- Email: [email protected]
MRI cytoarchitectonics: the next level?
Journal of the Neurological Sciences 211 (2003) 1 – 3 www.elsevier.com/locate/jns
Editorial
MRI cytoarchitectonics: the next level? Over the centuries, neuroscientists have sought to describe, define, and understand the anatomy and function of the human brain in health and disease. After the basic gross and histologic anatomy of the cerebral cortex was described, clinicians and investigators such as John Hughlings Jackson, [1] Vittorio Marchi, and many others, using clinicoanatomic and clinicopathologic correlations, electrical brain stimulation, and other experimental techniques, began to establish areas of functional localization within the cortex and delineate pathways and connections between different parts of the central nervous system. A century ago Brodmann [2] described a cytoarchitectonic map of the cerebral cortex, which parceled the cortex into 47 histologically distinctive areas. Although by no means the only cortical map to be proposed, the Brodmann map continues to be the most widely used and many of its anatomically defined areas conform to known regions of functional localization. In the mid-20th century, investigators such as Penfield, Rasmussen, and Jasper [3,4], using intraoperative cortical stimulation, further expanded our knowledge of functional localization within the cortex. Almost two decades ago, a powerful new modality for investigating the structure and function of the brain was developed: the clinical MRI scanner. Soon neuroscientists were developing quantitative techniques to use this tool to study brain structure in disease and in health. Initially, researchers measured the total volume of the brain or one of its lobes or segmented the brain into its parts—gray matter, white matter, cerebrospinal fluid, subcortical nuclei [5]. By the late 1980s and early 1990s, protocols were developed for the volumetric and morphometric analysis of small but well-defined structures such as the hippocampus and amygdala in normal control subjects and in patients with temporal lobe epilepsy, amnesia, Alzheimer’s disease, and neuropsychiatric disorders [6 –21]. These findings were correlated with neuropathological, neuropsychological, and electrophysiological studies as well as treatment outcome [22 – 32]. In recent years, morphometric analysis of temporal and extratemporal cortical, subcortical, and other limbic structures with direct or remote connections with hippocampus and amygdala has shown involvement of those regions as well [33 –43]. In this issue, Bendersky et al. [44] report their findings in 22 normal adult subjects who had T2 signal intensity measurements on FLAIR MRI images of 12 regions of the
cerebral cortex. The purpose was to determine if differences in signal intensity allowed discrimination of different cytoarchitectonic areas of the cerebral cortex. By combining the regions sampled into five groups with similar cortical architecture, they found significant differences in signal intensity between the groups. The authors conclude that cytoarchitectonic characteristics of the cortical regions cause differences in signal intensity detectable with FLAIR MR imaging. These interesting, although preliminary, observations corroborate the often-noted qualitative impression that limbic structures such as the hippocampus, anterior insula, and anterior cingulate gyrus are ‘‘brighter’’ on FLAIR images than other regions of the cerebral cortex. If replicated and extended by future studies, this approach may move MRI-based morphometric analysis from the macroscopic to the microscopic level. For this to occur, future studies will need to address and resolve possible technical questions such as whether these regional variations in signal intensity are actually due to cytoarchitectonic differences or perhaps related to inhomogeneities in the magnetic or radiofrequency fields and whether normalizing the signal intensity of the cortical region in question by the signal from the CSF is the best choice. In other words, is what Bendersky and colleagues proposed to do possible using these methods and have they done it? As with the macroscopic MRI morphometric techniques mentioned above, future studies measuring inter-rater and intra-rater reliability will also be needed. One way to test the ‘‘limits of this approach’’ may be to attempt to map the entire cortex and determine how closely it resembles Brodmann’s cytoarchitectonic map, as the authors suggest. One expects that with technological advances in image acquisition and processing, continued refinement of functional MRI methodology, and other new modalities such as pathway imaging with diffusion tensor imaging, we will soon be able to produce beautiful and detailed in vivo images of the structure, function, and connectivity of the human brain.
References [1] Jackson JH. In: Taylor J, editor. Selected writings of John Hughlings Jackson, vol. 1. New York: Basic Books; 1958.
0022-510X/03/$ - see front matter D 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0022-510X(03)00085-6
2
Editorial
[2] Brodmann K. Vergleichende Lokalisationlehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: J.A. Barth; 1909. [3] Penfield W, Rasmussen T. The cerebral cortex of man: a clinical study of localization of function. New York: Hafner Publishing; 1950. [4] Penfield W, Jasper H. Epilepsy and the functional anatomy of the human brain. Boston: Little, Brown and Company; 1954. [5] Murphy GM, DeCarli C, Schapiro MB, Rapoport SI, Horwitz B. Agerelated differences in volumes of subcortical nuclei, brain matter, and cerebrospinal fluid in healthy men as measured with magnetic resonance imaging. Arch Neurol 1992;49:839 – 45. [6] Jack CR, Gehring DG, Sharbrough FW, Felmlee JP, Forbes G, Hench VS, et al. Temporal lobe volume measurements from MR images: accuracy and left-right asymmetry in normal persons. J Comput Assist Tomogr 1988;12:21 – 9. [7] Jack CR, Twomey CK, Zinsmeister AR, Sharbrough FW, Petersen RC, Cascino GD. Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. Radiology 1989;172:549 – 54. [8] Jack CR, Bentley MD, Twomey CK, Zinsmeister AR. MR imaging-based volume measurements of the hippocampal formation and anterior temporal lobe: validation studies. Radiology 1990;176: 205 – 9. [9] Watson C, Andermann F, Gloor P, Jones-Gotman M, Peters T, Evans A, et al. Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging. Neurology 1992;42: 1743 – 50. [10] Jack CR, Sharbrough FW, Twomey CK, Cascino GD, Hirschorn KA, Marsh WR, et al. Temporal lobe seizures: lateralization with MR volume measurements of the hippocampal formation. Radiology 1990;175:423 – 9. [11] Ashtari M, Barr WB, Schaul N, Bogerts B. Three-dimensional fast low-angle shot imaging and computerized volume measurement of the hippocampus in patients with chronic epilepsy of the temporal lobe. Am J Neuroradiol 1991;12:941 – 7. [12] Cook MJ, Fish DR, Shorvon SD, Straughan K, Stevens JM. Hippocampal volumetric and morphometric studies in frontal and temporal lobe epilepsy. Brain 1992;115:1001 – 15. [13] Cendes F, Andermann F, Gloor P, Evans A, Jones-Gotman M, Watson C, et al. MRI volumetric measurement of amygdala and hippocampus in temporal lobe epilepsy. Neurology 1993;43:719 – 25. [14] Press GA, Amaral DG, Squire LR. Hippocampal abnormalities in amnesic patients revealed by high-resolution magnetic resonance imaging. Nature 1989;341:54 – 7. [15] Squire LR, Amaral DG, Press GA. Magnetic resonance imaging of the hippocampal formation and mammillary nuclei distinguish medial temporal lobe and diencephalic amnesia. J Neurosci 1990;10: 3106 – 17. [16] Seab JP, Jagust WJ, Wong STS, Roos MS, Reed BR, Budinger TF. Quantitative NMR measurements of hippocampal atrophy in Alzheimer’s disease. Magn Reson Med 1988;8:200 – 8. [17] Kesslak JP, Nalcioglu O, Cotman CW. Quantification of magnetic resonance scans for hippocampal and parahippocampal atrophy in Alzheimer’s disease. Neurology 1991;41:51 – 4. [18] Jack CR, Petersen RC, O’Brien PC, Tangalos EG. MR-based hippocampal volumetry in the diagnosis of Alzheimer’s disease. Neurology 1992;42:183 – 8. [19] Bogerts B, Ashtari M, Degreef G, Alvir JM, Bilder RM, Lieberman JA. Reduced temporal limbic structure volumes on magnetic resonance images in first episode schizophrenia. Psychiatry Res 1990; 35:1 – 13. [20] Suddath RL, Christison GW, Torrey EF, Casanova MF, Weinberger DR. Anatomical abnormalities in the brains of monozygotic twins discordant for schizophrenia. N Engl J Med 1990;322:789 – 94. [21] Barta PE, Pearlson GD, Powers RE, Richards SS, Tune LE. Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. Am J Psychiatry 1990;147:1457 – 62.
[22] Cascino GD, Jack CR, Parisi JE, Sharbrough FW, Hirschorn KA, Meyer FB, et al. Magnetic resonance imaging-based volume studies in temporal lobe epilepsy: pathological correlations. Ann Neurol 1991;30:31 – 6. [23] Lencz T, McCarthy G, Bronen RA, Scott TM, Inserni JA, Sass KJ, et al. Quantitative magnetic resonance imaging in temporal lobe epilepsy: relationship to neuropathology and neuropsychological function. Ann Neurol 1992;31:629 – 37. [24] Lee N, Tien RD, Lewis DV, Friedman AH, Felsberg GJ, Crain B, et al. Fast spin-echo, magnetic resonance imaging-measured hippocampal volume: correlation with neuronal density in anterior temporal lobectomy patients. Epilepsia 1995;36:899 – 904. [25] Watson C, Nielsen SL, Cobb C, Burgerman R, Williamson B. Pathological grading system for hippocampal sclerosis: correlation with MRI-based volume measurements of the hippocampus. J Epilepsy 1996;9:56 – 64. [26] Loring DW, Murro AM, Meador KJ, Lee GP, Gratton CA, Nichols ME, et al. Wada memory testing and hippocampal volume measurements in the evaluation for temporal lobectomy. Neurology 1993; 43:1789 – 93. [27] Trenerry MR, Jack CR, Ivnik RJ, Sharbrough FW, Cascino GD, Hirschorn KA, et al. MRI hippocampal volumes and memory function before and after temporal lobectomy. Neurology 1993;43: 1800 – 5. [28] Trenerry MR, Jack CR, Cascino GD, Sharbrough FW, Ivnik RJ. Gender differences in post-temporal lobectomy verbal memory and relationships between MRI hippocampal volumes and preoperative verbal memory. Epilepsy Res 1995;20:69 – 76. [29] Fuerst D, Shah J, Kupsky WJ, Johnson R, Shah A, HaymanAbello B, et al. Volumetric MRI, pathological, and neuropsychological progression in hippocampal sclerosis. Neurology 2001;57: 184 – 8. [30] Jack CR, Sharbrough FW, Cascino GD, Hirschorn KA, O’Brien PC, Marsh WR. Magnetic resonance image-based hippocampal volumetry: correlation with outcome after temporal lobectomy. Ann Neurol 1992;31:138 – 46. [31] Arruda F, Cendes F, Andermann F, Dubeau F, Villemure JG, JonesGotman M, et al. Mesial atrophy and outcome after amygdalohippocampectomy or temporal lobe removal. Ann Neurol 1996;40: 446 – 50. [32] Watson C, Jack CR, Cendes F. Volumetric magnetic resonance imaging: clinical applications and contributions to the understanding of temporal lobe epilepsy. Arch Neurol 1997;54:1521 – 31. [33] Lee JW, Andermann F, Dubeau F, Bernasconi A, MacDonald D, Evans A, et al. Morphometric analysis of the temporal lobe in temporal lobe epilepsy. Epilepsia 1998;39:727 – 36. [34] Briellmann RS, Jackson GD, Kalnins R, Berkovic SF. Hemicranial volume deficits in patients with temporal lobe epilepsy with and without hippocampal sclerosis. Epilepsia 1998;39:1174 – 81. [35] DeCarli C, Hatta J, Fazilat S, Fazilat S, Gaillard WD, Theodore WH. Extratemporal atrophy in patients with complex partial seizures of left temporal origin. Ann Neurol 1998;43:41 – 5. [36] Bernasconi N, Bernasconi A, Andermann F, Dubeau F, Feindel W, Reutens DC. Entorhinal cortex in temporal lobe epilepsy: a quantitative MRI study. Neurology 1999;52:1870 – 6. [37] Kuzniecky R, Bilir E, Gilliam F, Faught E, Martin R, Hugg J. Quantitative MRI in temporal lobe epilepsy: evidence for fornix atrophy. Neurology 1999;53:496 – 501. [38] Juhasz C, Nagy F, Watson C, da Silva EA, Muzik O, Chugani DC, et al. Glucose and [11C] flumazenil PET abnormalities of thalamic nuclei in temporal lobe epilepsy. Neurology 1999;53:2037 – 45. [39] Sandok EK, O’Brien TJ, Jack CR, So EL. Significance of cerebellar atrophy in intractable temporal lobe epilepsy: a quantitative MRI study. Epilepsia 2000;41:1315 – 20. [40] Salmenpera T, Kalviainen R, Partanen K, Pitkanen A. Quantitative MRI volumetry of the entorhinal cortex in temporal lobe epilepsy. Seizure 2000;9:208 – 15.
Editorial [41] Bernasconi N, Bernasconi A, Caramanos Z, Dubeau F, Richardson J, Andermann F, et al. Entorhinal cortex atrophy in epilepsy patients exhibiting normal hippocampal volumes. Neurology 2001;56: 1335 – 9. [42] Dreifuss S, Vingerhoets FJG, Lazeyras F, Andino SG, Spinelli L, Delavelle J, et al. Volumetric measurements of subcortical nuclei in patients with temporal lobe epilepsy. Neurology 2001;57:1636 – 41. [43] Coste S, Ryvlin P, Hermier M, Ostrowsky K, Adeleine P, Froment JC, et al. Temporopolar changes in temporal lobe epilepsy: a quantitative MRI-based study. Neurology 2002;59:855 – 61. [44] Bendersky M, Rugilo C, Kochen S, Schuster G, Sica REP. Magnetic
3 resonance imaging identifies cytoarchitectonic subtypes of the normal human cerebral cortex. J Neurol Sci 2003;211:78 – 80 (This issue).
Craig Watson Department of Neurology, School of Medicine Wayne State University Detroit, MI 48201 USA E-mail address: [email protected]
Editorial
MRI cytoarchitectonics: the next level? Over the centuries, neuroscientists have sought to describe, define, and understand the anatomy and function of the human brain in health and disease. After the basic gross and histologic anatomy of the cerebral cortex was described, clinicians and investigators such as John Hughlings Jackson, [1] Vittorio Marchi, and many others, using clinicoanatomic and clinicopathologic correlations, electrical brain stimulation, and other experimental techniques, began to establish areas of functional localization within the cortex and delineate pathways and connections between different parts of the central nervous system. A century ago Brodmann [2] described a cytoarchitectonic map of the cerebral cortex, which parceled the cortex into 47 histologically distinctive areas. Although by no means the only cortical map to be proposed, the Brodmann map continues to be the most widely used and many of its anatomically defined areas conform to known regions of functional localization. In the mid-20th century, investigators such as Penfield, Rasmussen, and Jasper [3,4], using intraoperative cortical stimulation, further expanded our knowledge of functional localization within the cortex. Almost two decades ago, a powerful new modality for investigating the structure and function of the brain was developed: the clinical MRI scanner. Soon neuroscientists were developing quantitative techniques to use this tool to study brain structure in disease and in health. Initially, researchers measured the total volume of the brain or one of its lobes or segmented the brain into its parts—gray matter, white matter, cerebrospinal fluid, subcortical nuclei [5]. By the late 1980s and early 1990s, protocols were developed for the volumetric and morphometric analysis of small but well-defined structures such as the hippocampus and amygdala in normal control subjects and in patients with temporal lobe epilepsy, amnesia, Alzheimer’s disease, and neuropsychiatric disorders [6 –21]. These findings were correlated with neuropathological, neuropsychological, and electrophysiological studies as well as treatment outcome [22 – 32]. In recent years, morphometric analysis of temporal and extratemporal cortical, subcortical, and other limbic structures with direct or remote connections with hippocampus and amygdala has shown involvement of those regions as well [33 –43]. In this issue, Bendersky et al. [44] report their findings in 22 normal adult subjects who had T2 signal intensity measurements on FLAIR MRI images of 12 regions of the
cerebral cortex. The purpose was to determine if differences in signal intensity allowed discrimination of different cytoarchitectonic areas of the cerebral cortex. By combining the regions sampled into five groups with similar cortical architecture, they found significant differences in signal intensity between the groups. The authors conclude that cytoarchitectonic characteristics of the cortical regions cause differences in signal intensity detectable with FLAIR MR imaging. These interesting, although preliminary, observations corroborate the often-noted qualitative impression that limbic structures such as the hippocampus, anterior insula, and anterior cingulate gyrus are ‘‘brighter’’ on FLAIR images than other regions of the cerebral cortex. If replicated and extended by future studies, this approach may move MRI-based morphometric analysis from the macroscopic to the microscopic level. For this to occur, future studies will need to address and resolve possible technical questions such as whether these regional variations in signal intensity are actually due to cytoarchitectonic differences or perhaps related to inhomogeneities in the magnetic or radiofrequency fields and whether normalizing the signal intensity of the cortical region in question by the signal from the CSF is the best choice. In other words, is what Bendersky and colleagues proposed to do possible using these methods and have they done it? As with the macroscopic MRI morphometric techniques mentioned above, future studies measuring inter-rater and intra-rater reliability will also be needed. One way to test the ‘‘limits of this approach’’ may be to attempt to map the entire cortex and determine how closely it resembles Brodmann’s cytoarchitectonic map, as the authors suggest. One expects that with technological advances in image acquisition and processing, continued refinement of functional MRI methodology, and other new modalities such as pathway imaging with diffusion tensor imaging, we will soon be able to produce beautiful and detailed in vivo images of the structure, function, and connectivity of the human brain.
References [1] Jackson JH. In: Taylor J, editor. Selected writings of John Hughlings Jackson, vol. 1. New York: Basic Books; 1958.
0022-510X/03/$ - see front matter D 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0022-510X(03)00085-6
2
Editorial
[2] Brodmann K. Vergleichende Lokalisationlehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: J.A. Barth; 1909. [3] Penfield W, Rasmussen T. The cerebral cortex of man: a clinical study of localization of function. New York: Hafner Publishing; 1950. [4] Penfield W, Jasper H. Epilepsy and the functional anatomy of the human brain. Boston: Little, Brown and Company; 1954. [5] Murphy GM, DeCarli C, Schapiro MB, Rapoport SI, Horwitz B. Agerelated differences in volumes of subcortical nuclei, brain matter, and cerebrospinal fluid in healthy men as measured with magnetic resonance imaging. Arch Neurol 1992;49:839 – 45. [6] Jack CR, Gehring DG, Sharbrough FW, Felmlee JP, Forbes G, Hench VS, et al. Temporal lobe volume measurements from MR images: accuracy and left-right asymmetry in normal persons. J Comput Assist Tomogr 1988;12:21 – 9. [7] Jack CR, Twomey CK, Zinsmeister AR, Sharbrough FW, Petersen RC, Cascino GD. Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. Radiology 1989;172:549 – 54. [8] Jack CR, Bentley MD, Twomey CK, Zinsmeister AR. MR imaging-based volume measurements of the hippocampal formation and anterior temporal lobe: validation studies. Radiology 1990;176: 205 – 9. [9] Watson C, Andermann F, Gloor P, Jones-Gotman M, Peters T, Evans A, et al. Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging. Neurology 1992;42: 1743 – 50. [10] Jack CR, Sharbrough FW, Twomey CK, Cascino GD, Hirschorn KA, Marsh WR, et al. Temporal lobe seizures: lateralization with MR volume measurements of the hippocampal formation. Radiology 1990;175:423 – 9. [11] Ashtari M, Barr WB, Schaul N, Bogerts B. Three-dimensional fast low-angle shot imaging and computerized volume measurement of the hippocampus in patients with chronic epilepsy of the temporal lobe. Am J Neuroradiol 1991;12:941 – 7. [12] Cook MJ, Fish DR, Shorvon SD, Straughan K, Stevens JM. Hippocampal volumetric and morphometric studies in frontal and temporal lobe epilepsy. Brain 1992;115:1001 – 15. [13] Cendes F, Andermann F, Gloor P, Evans A, Jones-Gotman M, Watson C, et al. MRI volumetric measurement of amygdala and hippocampus in temporal lobe epilepsy. Neurology 1993;43:719 – 25. [14] Press GA, Amaral DG, Squire LR. Hippocampal abnormalities in amnesic patients revealed by high-resolution magnetic resonance imaging. Nature 1989;341:54 – 7. [15] Squire LR, Amaral DG, Press GA. Magnetic resonance imaging of the hippocampal formation and mammillary nuclei distinguish medial temporal lobe and diencephalic amnesia. J Neurosci 1990;10: 3106 – 17. [16] Seab JP, Jagust WJ, Wong STS, Roos MS, Reed BR, Budinger TF. Quantitative NMR measurements of hippocampal atrophy in Alzheimer’s disease. Magn Reson Med 1988;8:200 – 8. [17] Kesslak JP, Nalcioglu O, Cotman CW. Quantification of magnetic resonance scans for hippocampal and parahippocampal atrophy in Alzheimer’s disease. Neurology 1991;41:51 – 4. [18] Jack CR, Petersen RC, O’Brien PC, Tangalos EG. MR-based hippocampal volumetry in the diagnosis of Alzheimer’s disease. Neurology 1992;42:183 – 8. [19] Bogerts B, Ashtari M, Degreef G, Alvir JM, Bilder RM, Lieberman JA. Reduced temporal limbic structure volumes on magnetic resonance images in first episode schizophrenia. Psychiatry Res 1990; 35:1 – 13. [20] Suddath RL, Christison GW, Torrey EF, Casanova MF, Weinberger DR. Anatomical abnormalities in the brains of monozygotic twins discordant for schizophrenia. N Engl J Med 1990;322:789 – 94. [21] Barta PE, Pearlson GD, Powers RE, Richards SS, Tune LE. Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. Am J Psychiatry 1990;147:1457 – 62.
[22] Cascino GD, Jack CR, Parisi JE, Sharbrough FW, Hirschorn KA, Meyer FB, et al. Magnetic resonance imaging-based volume studies in temporal lobe epilepsy: pathological correlations. Ann Neurol 1991;30:31 – 6. [23] Lencz T, McCarthy G, Bronen RA, Scott TM, Inserni JA, Sass KJ, et al. Quantitative magnetic resonance imaging in temporal lobe epilepsy: relationship to neuropathology and neuropsychological function. Ann Neurol 1992;31:629 – 37. [24] Lee N, Tien RD, Lewis DV, Friedman AH, Felsberg GJ, Crain B, et al. Fast spin-echo, magnetic resonance imaging-measured hippocampal volume: correlation with neuronal density in anterior temporal lobectomy patients. Epilepsia 1995;36:899 – 904. [25] Watson C, Nielsen SL, Cobb C, Burgerman R, Williamson B. Pathological grading system for hippocampal sclerosis: correlation with MRI-based volume measurements of the hippocampus. J Epilepsy 1996;9:56 – 64. [26] Loring DW, Murro AM, Meador KJ, Lee GP, Gratton CA, Nichols ME, et al. Wada memory testing and hippocampal volume measurements in the evaluation for temporal lobectomy. Neurology 1993; 43:1789 – 93. [27] Trenerry MR, Jack CR, Ivnik RJ, Sharbrough FW, Cascino GD, Hirschorn KA, et al. MRI hippocampal volumes and memory function before and after temporal lobectomy. Neurology 1993;43: 1800 – 5. [28] Trenerry MR, Jack CR, Cascino GD, Sharbrough FW, Ivnik RJ. Gender differences in post-temporal lobectomy verbal memory and relationships between MRI hippocampal volumes and preoperative verbal memory. Epilepsy Res 1995;20:69 – 76. [29] Fuerst D, Shah J, Kupsky WJ, Johnson R, Shah A, HaymanAbello B, et al. Volumetric MRI, pathological, and neuropsychological progression in hippocampal sclerosis. Neurology 2001;57: 184 – 8. [30] Jack CR, Sharbrough FW, Cascino GD, Hirschorn KA, O’Brien PC, Marsh WR. Magnetic resonance image-based hippocampal volumetry: correlation with outcome after temporal lobectomy. Ann Neurol 1992;31:138 – 46. [31] Arruda F, Cendes F, Andermann F, Dubeau F, Villemure JG, JonesGotman M, et al. Mesial atrophy and outcome after amygdalohippocampectomy or temporal lobe removal. Ann Neurol 1996;40: 446 – 50. [32] Watson C, Jack CR, Cendes F. Volumetric magnetic resonance imaging: clinical applications and contributions to the understanding of temporal lobe epilepsy. Arch Neurol 1997;54:1521 – 31. [33] Lee JW, Andermann F, Dubeau F, Bernasconi A, MacDonald D, Evans A, et al. Morphometric analysis of the temporal lobe in temporal lobe epilepsy. Epilepsia 1998;39:727 – 36. [34] Briellmann RS, Jackson GD, Kalnins R, Berkovic SF. Hemicranial volume deficits in patients with temporal lobe epilepsy with and without hippocampal sclerosis. Epilepsia 1998;39:1174 – 81. [35] DeCarli C, Hatta J, Fazilat S, Fazilat S, Gaillard WD, Theodore WH. Extratemporal atrophy in patients with complex partial seizures of left temporal origin. Ann Neurol 1998;43:41 – 5. [36] Bernasconi N, Bernasconi A, Andermann F, Dubeau F, Feindel W, Reutens DC. Entorhinal cortex in temporal lobe epilepsy: a quantitative MRI study. Neurology 1999;52:1870 – 6. [37] Kuzniecky R, Bilir E, Gilliam F, Faught E, Martin R, Hugg J. Quantitative MRI in temporal lobe epilepsy: evidence for fornix atrophy. Neurology 1999;53:496 – 501. [38] Juhasz C, Nagy F, Watson C, da Silva EA, Muzik O, Chugani DC, et al. Glucose and [11C] flumazenil PET abnormalities of thalamic nuclei in temporal lobe epilepsy. Neurology 1999;53:2037 – 45. [39] Sandok EK, O’Brien TJ, Jack CR, So EL. Significance of cerebellar atrophy in intractable temporal lobe epilepsy: a quantitative MRI study. Epilepsia 2000;41:1315 – 20. [40] Salmenpera T, Kalviainen R, Partanen K, Pitkanen A. Quantitative MRI volumetry of the entorhinal cortex in temporal lobe epilepsy. Seizure 2000;9:208 – 15.
Editorial [41] Bernasconi N, Bernasconi A, Caramanos Z, Dubeau F, Richardson J, Andermann F, et al. Entorhinal cortex atrophy in epilepsy patients exhibiting normal hippocampal volumes. Neurology 2001;56: 1335 – 9. [42] Dreifuss S, Vingerhoets FJG, Lazeyras F, Andino SG, Spinelli L, Delavelle J, et al. Volumetric measurements of subcortical nuclei in patients with temporal lobe epilepsy. Neurology 2001;57:1636 – 41. [43] Coste S, Ryvlin P, Hermier M, Ostrowsky K, Adeleine P, Froment JC, et al. Temporopolar changes in temporal lobe epilepsy: a quantitative MRI-based study. Neurology 2002;59:855 – 61. [44] Bendersky M, Rugilo C, Kochen S, Schuster G, Sica REP. Magnetic
3 resonance imaging identifies cytoarchitectonic subtypes of the normal human cerebral cortex. J Neurol Sci 2003;211:78 – 80 (This issue).
Craig Watson Department of Neurology, School of Medicine Wayne State University Detroit, MI 48201 USA E-mail address: [email protected]