collateral sulcus (C) points toward the hippocampus while the occipitotemporal sulcus (0) is directed toward but not at the temporal horn.
Marked asymmetry 1** 0 1 0 4 0 evaluated due to
temporal horn. Not infrequently, the occipitotemporal sulcus with its cortical cap was the largest sulcus pointing to the temporal horn. The collateral sulcus is sometimes directed toward the hippocampal formation rather than the collateral eminence, the floor of the temporal horn. Choroidal Fissure The choroidal fissure height was symmetric in 18/29 subjects (Fig. 4). There was mild asymmetry of the fissure at the level of the hippocampal head in 9/29, with prominence of the right side in 8 of these 9. In only 2/29 was there mild asymmetry of the choroidal fissure posterior to the hippocampal head. The more prominent fissure was on the right in both subjects. Marked asymmetry or dilatation of choroidal fissure was never observed. No choroidal fissure cysts were seen in this group. Temporal Horn There was definite dilatation of the temporal horn in two patients, one left- and one right-sided. In the patient with the right temporal horn dilatation, there was concomitant right lateral body ventricle enlargement. In two patients, there was subtle or questionable temporal horn dilatation on the right side. In one of these, there was ipsilateral enlargement of the body of the lateral ventricle. In 25 subjects there was no significant temporal horn dilatation, but a mild asymmetry occurred in 16. The right side was mildly larger in 15 of these 16. This mild asymmetry often occurred anteriorly, as the temporal horn sweeps medially separating the amygdala from the hippocampal head (Figs. 2, 4). The body of the lateral ventricle was slightly enlarged on the right side in four subjects. In was definitely enlarged on the right in four others, and in two on the left.
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Sylvian Fissure Mild asymmetric dilatation of the Sylvian fissure occurred in 4 of the 29, 3 on the left and 1 on the right (Fig. 2). DISCUSSION Lateralization of brain function is well described. 5*6Certain mo r p hologic differences of the cerebral hemispheres appear to be closely related to the lateralization of brain function.29-33 Other asymmetries which may be related in some manner to handedness are more difficult to link to specific functions, yet are remarkedly consistent.34-37 Inherent cerebral asymmetries in normals can lead to gross miscalculations in the evaluation of disease states if one does not factor in these normal variations. The purpose of this study is to investigate the normal variations of the temporal lobe, particularly the medial portion, with MRI. MRI assessment of temporal lobe structures has recently been used to evaluate amnesia, Alzheimer’s disease, schizophrenia, and epilepsy.3,4,9-‘5 Since our eventual objective is to acquire normative data in order to evaluate imaging of epileptics, we focused our attention on the structures which have been reported to be abnormal in epilepsy, and in particular hippocampal sclerosis. These structures include the hippocampus, temporal lobe, uncus, CWM, choroidal fissure, temporal horn, and Sylvian fissure.4,12-23 Temporal Lobe Indirect support for temporal lobe asymmetry is available from studies of Sylvian fissure position. The vertical height of the temporal lobe, and thus its size on coronal slices, is dependent on Sylvian fissure position. As one proceeds posteriorly, the right Sylvian fissure is usually shorter and higher than the left.32,38-4’ The longer length of the Sylvian fissure on the left appears to be related to the larger planum temporale, which is speculated to be the morphologic substrate of language. 29-33Recent quantitative MRI studies have confirmed temporal lobe asymmetry.8~24*25In righthanded subjects, the anterior portion of the right temporal lobe is larger than the left by a small but statistically significant amount. The mean difference of 2.3 cm3 (4Oro)is probably difficult to appreciate visually. However, the range of differences approaches 20% of the temporal lobe volume, an amount which may be detected visually. 24Our study confirms these findings. The temporal lobes were visually symmetric in most. When asymmetry was visualized, the right temporal lobe was usually Iarger. In patients with temporal lobe epilepsy, asymmetry
of the temporal lobe and middle cranial fossa has been used to lateralize the seizure focus. 13-17*24*25 One must be aware of the inherent differences in normals to interpret these findings correctly. Since the right temporal lobe is frequently larger than the left, a smaller right temporal lobe is a much more significant finding than a smaller left lobe in the evaluation of epilepsy. Uncus It was theorized by Earle et al. that hippocampal sclerosis, or “incisural sclerosis” as they called it, is produced by hippocampal herniation at birth.42 This supposedly transient herniation was thought to cause anoxia to the medial temporal lobe via compression of the anterior choroidal and posterior cerebral arteries. Protrusion of the uncus medial to the tentorial edge, and grooving of the uncus by the tentorium have been used as signs of pathologic uncal herniation.43 Turner and Wyler found herniation of the medial temporal lobe structures in 12 of 16 with hippocampal sclerosis. I8 Although Bolender and Wyler reported CT evidence of medial temporal lobe herniation posteriorly in these same patients, quantitative separation of the “non-herniated” from the “herniated” group could only be obtained by mathematical manipulation of the data. I9320Other studies of epilepsy reported no herniation by either CT or MRI.‘4,44 Our data may help resolve this issue. Asymmetric protrusion of an uncus medially was not seen in any of our 29 volunteers. Notching of the uncus either by the tentorium or an adjacent vessel was seen frequently (76%) in our normal group. Variations exist in the degree of notching. The notching was frequently bilateral. In fact, uncal extension medial to the tentorial edge by 3 to 4 mm and mild grooving of the uncus are normal findings. ‘*45Thus, the uncal notching seen during epilepsy surgery may be unrelated to epilepsy. Since hippocampal sclerosis is an atrophic process, it seems unreasonable that it should be associated with the mass effect implied by uncal herniation. The “incisural sclerosis” theory falters for other reasons, as discussed by Falconer et al., and is not currently in vogue.46 Collateral White Matter Collateral white matter was visually symmetrical in 21 (72%) subjects, questionably asymmetric in 6 (21%) and definitely asymmetric in 2 (70/o). Since CWM asymmetry seen in hippocampal sclerosis may often be subtle,4 the normal population variation should lead one to use this finding as a secondary confirmatory rather than primary sign of hippocampal sclerosis.
MR of the temporal lobe 0 R.A.
The collateral eminence has been described as a bulge in the floor of the temporal horn due to the protrusion of the white and gray matter capping the collateral SU~CUS.‘*~~ Our findings suggest a moderate amount of variation. The collateral sulcus may point to the hippocampal formation rather than the temporal horn, while the occipitotemporal sulcus may point to the temporal horn. Choroidal Fissure Terminology surrounding the choroidal fissure is complex. We will use terms Duvernoy and Naidich et al. have used to describe the CSF spaces associated with the temporal lobe. 1,28The ambient cistern is located between the midbrain and the temporal lobe. Laterally, this cistern is renamed the “transverse fissure” or the “wing of the ambient cistern.” The floor of the transverse fissure is composed of the subiculum, while the roof is formed by the lateral geniculate body and thalamic pulvinar. The choroidal fissure is situated between the transverse fissure and the temporal horn of the lateral ventricle. Two pial layers (tenae) originating from the fimbria and stria semicircularis unite to form the choroid plexus. By strict definition, the choroidal fissure refers only to the region between these two tenae. In common usage and radiologic literature, the choroid fissure refers to the entire CSF space space forming the roof of the hippocampal formation.28 Visually, the choroidal fissure is rarely asymmetric posterior to the hippocampal head. Mild asymmetry at the hippocampal head is not uncommon (strictly speaking, this is the temporal horn, since the choroida1 plexus is not present at the level of the head). ’ This asymmetry was encountered in nine (31%) subjects, almost exclusively on the right side. Silver et al. noted a low association of choroid fissure cysts with epilepsy. 21We did not find any cysts among our normal subjects. CT (and MR) detection of choroidal fissure enlargement has been shown to be highly sensitive for diagnosing Alzheimer’s disease.47 Fissure enlargement appears related to atrophic changes occurring focally in the hippocampus. Sylvian Fissure While reproducible asymmetries of Sylvian fissure length have been reported30~38~39.4’*48 little has been published regarding fissure dilatation. Subtle asymmetric dilatation of the Sylvian fissures occurred in 4 (14%) of our subjects. Sylvian fissure enlargement has not been a particularly useful finding in evaluation of temporal lobe epilepsy. Theodore et a1.22 found unilateral Sylvian fissure enlargement in 2 of 36 epilep-
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tics, while McLachlan et al. l4 noted that this occurred with equal frequency in both epileptics and controls. Temporal Horn Asymmetry of the lateral ventricles and temporal horns in normals has been studied by a variety of methods. The body of lateral ventricle has been found to be larger on the left in 32%-72% of cases studied by pathology,4’*49 pneumoencephalography,41 CT 735so-52and ultrasound.53 During pneumoencephalography, the temporal horn was found to be larger on the left in 6890, and on the right in 11070.~’In our series, unilateral temporal horn dilatation occurred infrequently, in four patients. However, mild asymmetry at the level of the amygdala-hippocampal junction occurs commonly on coronal MR and can often be attributed to head rotation. The temporal horn has its greatest transverse diameter at this location and is known as the uncal recess. With head rotation, the larger uncal recess of one temporal horn may be imaged on the same slice as a smaller, more posterior portion of the contralateral temporal horn. Since mild temporal horn asymmetry appears to be common in normal subjects, one must temper reliance on it for detecting abnormal conditions. With regards to epilepsy and hippocampal sclerosis, the literature has been divided as to the usefulness of temporal horn asymmetry. 4.14,16,17,23.S4.55 REFERENCES 1. Duvernoy, H.M. The Human Hippocampus. An Atlas of Applied Anatomy. Munchen: J.D. Berman Verlag; 1988:~~. l-45. 2. Dam, A.M. Hippocampal neuron loss in epilepsy and after experimental seizures. Actu Neural. Scandinav. 66: 601-642; 1982. 3. Press, G.A.; Amaral, D.G.; Squire, L.R. Hippocampal abnormalities in amnesic patients revealed by high-resolution magnetic resonance imaging. Nature 341:54-57; 1989. 4. Bronen, R.A.; Cheung, G.; Charles, J.T.; et al. Pathologic study of mesial temporal sclerosis: Comparison of scalp EEG, MR, CT and angiography. American Society of Neuroradiology, Orlando, March 19-24, 1989. 5. Geschwind, N. The organization of language and the brain. Science 170:940-944; 1970. 6. Geschwind, N.; Galaburda, A.M. Cerebral Dominance. The Biological Foundations. Cambridge: Harvard University Press; 1984. I. Zhu, X.P.; Checkley, D.R.; Hickey, D.S.; Isherwood, I. Accuracy of area measurements made from MR images compared with computed tomography. J. Comput. Assist. Tomogr. 10:96-102; 1986. F.W.; et al. 8. Jack, C.R.; Gehring, D.G.; Sharbrough,
506
10.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
Magnetic Resonance Imaging 0 Volume 9, Number 4, 1991 Temporal lobe volume measurements from MR images: Accuracy and left-right asymmetry in normal persons. J. Comput. Assist. 12:21-29; 1988. Suddath, R.L.; G.W.; Torrey, Casanova, Weinberger, D.R. abnormalities in brains of twins discordant schizophrenia. New J Med. 1990. M.M. Schizophrenia the brain. Engi. J. 322:842-845; 1990. Fazekas, F., J.B.; Alavi, Hurtia, H.I.; R.A. MR abnormalities at ST in dementia and aging. AJNR 426; 1987 AJR 149:351-356; Bronen, Kim, H.; G.; Spencer, Sze, G. temporal sclerosis: of hipposize at with neuronal density. Preat the meeting of Society of America, Chicago, 1989. R.; de Sayette, V.; R.; et Magnetic imaging in lobe epilepsy: correlations. Ann. 22:341-347; 1987. McLachlan, R.S.; Nicholson, R.L.; Black, S.; Carr, T.; Blume, W.T. Nuclear magnetic resonance imaging, a new approach to the investigation of refractory temporal lobe epilepsy. Epilepsia 26:555-562; 1985. Jack, C.R.; Sharbrough, F.W.; Twomey, C.K.; et al. Temporal lobe seizures: Lateralization with MR volume measurements of the hippocampal formation. Radiofogy 175:423-429; 1990. Newcombe, R.L.; Shah, S.H. Radiological abnormalities in temporal lobe epilepsy with clinicopathological correlations. J. Neurol. Neurosurg. Psychiatr. 38:279287; 1975. McRae, D.L. Focal epilepsy: Correlation of the pathological and radiological findings. RadioZogy 50:439-457; 1948. Turner, D.W.; Wyler, A.R. Temporal lobectomy for epilepsy: Mesial temporal herniation as an operative and prognostic finding. Epilepsia 22:623-629; 1981. Bolender, N.F.; Wyler, A.R. CT measurements of mesial temporal lobe herniation in epileptics. Epilepsia 23: 409-416; 1982. Wyler, A.R.; Bolender, N.F. Preoperative CT diagnosis of mesial temporal sclerosis for surgical treatment of epilepsy. Ann. Neurol. 13:59-64; 1983. Silver, A.J.; Cross, D.T.; Friedman, D.P.; Belle, J.A.; Hilal, S.K. Medial temporal lobe: Choroid fissure cysts and hippocampal sclerosis. Presented at 75th annual meeting of Radiological Society of North America, Chicago, November 1989, p. 287. Theodore, W.H.; Dorwart, R.; Homes, M.; Porter, R.J.; DiChiro, G. Neuroimaging in refractory partial seizures: Comparison of PET, CT, and MRI. Neurology 36:750-759; 1986. Brooks, B.S.; King, D.W.; El Gammal, T.; et al. MR imaging in patients with intractable complex partial epileptic seizures. AJNR 11:93-99; 1990. Jack, C.R.; Twomey, C.K.; Zinmeister, A.R.; Shar-
26. 27.
28.
29.
30.
31.
32.
33.
34.
35.
36. 37.
38.
39.
40. 41.
F.W.; Petersen, Cascino, G.D. temporal lobes hippocampal formations: volumetric measurements MR images young adults. 1721549-554; 1989. Lencz, T.; G. ; Bronen, R.; Inserni, J.; Kim, J.H.; Spencer, D.D. The hippocampus in temporal lobe epilepsy: Correlation of pre-surgical MRI volumetrics with post-surgical cell counts. EpiZepsia31667-668; 1990. Bronen, R.A.; Cheung, G. MRI of the normal hippocampus. Magn. Resort. Imaging 9(4):497-500; 1991. Bronen, R.A.; Cheung, G. Relationship of the hippocampus and amygdala to coronal MRI landmarks. Magn. Resort. Imaging 9(3):449-457; 1991. Naidich, T.P.; Daniels, D.L.; Haughton, F.M.; et al. Hippocampal formation and related structures of the limbic lobe: Anatomic-MR correlation. Part I. Surface features and coronal sections. Radiology 162:747-754; 1987. Geschwind, N.; Levitsky, W. Human brain: Left-right asymmetries in temporal speech region. Science 161: 186-187; 1968. Galaburda, A.M.; LeMay, M.; Kemper, T.L.; Geschwind, N. Right-left asymmetries in the brain. Structural differences between the hemispheres may underlie cerebral dominance. Science 199:852-856; 1978. Galaburda, A.M.; Sanides, F.; Geschwind, N. Human brain. Cytoarchitectonic left-right asymmetries in the temporal speech region. Arch. Neural. 35:812-817; 1978. Wada, J.A.; Clarke, R.; Hamm, A. Cerebral hemispheric asymmetry in humans. Cortical speech zones in 100 adult and 100 infant brains. Arch. Nemo/. 32:239246; 1975. Ratcliff, G.; Dila, C.; Laughlin, T.; Milner, B. The morphological asymmetry of the hemispheres and cerebral dominance for speech: A possible relationship. Brain and Language 11:87-98; 1980. LeMay, M.; Kido, D.K. Asymmetries of the cerebral hemispheres on computed tomograms. J. Comput. Assist. Tomogr. 2:471-476; 1978. Shapiro, R.; Galloway, S.J.; Shapiro, M.D. Minimal asymmetry of the brain: A normal variant. AJR 147: 753-756; 1986. Hadziselimovic, H. Asymmetry of the human brain. J. Mrnforsch 2 1:265-270; 1980. Weinberger, D.R.; Luchins, D.J.; Morihisa, J.; Wyatt, R.J. Asymmetrical volumes of the right and left frontal and occipital regions of the human brain. Neurol. 11: 97-100; 1982. LeMay, M.; Culebras, A. Human brain: Morphologic differences in the hemispheres demonstrable by carotid arteriography. New Engl. J. Med. 287:168-170; 1972. Rubens, A.L.; Mahowalk, M.W.; Hutton, J.T. Asymmetry of the lateral (Sylvian) fissures in man. Neurology 26:620-624; 1976. Hochberg, F.H.; LeMay, M. Arteriographic correlates of handedness. Neurology 25:218-222; 1974. LeMay, M. Radiological, developmental, and fossil asymmetries. In: Geschwind, N.; Galaburda, A.M.
MR of the temporal lobe 0 R.A. BRONEN AND G. CHEUNG (Eds.), Cerebral Dominance. The Biological Foundations. Cambridge: Harvard University Press; 1984:~~. 26-42. 42. Earle, KM.; Baldwin, M.; Penfield, W. Incisural sclerosis and temporal lobe seizures produced by hippocampal herniation at birth. Arch. Neural. Psych. (AMA) 69~21-42; 1953. 43. Schwarz, G.A.; Rosner, A.A. Displacement and herni-
ation of the hippocampal gyrus through the incisura tentorii. A clinicopathologic study. Arch. Neurol. Psych. 46:297-321; 1941. 44. El Gammal, T.; Adams, R.J.; King, D.W.; So, E.L.; Gallagher, B.B. Modified CT techniques in the evaluation of temporal lobe epilepsy prior to lobectomy. AJNR 8:131-134;
507
48. Habib, M.; Renucci, R.L.; Vanier, M.; Corbaz, J.M.; Salamon, G. CT assessment of right-left asymmetries in the human cortex. J. Comput. Assist. Tomogr. 8:922927; 1984. 49. Last, R.J.; Thompsett, D.H. Casts of cerebral ventricles. Brit. J. Surg. 40~525-542; 1953. 50. Gyldensted, C. Measurements of the normal ventricu-
51.
52.
1987.
45. Quest, D.O. Increased intracranial pressure, brain herni-
lar system and hemispheric sulci of 100 adults with computed tomography. Neuroradiology 14:183-192; 1977. Schwartz, M.; Creasey, H.; Grady, C.L.; et al. Computed tomographic analysis of brain morphometrics in 30 healthy men, aged 21-81 years. Ann. Neurol. 17:146157; 1985. Zatz, L.M.; Jernigan, T.L.; Ahumada, A.J. Changes on computed cranial tomography with aging: Intracranial fluid volume. AJNR 3:1-11; 1982. Hobar, J.D.; Leahy, K.A.; Lucey, J.F. Ultrasound identification of lateral ventricular asymmetry in the human neonate. J. Clin. Ultrasound 11:67-69; 1983. Castorina, G.; McRae, D.L. Radiology findings in temporal lobe epilepsy of non-tumoral origin. Acta Radiol.
ation, and their control. In: Wilkins, R.H.; Rengachary, S.S. (Eds.), Neurosurgery. New York: McGraw-Hill; 1985:~~. 332-342. 46. Falconer, M.A.; Serafetinides, E.A.; Corsellis, J.A.N. Etiology and pathogenesis of temporal lobe epilepsy.
53.
Arch. Neurol. 10:238-248; 1964. 47. George, A.E. ; de Leon, M. J.; Stylopoulos,
[DiagnJ (Stand.) 1:541-557; 1963. 55. Duncan, R.; Patterson, J.; Hadley, D.M.; et al. CT,
L.A.; et al. CT diagnostic features of Alzheimer’s disease: Importance of choroidal/hippocampal fissure complex. AJNR 1 l:lOl-107:
1990.
54.
MR, and SPECT imaging in temporal lobe epilepsy. J. Psychiatr. 53: 11-15; 1990.
Neuroi. Neurosurg.