The Neuroradiology Journal 20: 218-223, 2007
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Thalamic Changes in Mesial Temporal Sclerosis: a Limbic System Pathology A Case Report F. CARANCI, F. BARTIROMO, L.CIRILLO, A. AIELLO, S. CIRILLO*, A. BRUNETTI Neuroradiology Department, “Federico II” University of Naples; Italy * Neuroradiology Department, Second University of Naples; Italy
Key words: temporal lobe epilepsy, mesial temporal sclerosis, thalamus, magnetic resonance imaging
SUMMARY – Hippocampal abnormalities correlated with mesial temporal sclerosis (MTS) are well documented. MTS may be associated with extrahippocampal anomalies involving limbic structures along a known neuroanatomic pathway (Papez circuit). We report a patient with MTS and thalamic changes. Seizure-related thalamic damage could have been caused by abnormal electric discharges from the mamillary body to the anterior thalamus through the mamillothalamic tract. This suggests that MTS is not limited to the temporal lobe but could represent a limbic system pathology.
Introduction Temporal lobe epilepsy (TLE) is the most common form of pharmacoresistent epilepsy, and it is often associated with mesial temporal sclerosis (MTS) 1,2. MTS is histologically characterized by neuronal loss and fibrillary gliosis in the pyramidal cell layer of Ammon’s horn, with resulting atrophy of the hippocampus (3). TLE magnetic resonance imaging (MRI) findings are well documented 4,5,6. Despite the many neuroimaging studies on characteristic hippocampal findings in MTS and epilepsy, relatively few neuroimaging reports have addressed the extrahippocampal abnormalities, including the limbic system 7,8. These data may be useful for the diagnosis of lateralization in presurgical studies of bilateral MTS. The aim of this article is to describe the extrahippocampal anomalies related to MTS, particularly those involving the thalamus, and to discuss their origin. Case Report The patient was a 42-year-old woman with a history of medically intractable complex partial seizures. 218
Because of such complex partial seizures, a MR study was performed by a 1.5 T MR unit. The pulse sequences included T2-weighted spin-echo acquisitions on the axial plane parallel to the intercommisural line and on the coronal plane perpendicular to the long axis of the hippocampus (TR 4200, TE 100, thickness 3 mm, spacing 2 mm, FOV 24 cm, matrix 256 × 256); FLAIR on the axial plane (TR 9000, TE 98, thickness 5 mm, FOV 24 cm, matrix 256 × 256). A spectroscopic examination was performed using a PRESS single voxel technique (TE 35 and 144 ms); voxel of 2.0 cm3 was localized in the right thalamic region and in the controlateral region. MRI showed an unequivocal volume loss of the right thalamus bulk (figure 1), with a consequent ipsilateral ventricular enlargement. The anterior thalamus generally produced a convexity in the lateral ventricle posteriorly to the foramen of Monro, varying from a slight bulge to a prominent tubercle (figure 2) 16. The more posterior mediodorsal complex generally produced a convex contour (figure 2). In our case asymmetry of these contours was noted: the anterior and mediodorsal nuclei were markedly flattened or concave (figure 2).
F. Caranci
Thalamic Changes in Mesial Temporal Sclerosis: a Limbic System Pathology
A
B
➤ C
D
Figure 1 Axial T2-weighted (A,C) and FLAIR images (B,D). Marked atrophy and hyperintense signal involving the right thalamus, with consensual ventricular enlargement. The left mamillothalamic tract (C, arrow) shows a normal signal.
Moreover T2-weighted images showed a high signal involving the affected thalamus, not only in the medial nucleus but extending through the anterior part and more evident in the lateral nucleus (figure 1A). Volume loss and a high signal on T2-weighted images of the right hippocampus, representing MTS, was noted, associated with a mild enlargement of the ipsilateral temporal horn (fi-
gure 3). Atrophy of the ipsilateral column of the fornix (figure 3) was also present, less evident at the level of the body. Spectroscopic examination (in spite of the low signal-to-noise ratio) (figure 4), showed a mild reduction of Naa in the right thalamic region (Naa/Cr 1.46 short TE; 1.99 long TE) compared with the controlateral side (Naa/Cr 1.89 short TE; 2.31 long TE). 219
Thalamic Changes in Mesial Temporal Sclerosis: a Limbic System Pathology
F. Caranci
A
✢
➤
✢
➤
Table 1 Anatomy of the limbic system and circuit of Papez.
B
Figure 2 Coronal T2-weighted images. A,B) Physiologic convexity of the left thalamus toward the lateral ventricle, posteriorly to the foramen of Monro (arrow); flattened upper border of the right anterior thalamus (star, A) and of the more posterior mediodorsal complex (star, B).
Discussion In 1937 a closed system, now known as the circuit of Papez 9 (table1), was described linking the hippocampus, fornix, mamillary body, thalamus and cingulum. This circuit was hypothesized as an essential part of the structural basis of memory and emotion. Fibers from the hippocampal formation, in220
cluding the hippocampus (cornu ammonis and dentate gyrus) and parahippocampal structures (subiculum), contribute to the alveus, which medially coalesces to form the fimbria 9 . The fimbria forms the arching fornix, which projects mainly to the mamillary body via the postcommissural fornix. The circuit is completed by connections from the mamillary body to the anterior thalamic nucleus via the mamil-
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The Neuroradiology Journal 20: 218-223, 2007
➤
A
B
Figure 3 Coronal T2-weighted images (A-B). Volume loss and high signal in the right hippocampus; modest enlargement of the ipsilateral temporal horn. Ipsilateral forniceal atrophy, more evident at level of the columns (arrows).
Figure 4 1HMR spectroscopy. A) Voxel on the right thalamus (TE 35 ms; TE 144 ms). B) Voxel on the left thalamus (TE 35 ms; TE 144 ms).
221
Thalamic Changes in Mesial Temporal Sclerosis: a Limbic System Pathology
lothalamic tract (MTT) 22, with a minor contribution directly from the fornix and the anterior thalamic nucleus to the cingulate gyrus via the thalamocingulate fibers (table 1) 10. More recent anatomic investigations have contributed to find many intrinsic connections between the hippocampal formation and the enthorinal cortex (located in the anterior part of the parahippocampal gyrus) 10,11,12 and to show that most of the efferent forniceal fibers originate from the subiculum and not from the hippocampus. Recent studies have identified thalamic volume loss in patients with TLE 13, and changes in the anterior thalamus in patients with mesial temporal sclerosis, detected by MRI 14 or seen post mortem, after temporal lobectomy 15. Besides a natural thalamic asymmetry 13, particularly in its posterior part 17, there are currently two hypotheses explaining ipsilateral thalamic atrophy due to the changes in MTS: excitotoxicity and transneuronal damage. Excitotoxicity is described as the mechanism of neuronal damage related to overproduction of excitatory amino-acid neurotransmitters. This concept is supported by animal model studies: limbic seizures and subsequent extrahippocampal changes, confirmed in histopathologic examination, were induced by systemic injection of excitatory amino-acid neurotransmitters, such as glutamate and kainic acid (an analogue of glutamate) 18,19. Abnormal electric activity, effect of repeated seizures, can propagate along a pathway (such as the Papez circuit) to achieve target efferent structures (fornix, mamillary body, thalamus). Many recent spectroscopic studies have tried to confirm this hypothesis by depicting metabolic changes, particularly increased levels of glutamate and glutamine 20. Oikawa et Al reported that the lack of signal changes or abnormalities in MTT may be more suggestive of excitotoxicity rather than transneuronal degeneration. MTT is identifiable on axial PD and T2 weighted images as a low signal in the anterior thalamus 22 (figure 1C). Thalamus atrophy may also be a result of hippocampal transneuronal degeneration following MTS or temporal lobectomy 21. Moreover, thalamic degeneration may be secondary to an abnormal developmental process, in association with MTS and global cerebral hemiatrophy 25. Histopathologic analysis has shown that the increased signal
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intensity of the anterior temporal lobe in MTS is not associated with dysplasia or gliosis, but represents a persisting developmental stage with immature myelin and immature cells as a consequence of early seizures 26. Interestingly, abnormalities along the Papez circuit, not only in efferent structures of the pathway (such as thalamus, fornix, mamillary body and cingulum gyrus), but also in major afferent structures (parahippocampal gyrus, including subiculum and enthorinal cortex) have been reported. The origin of the post-commissural forniceal fibers from the subiculum and not from Ammon’s horn has been established 27. This could explain why fornix and mamillary changes are less frequent than those in the hippocampus in MTS. The variable percentable of fornix atrophy reported (39-94%) 8,14 may be also due to different MRI techniques and measurement criteria. The fornix should be considered in all its parts, including body, crura and columns, using multiplanar thin slice images to avoid the effects of physiologic asymmetry. Various parahippocampal gyrus injuries, such as herpes encephalitis 28 or surgical changes (temporal lobectomy reported in 1%) 29, can cause abnormalities in the Papez circuit. Chan et Al found a correlation between MTS and many other findings; they reported cerebral hemiatrophy, amygdalar sclerosis, gliosis of the anterior temporal lobe and cerebellar diaschisis 14. Conclusions The correlation between limbic system abnormalities and clinical pathway is not clear. The extent and severity do not seem to correlate with the clinical severity: some authors have found that patients with extensive limbic system anomalies maybe well controlled, whereas patients with only parahippocampal changes show refractory epilepsy 30. Even if the Papez circuit is considered a major anatomical substrate for emotion and memory, neurologic deficits are not observed. Nevertheless, the detection of limbic system anomalies can be useful in increasing the confidence of lateralization in presurgical studies of bilateral MTS. The identification of thalamic changes could add explanations about the anatomy and possible modality of propagation of TLE.
www. centauro. it
The Neuroradiology Journal 20: 218-223, 2007
References 1 Pasquier B, Peoc’h M, Barnoud R et Al: Prédilection lésionnelle pour le lobe temporal dans l’épilepsie partielle pharmaco-résistante : aspect neuropathologique d’une série de 180 patients. Boll Lega It Epil 95: 57-64, 1996. 2 Jackson GD, Berkovic SF, Tress BM et Al: Hippocampal sclerosis can be reliably detected by magnetic resonance imaging. Neurology 40: 1869-75; 1990. 3 Honavar M, Meldrum BS: Epilepsy. In: Graham DI, Lantos PL(eds) Greenfield’s neuropathology, 6th ed. Arnold, London 1998: 931-971. 4 Berkovic SF, Andermann F, Olivier A et Al: Hippocampal sclerosis in temporal lobe epilepsy demonstrated by magnetic resonance imaging. Ann Neurol 29: 175-182, 1991. 5 Bronen RA, Cheung GC, Charles JT et Al: Imaging findings in hippocampal sclerosis: correlation with pathology. Am J Neuroradiol 12: 933-940, 1991. 6 Bronen RA: Epilepsy: the role of MR imaging. Am J Radiol 159: 1165-1174, 1992. 7 Meiners LC, van Gils A, Jansen GH et Al: Temporal lobe epilepsy: the various MR appearances of histologically proven mesial temporal sclerosis. Am J Neuroradiol 15: 1547-1555, 1994. 8 Baldwin GN, Tsuruda JS, Maravilla KR et Al: Fornix in patients with seizures caused by unilateral hippocampal sclerosis: detection of unilateral volume loss on MR images. Am J Radiol 162: 1185-1189, 1994. 9 Papez JW: A proposed mechanism of emotion. Arch Neurol Psychiatry 38: 725-743, 1937. 10 Martin JH: Neuroanatomy: Text and atlas. New York, NY: Elsevier 1989: 375-395. 11 Carpenter MB: Core text of neuroanatomy ,4th edn. Williams & Williams , Baltimore 1991: 361-386. 12 Mai JK, Assheuer J, Paxinos G: Atlas of the human brain. Academic Press, San Diego 1997: 80-83. 13 De Carli C, Hatta J, Fazilat S et Al: Extra temporal atrophy in patients with complex partial seizures of left temporal origin. Ann Neurol 43: 41-45, 1998. 14 Chan S, Erickson JK, Yoon SS: Limbic system abnormalities associated with mesial temporal sclerosis: a model of chronic cerebral changes due to seizures. Radiographics 17: 1095-1110, 1997. 15 Mamourian AC, Cho CH, Saykin AJ et Al: Association between size of the lateral ventricle and asymmetry of the fornix in patients with temporal lobe epilepsy. Am J Neuroradiol 19: 9-13, 1998. 16 Nieuwenhuys R, Voogd J, van Huijzen C: The human central nervous system. A synopsis and atlas. 3rd ed. Springer, Berlin Heidelberg New York 1988: 71-91. 17 Eidelberg D, Galaburda AM: Symmetry and asymmetry in the human posterior thalamus I. Cytoarchitecture analysis in normal persons. Arch Neurol 39: 325332, 1982. 18 Schwob JE, Fuller T, Price TL et Al: Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study. Neuroscience 5: 991-1014, 1980. 19 Lothman EW, Collins RC: Kainic acid induced limbic seizures: metabolic, behavioral, electroencephalographic and neuropathological correlates. Brain Res 218: 299-318, 1981. 20 Fazekas F, Kapeller P, Schmidt R et Al: Magnetic resonance imaging and spectroscopy findings after focal status epilepticus. Epilepsia 36: 946-949; 1995. 21 Van Buren JM, Borke RC: Variations and connections of the human thalamus. Springer, Berlin Heidelberg New York 1972: 60-65. 22 Wirth BA: MR imaging of the mamillothalamic tract. Presented at the 80th Scientific Assembly and Annual Meeting of the Radiological Society of North America, Chicago 1994. 23 Yamada K, Shrier DA, Rubio A et Al: MR imaging of
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25
26
27 28
29
30
the mamillothalamic tract. Radiology 207: 593-598, 1998. Ogawa T, Yoshida Y, Okudera T et Al: Secondary thalamic degeneration after cerebral infarction in the middle cerebral artery distribution: evaluation with MR imaging. Radiology 204: 255-262, 1997. Dix JE, Cail WS: Cerebral hemiatrophy: classification on the basis of MR imaging findings of mesial temporal sclerosis and childhood febrile seizures. Radiology 203: 269-274, 1997. Briellmann RS, Syngeniotis A, Fleming S et Al: Increased anterior temporal lobe T2 times in cases of hippocampal sclerosis: a multi-echo T2 relaxometry study at 3 T. Am J Neuroradiol 25: 389-394, 2004. Swanson LW, Cowan WM: Hippocampo-hypothalamic connections: origin in subicular cortex, not Ammon’s horn. Science 189: 303-304, 1975. Kapur N, Barker S, Burrows EH et Al: Herpes simplex encephalitis ; long term magnetic resonance imaging and neuropsichological profile. J Neurol Neurosurg Psychiatry 57: 1334-1342, 1994. Kim JH, Tien RD, Felsberg GJ et Al: Clinical significance of asimmetry of the fornix and mamillary body on MR in hippocampal sclerosis. Am J Neuroradiol 16: 509-515, 1995. Oikawa H, Sasaki M et Al: The circuit of Papez in mesial temporal sclerosis. Neuroradiology 43: 205-210, 2001.
Dr Ferdinando Caranci Cattedra di Neuroradiologia Università Federico II Via Pansini 5 80131 Naple, Italy Tel.: 081 7462563 E-mail: [email protected]
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Thalamic Changes in Mesial Temporal Sclerosis: a Limbic System Pathology A Case Report F. CARANCI, F. BARTIROMO, L.CIRILLO, A. AIELLO, S. CIRILLO*, A. BRUNETTI Neuroradiology Department, “Federico II” University of Naples; Italy * Neuroradiology Department, Second University of Naples; Italy
Key words: temporal lobe epilepsy, mesial temporal sclerosis, thalamus, magnetic resonance imaging
SUMMARY – Hippocampal abnormalities correlated with mesial temporal sclerosis (MTS) are well documented. MTS may be associated with extrahippocampal anomalies involving limbic structures along a known neuroanatomic pathway (Papez circuit). We report a patient with MTS and thalamic changes. Seizure-related thalamic damage could have been caused by abnormal electric discharges from the mamillary body to the anterior thalamus through the mamillothalamic tract. This suggests that MTS is not limited to the temporal lobe but could represent a limbic system pathology.
Introduction Temporal lobe epilepsy (TLE) is the most common form of pharmacoresistent epilepsy, and it is often associated with mesial temporal sclerosis (MTS) 1,2. MTS is histologically characterized by neuronal loss and fibrillary gliosis in the pyramidal cell layer of Ammon’s horn, with resulting atrophy of the hippocampus (3). TLE magnetic resonance imaging (MRI) findings are well documented 4,5,6. Despite the many neuroimaging studies on characteristic hippocampal findings in MTS and epilepsy, relatively few neuroimaging reports have addressed the extrahippocampal abnormalities, including the limbic system 7,8. These data may be useful for the diagnosis of lateralization in presurgical studies of bilateral MTS. The aim of this article is to describe the extrahippocampal anomalies related to MTS, particularly those involving the thalamus, and to discuss their origin. Case Report The patient was a 42-year-old woman with a history of medically intractable complex partial seizures. 218
Because of such complex partial seizures, a MR study was performed by a 1.5 T MR unit. The pulse sequences included T2-weighted spin-echo acquisitions on the axial plane parallel to the intercommisural line and on the coronal plane perpendicular to the long axis of the hippocampus (TR 4200, TE 100, thickness 3 mm, spacing 2 mm, FOV 24 cm, matrix 256 × 256); FLAIR on the axial plane (TR 9000, TE 98, thickness 5 mm, FOV 24 cm, matrix 256 × 256). A spectroscopic examination was performed using a PRESS single voxel technique (TE 35 and 144 ms); voxel of 2.0 cm3 was localized in the right thalamic region and in the controlateral region. MRI showed an unequivocal volume loss of the right thalamus bulk (figure 1), with a consequent ipsilateral ventricular enlargement. The anterior thalamus generally produced a convexity in the lateral ventricle posteriorly to the foramen of Monro, varying from a slight bulge to a prominent tubercle (figure 2) 16. The more posterior mediodorsal complex generally produced a convex contour (figure 2). In our case asymmetry of these contours was noted: the anterior and mediodorsal nuclei were markedly flattened or concave (figure 2).
F. Caranci
Thalamic Changes in Mesial Temporal Sclerosis: a Limbic System Pathology
A
B
➤ C
D
Figure 1 Axial T2-weighted (A,C) and FLAIR images (B,D). Marked atrophy and hyperintense signal involving the right thalamus, with consensual ventricular enlargement. The left mamillothalamic tract (C, arrow) shows a normal signal.
Moreover T2-weighted images showed a high signal involving the affected thalamus, not only in the medial nucleus but extending through the anterior part and more evident in the lateral nucleus (figure 1A). Volume loss and a high signal on T2-weighted images of the right hippocampus, representing MTS, was noted, associated with a mild enlargement of the ipsilateral temporal horn (fi-
gure 3). Atrophy of the ipsilateral column of the fornix (figure 3) was also present, less evident at the level of the body. Spectroscopic examination (in spite of the low signal-to-noise ratio) (figure 4), showed a mild reduction of Naa in the right thalamic region (Naa/Cr 1.46 short TE; 1.99 long TE) compared with the controlateral side (Naa/Cr 1.89 short TE; 2.31 long TE). 219
Thalamic Changes in Mesial Temporal Sclerosis: a Limbic System Pathology
F. Caranci
A
✢
➤
✢
➤
Table 1 Anatomy of the limbic system and circuit of Papez.
B
Figure 2 Coronal T2-weighted images. A,B) Physiologic convexity of the left thalamus toward the lateral ventricle, posteriorly to the foramen of Monro (arrow); flattened upper border of the right anterior thalamus (star, A) and of the more posterior mediodorsal complex (star, B).
Discussion In 1937 a closed system, now known as the circuit of Papez 9 (table1), was described linking the hippocampus, fornix, mamillary body, thalamus and cingulum. This circuit was hypothesized as an essential part of the structural basis of memory and emotion. Fibers from the hippocampal formation, in220
cluding the hippocampus (cornu ammonis and dentate gyrus) and parahippocampal structures (subiculum), contribute to the alveus, which medially coalesces to form the fimbria 9 . The fimbria forms the arching fornix, which projects mainly to the mamillary body via the postcommissural fornix. The circuit is completed by connections from the mamillary body to the anterior thalamic nucleus via the mamil-
www. centauro. it
The Neuroradiology Journal 20: 218-223, 2007
➤
A
B
Figure 3 Coronal T2-weighted images (A-B). Volume loss and high signal in the right hippocampus; modest enlargement of the ipsilateral temporal horn. Ipsilateral forniceal atrophy, more evident at level of the columns (arrows).
Figure 4 1HMR spectroscopy. A) Voxel on the right thalamus (TE 35 ms; TE 144 ms). B) Voxel on the left thalamus (TE 35 ms; TE 144 ms).
221
Thalamic Changes in Mesial Temporal Sclerosis: a Limbic System Pathology
lothalamic tract (MTT) 22, with a minor contribution directly from the fornix and the anterior thalamic nucleus to the cingulate gyrus via the thalamocingulate fibers (table 1) 10. More recent anatomic investigations have contributed to find many intrinsic connections between the hippocampal formation and the enthorinal cortex (located in the anterior part of the parahippocampal gyrus) 10,11,12 and to show that most of the efferent forniceal fibers originate from the subiculum and not from the hippocampus. Recent studies have identified thalamic volume loss in patients with TLE 13, and changes in the anterior thalamus in patients with mesial temporal sclerosis, detected by MRI 14 or seen post mortem, after temporal lobectomy 15. Besides a natural thalamic asymmetry 13, particularly in its posterior part 17, there are currently two hypotheses explaining ipsilateral thalamic atrophy due to the changes in MTS: excitotoxicity and transneuronal damage. Excitotoxicity is described as the mechanism of neuronal damage related to overproduction of excitatory amino-acid neurotransmitters. This concept is supported by animal model studies: limbic seizures and subsequent extrahippocampal changes, confirmed in histopathologic examination, were induced by systemic injection of excitatory amino-acid neurotransmitters, such as glutamate and kainic acid (an analogue of glutamate) 18,19. Abnormal electric activity, effect of repeated seizures, can propagate along a pathway (such as the Papez circuit) to achieve target efferent structures (fornix, mamillary body, thalamus). Many recent spectroscopic studies have tried to confirm this hypothesis by depicting metabolic changes, particularly increased levels of glutamate and glutamine 20. Oikawa et Al reported that the lack of signal changes or abnormalities in MTT may be more suggestive of excitotoxicity rather than transneuronal degeneration. MTT is identifiable on axial PD and T2 weighted images as a low signal in the anterior thalamus 22 (figure 1C). Thalamus atrophy may also be a result of hippocampal transneuronal degeneration following MTS or temporal lobectomy 21. Moreover, thalamic degeneration may be secondary to an abnormal developmental process, in association with MTS and global cerebral hemiatrophy 25. Histopathologic analysis has shown that the increased signal
222
F. Caranci
intensity of the anterior temporal lobe in MTS is not associated with dysplasia or gliosis, but represents a persisting developmental stage with immature myelin and immature cells as a consequence of early seizures 26. Interestingly, abnormalities along the Papez circuit, not only in efferent structures of the pathway (such as thalamus, fornix, mamillary body and cingulum gyrus), but also in major afferent structures (parahippocampal gyrus, including subiculum and enthorinal cortex) have been reported. The origin of the post-commissural forniceal fibers from the subiculum and not from Ammon’s horn has been established 27. This could explain why fornix and mamillary changes are less frequent than those in the hippocampus in MTS. The variable percentable of fornix atrophy reported (39-94%) 8,14 may be also due to different MRI techniques and measurement criteria. The fornix should be considered in all its parts, including body, crura and columns, using multiplanar thin slice images to avoid the effects of physiologic asymmetry. Various parahippocampal gyrus injuries, such as herpes encephalitis 28 or surgical changes (temporal lobectomy reported in 1%) 29, can cause abnormalities in the Papez circuit. Chan et Al found a correlation between MTS and many other findings; they reported cerebral hemiatrophy, amygdalar sclerosis, gliosis of the anterior temporal lobe and cerebellar diaschisis 14. Conclusions The correlation between limbic system abnormalities and clinical pathway is not clear. The extent and severity do not seem to correlate with the clinical severity: some authors have found that patients with extensive limbic system anomalies maybe well controlled, whereas patients with only parahippocampal changes show refractory epilepsy 30. Even if the Papez circuit is considered a major anatomical substrate for emotion and memory, neurologic deficits are not observed. Nevertheless, the detection of limbic system anomalies can be useful in increasing the confidence of lateralization in presurgical studies of bilateral MTS. The identification of thalamic changes could add explanations about the anatomy and possible modality of propagation of TLE.
www. centauro. it
The Neuroradiology Journal 20: 218-223, 2007
References 1 Pasquier B, Peoc’h M, Barnoud R et Al: Prédilection lésionnelle pour le lobe temporal dans l’épilepsie partielle pharmaco-résistante : aspect neuropathologique d’une série de 180 patients. Boll Lega It Epil 95: 57-64, 1996. 2 Jackson GD, Berkovic SF, Tress BM et Al: Hippocampal sclerosis can be reliably detected by magnetic resonance imaging. Neurology 40: 1869-75; 1990. 3 Honavar M, Meldrum BS: Epilepsy. In: Graham DI, Lantos PL(eds) Greenfield’s neuropathology, 6th ed. Arnold, London 1998: 931-971. 4 Berkovic SF, Andermann F, Olivier A et Al: Hippocampal sclerosis in temporal lobe epilepsy demonstrated by magnetic resonance imaging. Ann Neurol 29: 175-182, 1991. 5 Bronen RA, Cheung GC, Charles JT et Al: Imaging findings in hippocampal sclerosis: correlation with pathology. Am J Neuroradiol 12: 933-940, 1991. 6 Bronen RA: Epilepsy: the role of MR imaging. Am J Radiol 159: 1165-1174, 1992. 7 Meiners LC, van Gils A, Jansen GH et Al: Temporal lobe epilepsy: the various MR appearances of histologically proven mesial temporal sclerosis. Am J Neuroradiol 15: 1547-1555, 1994. 8 Baldwin GN, Tsuruda JS, Maravilla KR et Al: Fornix in patients with seizures caused by unilateral hippocampal sclerosis: detection of unilateral volume loss on MR images. Am J Radiol 162: 1185-1189, 1994. 9 Papez JW: A proposed mechanism of emotion. Arch Neurol Psychiatry 38: 725-743, 1937. 10 Martin JH: Neuroanatomy: Text and atlas. New York, NY: Elsevier 1989: 375-395. 11 Carpenter MB: Core text of neuroanatomy ,4th edn. Williams & Williams , Baltimore 1991: 361-386. 12 Mai JK, Assheuer J, Paxinos G: Atlas of the human brain. Academic Press, San Diego 1997: 80-83. 13 De Carli C, Hatta J, Fazilat S et Al: Extra temporal atrophy in patients with complex partial seizures of left temporal origin. Ann Neurol 43: 41-45, 1998. 14 Chan S, Erickson JK, Yoon SS: Limbic system abnormalities associated with mesial temporal sclerosis: a model of chronic cerebral changes due to seizures. Radiographics 17: 1095-1110, 1997. 15 Mamourian AC, Cho CH, Saykin AJ et Al: Association between size of the lateral ventricle and asymmetry of the fornix in patients with temporal lobe epilepsy. Am J Neuroradiol 19: 9-13, 1998. 16 Nieuwenhuys R, Voogd J, van Huijzen C: The human central nervous system. A synopsis and atlas. 3rd ed. Springer, Berlin Heidelberg New York 1988: 71-91. 17 Eidelberg D, Galaburda AM: Symmetry and asymmetry in the human posterior thalamus I. Cytoarchitecture analysis in normal persons. Arch Neurol 39: 325332, 1982. 18 Schwob JE, Fuller T, Price TL et Al: Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study. Neuroscience 5: 991-1014, 1980. 19 Lothman EW, Collins RC: Kainic acid induced limbic seizures: metabolic, behavioral, electroencephalographic and neuropathological correlates. Brain Res 218: 299-318, 1981. 20 Fazekas F, Kapeller P, Schmidt R et Al: Magnetic resonance imaging and spectroscopy findings after focal status epilepticus. Epilepsia 36: 946-949; 1995. 21 Van Buren JM, Borke RC: Variations and connections of the human thalamus. Springer, Berlin Heidelberg New York 1972: 60-65. 22 Wirth BA: MR imaging of the mamillothalamic tract. Presented at the 80th Scientific Assembly and Annual Meeting of the Radiological Society of North America, Chicago 1994. 23 Yamada K, Shrier DA, Rubio A et Al: MR imaging of
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26
27 28
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30
the mamillothalamic tract. Radiology 207: 593-598, 1998. Ogawa T, Yoshida Y, Okudera T et Al: Secondary thalamic degeneration after cerebral infarction in the middle cerebral artery distribution: evaluation with MR imaging. Radiology 204: 255-262, 1997. Dix JE, Cail WS: Cerebral hemiatrophy: classification on the basis of MR imaging findings of mesial temporal sclerosis and childhood febrile seizures. Radiology 203: 269-274, 1997. Briellmann RS, Syngeniotis A, Fleming S et Al: Increased anterior temporal lobe T2 times in cases of hippocampal sclerosis: a multi-echo T2 relaxometry study at 3 T. Am J Neuroradiol 25: 389-394, 2004. Swanson LW, Cowan WM: Hippocampo-hypothalamic connections: origin in subicular cortex, not Ammon’s horn. Science 189: 303-304, 1975. Kapur N, Barker S, Burrows EH et Al: Herpes simplex encephalitis ; long term magnetic resonance imaging and neuropsichological profile. J Neurol Neurosurg Psychiatry 57: 1334-1342, 1994. Kim JH, Tien RD, Felsberg GJ et Al: Clinical significance of asimmetry of the fornix and mamillary body on MR in hippocampal sclerosis. Am J Neuroradiol 16: 509-515, 1995. Oikawa H, Sasaki M et Al: The circuit of Papez in mesial temporal sclerosis. Neuroradiology 43: 205-210, 2001.
Dr Ferdinando Caranci Cattedra di Neuroradiologia Università Federico II Via Pansini 5 80131 Naple, Italy Tel.: 081 7462563 E-mail: [email protected]
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