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Extratemporal quantitative MR volumetrics and neuropsychological status in temporal lobe epilepsy

Published online by Cambridge University Press:  02 March 2020

Hermann Bruce ,
Seidenberg Michael ,
Bell Brian ,
Rutecki Paul ,
Sheth Raj D. ,
Wendt Gary ,
O'Leary Daniel  and
Magnotta Vince
Hermann Bruce*
Affiliation:
Department of Neurology, University of Wisconsin, Madison
Seidenberg Michael
Affiliation:
Department of Psychology, Chicago Medical School, North Chicago
Bell Brian
Affiliation:
Department of Neurology, University of Wisconsin, Madison
Rutecki Paul
Affiliation:
Department of Neurology, University of Wisconsin, Madison Middleton VA Medical Center, Madison
Sheth Raj D.
Affiliation:
Department of Neurology, University of Wisconsin, Madison
Wendt Gary
Affiliation:
Department of Radiology, University of Wisconsin, Madison
O'Leary Daniel
Affiliation:
Department of Psychiatry, University of Iowa, Iowa City
Magnotta Vince
Affiliation:
Department of Psychiatry, University of Iowa, Iowa City
*
Reprint requests to: Bruce Hermann, Ph.D., Department of Neurology, University of Wisconsin, 600 N. Highland Ave., Madison WI 53792. E-mail: hermann@neurology.wisc.edu
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Abstract

Neuropsychological studies of temporal lobe epilepsy have focused heavily on the nature and extent of memory dysfunction and its relationship to the neuropathological status of the hippocampus and related mesial temporal lobe structures. In this study, we examined whole brain and lobar quantitative MRI volumes and comprehensive neuropsychological performance in 58 patients with temporal lobe epilepsy and 62 healthy controls in order to determine (1) the nature and degree of extratemporal structural abnormalities in localization-related temporal lobe epilepsy; (2) the nature and degree of cognitive abnormalities outside of anterograde memory function; and (3) the relationship of volumetric abnormalities to neuropsychological status. Temporal lobe epilepsy patients exhibited significant reduction in the volume of adjusted (age, gender, height) total cerebral tissue (−5.8%), more evident in white (−9.8%) compared to gray matter (−3.0%) tissue volumes. Significant volumetric reductions were evident across frontal, temporal and parietal but not occipital lobe regions. Subarachnoid but not total ventricular CSF was significantly increased in epilepsy patients. Neuropsychological abnormality was generalized in nature, consistent with the generalized nature of the morphometric abnormalities, and reductions in cerebral tissue volumes were directly associated with poorer cognitive performance. In summary, patients with temporal lobe epilepsy exhibited clinically significant structural and functional abnormalities that extended outside the epileptogenic temporal lobe. The degree to which these structural and cognitive abnormalities are due to factors that cause the epilepsy, as opposed to reflecting the consequences of chronic epilepsy (e.g., duration and severity of epilepsy), remain to be determined. (JINS, 2003, 9, 353–362.)

Keywords

Temporal lobe epilepsyMRINeuropsychologyComplex partial seizures
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 9 , Issue 3 , 25 March 2003 , pp. 353 - 362
Copyright
Copyright © The International Neuropsychological Society 2003

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References

Andreasen, N.C., Flashman, L., Flaum, M., Arndt, S., Swayze, V., O'Leary, D.S., Ehrhardt, J.C., & Yuh, W.T.C. (1994). Regional brain abnormalities in schizophrenia measured with magnetic resonance imaging. Journal of the American Medical Association, 272, 1763–1769.CrossRefGoogle Scholar
Andreasen, N.C., Rajarethinam, R., Cizadlo, T., Arndt, S., Swayze, V.W., Flashman, L.A., O'Leary, D.S., Ehrhardt, J.C., & Yuh, W.T. (1996). Automated atlas-based volume estimation of human brain regions from MR images. Journal of Computer Assisted Tomography, 20, 98–106.CrossRefGoogle Scholar
Baxendale, S.A., Sisodiya, S.M., Thompson, P.J., Free, S.L., Kitchen, N.D., Stevens, J.M., Harkness, W.F., Fish, D.R., & Shorvon, S.D. (1999). Disproportion in the distribution of gray and white matter: Neuropsychological correlates. Neurology, 52, 248–252.CrossRefGoogle Scholar
Benton, A., Hamsher, K., & Sivan, A. (1994a). Multilingual Aphasia Examination (3rd ed.). Iowa City: University of Iowa.Google Scholar
Benton, A., Sivan, A., Hamsher, K., Varney, N.R., & Spreen, O. (1994b). Contributions to neuropsychological assessment: A clinical manual (2nd ed.). New York: Oxford University Press.Google Scholar
Bernasconi, N., Bernasconi, A., Andermann, F., Dubeau, F., Feindel, W., & Reutens, D.C. (1999). Entorhinal cortex in temporal lobe epilepsy: A quantitative MRI study. Neurology, 52, 1870–1876.CrossRefGoogle Scholar
Bohnen, N.I., O'Brien, T.J., Mullan, B.P., & So, E.L. (1998). Cerebellar changes in partial seizures: Clinical correlation of quantitative SPECT and MRI analysis. Epilepsia, 39, 640–650.CrossRefGoogle Scholar
Briellmann, R., Jackson, G., Kalnins, R., & Berkovic, S. (1998). Hemicranial volume deficits in patients with temporal lobe epilepsy with and without hippocampal sclerosis. Epilepsia, 39, 1174–1181.CrossRefGoogle Scholar
Buschke, H. (1973). Selective reminding for analysis of memory and learning. Journal of Verbal Learning and Behavior, 12, 543–550.CrossRefGoogle Scholar
Buschke, H. (1974). Evaluating storage, retention, and retrieval in disordered memory and learning. Neurology, 24, 1019–1025.CrossRefGoogle Scholar
DeCarli, C., Hatta, J., Fazilat, S., Fazilat, S., Gaillard, W.D., & Theodore, W.H. (1998). Extratemporal atrophy in patients with complex partial seizures of left temporal origin. Annals of Neurology, 43, 41–45.CrossRefGoogle Scholar
Dwyer, B.E. & Wasterlain, C.G. (1982). Electroconvulsive seizures in the immature rat adversely affect myelin accumulation. Experimental Neurology, 78, 616–628.CrossRefGoogle Scholar
Filley, C. (2002). The behavioral neurology of white matter. New York: Oxford University Press.Google Scholar
Glosser, G., Cole, L.C., French, J.A., Saykin, A.J., & Sperling, M.R. (1997). Predictors of intellectual performance in adults with intractable temporal lobe epilepsy. Journal of the International Neuropsychological Society, 3, 252–259.CrossRefGoogle Scholar
Goodglass, H. & Kaplan, E. (1983). Boston Diagnostic Aphasia Examination. Philadelphia: Lea & Febiger.Google Scholar
Harris, G., Andreasen, N.C., Cizadlo, T., Bailey, J.M., Bockholt, H.J., Magnotta, V.A., & Arndt, S. (1999). Improving tissue classification in MRI: A three-dimensional multispectral discriminant analysis method with automated training class selection. Journal of Computer Assisted Tomography, 23, 144–154.CrossRefGoogle Scholar
Hermann, B.P. & Seidenberg, M. (1995). Executive system dysfunction in temporal lobe epilepsy: Effects of nociferous cortex versus hippocampal pathology. Journal of Clinical and Experimental Neuropsychology, 7, 809–819.CrossRefGoogle Scholar
Hermann, B.P., Seidenberg, M., Schoenfeld, J., & Davies, K. (1997). Neuropsychological characteristics of the syndrome of mesial temporal lobe epilepsy. Archives of Neurology, 54, 369–376.CrossRefGoogle Scholar
Hermann, B.P., Seidenberg, M., Bell, B., Rutecki, P., Sheth, R., Wendt, G., O'Leary, D., & Magnotta, V. (2002). The neurodevelopmental impact of childhood onset temporal lobe epilepsy on brain structure and function. Epilepsia, 43, 1062–1070.CrossRefGoogle Scholar
Jack, C.R., Sharbrough, F.W., Cascino, G.D., Hirschorn, K.A., O'Brien, P.C., & Marsh, W.R. (1992). Magnetic resonance image-based hippocampal volumetry: Correlation with outcome after temporal lobectomy. Annals of Neurology, 31, 138–146.CrossRefGoogle Scholar
Kalviainen, R., Salmenpera, T., Partanen, K., Vainio, P., Riekkinen, P., & Pitkanen, A. (1997). MRI volumetry and T2 relaxometry of the amygdala in newly diagnosed and chronic temporal lobe epilepsy. Epilepsy Research, 28, 39–50.CrossRefGoogle Scholar
Kongs, S., Thompson, L., Iverson, G., & Heaton, R. (2000). Wisconsin Card Sorting Test–64 Card Version. Lutz, FL: Psychological Assessment Resources.Google Scholar
Kuzniecky, R., Bilir, E., Gilliam, F., Faught, E., Martin, R., & Hugg, J. (1999). Quantitative MRI in temporal lobe epilepsy: Evidence for fornix atrophy. Neurology, 53, 496–501.CrossRefGoogle Scholar
Lawson, J.A., Vogrin, S., Bleasel, A.F., Cook, M.J., & Bye, A.M. (2000a). Cerebral and cerebellar volume reduction in children with temporal lobe epilepsy. Epilepsia, 41, 1456–1462.CrossRefGoogle Scholar
Lawson, J.A., Vogrin, S., Bleasel, A.F., Cook, M.J., Burns, L., McAnally, L., Pereira, & J., Bye A.M. (2000b). Predictors of hippocampal, cerebral, and cerebellar volume reduction in childhood epilepsy. Epilepsia, 41, 1540–1545.CrossRefGoogle Scholar
Lee, J.W., Andermann, F., Dubeau, F., Bernasconi, A., MacDonald, D., Evans, A., & Reutens, D.C. (1998). Morphometric analysis of the temporal lobe in temporal lobe epilepsy. Epilepsia, 39, 727–736.CrossRefGoogle Scholar
Magnotta, V.A., Harris, G., O'Leary, D.S., Andreasen, N.C., & Heckel, D. (2002). BRAINS 2: A structural imaging processing toolbox. Computerized Medical Imaging and Graphics, 26, 251–264.CrossRefGoogle Scholar
Magnotta, V.A., Andreasen, N.C., Schultz, S.K., Harris, G., Cizadlo, T., Heckel, D., Nopoulos, & P., Flaum M. (1999a). Quantitative in vivo measurement of gyrification in the human brain: Changes associated with aging. Cerebral Cortex, 9, 151–160.CrossRefGoogle Scholar
Magnotta, V.A., Heckel, D., Andreasen, N.C., Cizadlo, T., Corson, P.W., Ehrhardt, J.C., & Yuh, W.T. (1999b). Measurement of brain structures with artificial neural networks: Two- and three-dimensional applications. Radiology, 211, 781–790.CrossRefGoogle Scholar
Martin, R., Hugg, J.W., Roth, D.L., Bilar, E., Gilliam, F.G., Faught, E., & Kuzniecky, R. (1999). MRI extrahippocampal volumes and visual memory: Correlations independent of MRI hippocampal volumes in temporal lobe epilepsy. Journal of the International Neuropsychological Society, 5, 540–548.CrossRefGoogle Scholar
Marsh, L., Morrell, M.J., Shear, P.K., Sullivan, E.V., Freeman, H., Marie, A., Lim, K.O., & Pfefferbaum, A. (1997). Cortical and hippocampal volume deficits in temporal lobe epilepsy. Epilepsia, 38, 576–587.CrossRefGoogle Scholar
Moran, N.F., Lemieux, L., Kitchen, N.D., Fish, D.R., & Shorvon, S.D. (2001). Extrahippocampal temporal lobe atrophy in temporal lobe epilepsy and mesial temporal sclerosis. Brain, 124, 167–175.CrossRefGoogle Scholar
Ney, G.C., Lantos, G., Barr, W.B., & Schaul, N. (1994). Cerebellar atrophy in patients with long term phenytoin exposure and epilepsy. Archives of Neurology, 51, 767–771.CrossRefGoogle Scholar
Pantel, J., O'Leary, D.S., Cretsinger, K., Bockholt, H.J., Keefe, H., Magnotta, V.A., & Andreasen N.C. (2000). A new method for the in vivo volumetric measurement of the human hippocampus with high neuroanatomical accuracy. Hippocampus, 10, 752–758.3.0.CO;2-Y>CrossRefGoogle Scholar
Pilgrim, B., Meyers, J., Bayless, J., & Whetstone, M. (2000). Validity of the Ward seven-subtest WAIS–III short form in a neuropsychological population. Applied Neuropsychology, 6, 243–246.CrossRefGoogle Scholar
Quigg, M., Bertram, E.H., Jackson, T., & Laws, E. (1997). Volumetric magnetic resonance imaging evidence of bilateral hippocampal atrophy in mesial temporal lobe epilepsy. Epilepsia, 38, 588–594.CrossRefGoogle Scholar
Reitan, R.M. & Wolfson, D. (1993). The Halstead-Reitan Neuropsychological Test Battery: Theory and clinical interpretation. Tuscon, AZ: Neuropsychology Press.Google Scholar
Sandok, E.K., O'Brien, T.J., Jack, C.R., & So, E.L. (2000). Significance of cerebellar atrophy in intractable temporal lobe epilepsy: A quantitative MRI study. Epilepsia, 41, 1315–1320.CrossRefGoogle Scholar
Schoenfeld, J., Seidenberg, M., Woodard, A., Hecox, K., Inglese C., & Mack K., Hermann B. (1999). Neuropsychological and behavioral status of children with complex partial seizures. Developmental Medicine and Child Neurology, 41, 724–731.CrossRefGoogle Scholar
Seidenberg, M., Hermann, B.P., Bell, B., Sheth, R., Rutecki, P., Wendt, G., & Dow, C. (2002). Neuropsychological progression in childhood onset temporal lobe epilepsy. Manuscript submitted for publication.Google Scholar
Sisodiya, S.M., Moran, N., Free, S.L., Kitchen, N.D., Stevens, J.M., Harkness, W.F., Fish, D.R., & Shorvon, S.D. (1997). Correlation of widespread preoperative magnetic resonance imaging changes with unsuccessful surgery for hippocampal sclerosis. Annals of Neurology, 41, 490–496.CrossRefGoogle Scholar
Specht, U., May, T., Schulz, R., Rohde, M., Ebner, A., Schmidt, R.C., Schutz, M., & Wolf, P. (1997). Cerebellar atrophy and prognosis after temporal lobe resection. Journal of Neurology Neurosurgery and Psychiatry, 62, 501–506.CrossRefGoogle Scholar
Sutula, T.P. & Hermann, B. (1999). Progression in mesial temporal lobe epilepsy. Annals of Neurology, 45, 553–556.3.0.CO;2-D>CrossRefGoogle Scholar
Talairach, J. & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thieme Medical.Google Scholar
Tasch, E., Cendes, F., Li, L.M., Dubeau, F., Andermann, F., & Arnold, D.L. (1999). Neuroimaging evidence of progressive neuronal loss and dysfunction in temporal lobe epilepsy. Annals of Neurology, 45, 568–576.3.0.CO;2-P>CrossRefGoogle Scholar
Wasterlain, C.G., Thompson, K.W., Kornblum, H., Mazarati, A.M., Shirasaka, Y., Katsumori, H., Hantao, L., & Sankar, R. (1999). Long-term effects of recurrent seizures on the developing brain. In A. Nehlig, J. Motte, S.L. Moshe, & P. Plouin (Eds.), Childhood epilepsies and brain development (pp. 237–254). London: John Libby Inc.Google Scholar
Wechsler, D. (1997). Wechsler Adult Intelligence Scale (3rd ed.). San Antonio, TX: The Psychological Corporation.Google Scholar
Woermann, F.G., Barker, G.J., Birnie, K.D., Meencke, H.J., & Duncan, J.S. (1998). Regional changes in hippocampal T2 relaxation and volume: A quantitative magnetic resonance imaging study of hippocampal sclerosis. Journal of Neurology Neurosurgery and Psychiatry, 65, 656–664.CrossRefGoogle Scholar
Woods, R., Cherry, S., & Mazziotta, J. (1992). Rapid automated algorithm for aligning and reslicing PET images. Journal of Computer Assisted Tomography, 16, 620–633.CrossRefGoogle Scholar