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Memory Performance and Normalized Regional Brain Volumes in Patients with Pediatric-Onset Multiple Sclerosis

Published online by Cambridge University Press:  10 February 2012

Amanda Fuentes
Affiliation:
Department of Psychology, York University, Toronto, Ontario
Donald Louis Collins
Affiliation:
McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, QC
Daniel Garcia-Lorenzo
Affiliation:
McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, QC
John G. Sled
Affiliation:
Research Institute, The Hospital for Sick Children, Toronto, Ontario
Sridar Narayanan
Affiliation:
McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, QC
Douglas L. Arnold
Affiliation:
McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, QC
Brenda L. Banwell
Affiliation:
Research Institute, The Hospital for Sick Children, Toronto, Ontario Division of Neurology, Department of Paediatrics, University of Toronto, Toronto, Ontario
Christine Till*
Affiliation:
Department of Psychology, York University, Toronto, Ontario Research Institute, The Hospital for Sick Children, Toronto, Ontario
*
Correspondence and reprint requests to: Christine Till, Department of Psychology, York University, 4700 Keele Street, Toronto, Ontario M3J 1P3. E-mail: [email protected]

Abstract

Studies in adults with multiple sclerosis (MS) have associated regional brain abnormalities with memory impairment. While memory problems in children with MS are often reported, little is known about the neural correlates that may contribute to these difficulties. We measured verbal and nonverbal memory using the Test of Memory and Learning (TOMAL-2) in 32 children and adolescents with MS and 26 age- and sex-matched healthy controls. Memory performance was correlated with volumetric measures of the whole brain, hippocampus, amygdala, and thalamus. Brain volumes were normalized for age and sex using magnetic resonance imaging (MRI) data from the National Institutes of Health MRI Study of Normal Brain development. With the exception of story recall, performance on memory tests was similar to that of the control group. Relative to controls, patient with MS showed reduced volume in the whole brain (p < .001), amygdala (p < .005), and thalamus (p < .001), but not the hippocampus. In the patient group, word-list learning correlated with whole brain volume (r = .53) and hippocampal volume (r = .43), whereas visual recognition memory correlated with thalamic volume (r = .48). Findings are consistent with the well-established role of the hippocampus in learning and consolidation and also highlight the importance of diffuse brain pathology on memory function. (JINS, 2012, 18, 471–480)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2012

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References

Amato, M.P., Goretti, B., Ghezzi, A., Lori, S., Zipoli, V., Portaccio, E., Trojano, M. (2008). Cognitive and psychosocial features of childhood and juvenile MS. Neurology, 70, 18911897.CrossRefGoogle ScholarPubMed
Anderson, V.M., Fisniku, L.K., Khaleeli, Z., Summers, M.M., Penny, S.A., Altman, D.R., Miller, D.H. (2010). Hippocampal atrophy in relapsing-remitting and primary progressive MS: A comparative study. Multiple Sclerosis, 16, 10831090.CrossRefGoogle ScholarPubMed
Aubert-Broche, B., Fonov, V., Ghassemi, R., Narayanan, S., Arnold, D.L., Banwell, B., Collins, D.L. (2011). Regional brain atrophy in children with multiple sclerosis. Neuroimage, 58(2), 409415.CrossRefGoogle ScholarPubMed
Banwell, B.L., Anderson, P.E. (2005). The cognitive burden of multiple sclerosis in children. Neurology, 64, 891894.CrossRefGoogle ScholarPubMed
Benedict, R.H.B., Ramsamy, D., Munshauer, F., Weinstock-Guttman, B., Zivadinov, R. (2009). Memory impairment in multiple sclerosis: Correlation with deep grey matter and mesial temporal atrophy. Journal of Neurology, Neurosurgery, and Psychiatry, 80, 201206.CrossRefGoogle ScholarPubMed
Collins, D.L., Holmes, T.M., Peters, T.M., Evans, A.C. (1995). Automatic 3D model-based neuroanatomical segmentation. Human Brain Mapping, 3(3), 190208.CrossRefGoogle Scholar
Collins, D.L., Neelin, P., Peters, T.M., Evans, A.C. (1994). Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. Journal of Computer Assisted Tomography, 18(2), 192205.CrossRefGoogle ScholarPubMed
Collins, D.L., Pruessner, J.C. (2010). Towards accurate, automatic segmentation of the hippocampus and amygdala from MRI by augmenting ANIMAL with a template library and label fusion. Neuroimage, 52, 1355.CrossRefGoogle ScholarPubMed
Cowan, N., Wood, N., Keller, T., Nugent, L.D., Keller, C.V. (1998). Two separate verbal processing rates contributing to short-term memory span. Journal of Experimental Psychology: General, 127, 141160.CrossRefGoogle ScholarPubMed
de Haan, M., Mishkin, M., Baldeweg, T., Vargha-Khadem, F. (2006). Human memory development and its dysfunction after early hippocampal injury. Trends in Neurosciences, 29, 374381.CrossRefGoogle ScholarPubMed
Fonov, V., Evans, A.C., Botteron, K., Almli, C.R., McKinstry, R.C., Collins, L. (2011). Unbiased average age-appropriate atlases for pediatric studies. Neuroimage, 54(1), 313327.CrossRefGoogle ScholarPubMed
Fritsch, T., Larsen, J.D., Smyth, K.A. (2007). The role of adolescent IQ and gender in the use of cognitive support for remembering in aging. Aging, Neuropsychology, and Cognition, 14, 394416.CrossRefGoogle ScholarPubMed
Geurts, J.J., Bo, L., Roosendaal, S.D., Hazes, T., Daniels, R., Barkhof, F., van der Valk, P. (2007). Extensive hippocampal demyelination in multiple sclerosis. Journal of Neuropathology and Experimental Neurology, 66(9), 819827.CrossRefGoogle ScholarPubMed
Geurts, J.J., Reuling, I.E., Vrenken, H., Uitdehaag, B.M., Polman, C.H., Castelijns, J.A., Pouwels, P.J. (2006). MR spectroscopic evidence for thalamic and hippocampal, but not cortical, damage in multiple sclerosis. Magnetic Resonance in Medicine, 55(3), 478483.CrossRefGoogle Scholar
Greenstein, Y., Blachstein, H., Vakil, E. (2010). Interrelations between attention and verbal memory is affected by developmental age. Child Neuropsychology, 16, 4259.CrossRefGoogle ScholarPubMed
Haist, F., Shimamura, A.P., Squire, L.R. (1992). On the relationship between recall and recognition memory. Journal of Experimental Psychology: Learning, Memory, and Cognition, 18, 691702.Google ScholarPubMed
Holm, S. (1977). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6, 6570.Google Scholar
Janowsky, J.S., Shimamura, A.P., Kritchevsky, M., Squire, L.R. (1989). Cognitive impairment following frontal lobe damage and its relevance to human amnesia. Behavioral Neuroscience, 103, 548560.CrossRefGoogle ScholarPubMed
Kurtzke, J. (1983). Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS). Neurology, 33, 14441452.CrossRefGoogle ScholarPubMed
MacAllister, W.S., Belman, A.L., Milazzo, M., Weisbrot, D.M., Christodoulou, C., Scherl, W.F., Krupp, L.B. (2005). Cognitive functioning in children and adolescents with multiple sclerosis. Neurology, 64, 14221425.CrossRefGoogle ScholarPubMed
Nocentini, U., Pasqualetti, P., Bonavita, S., Buccafusca, M., De Caro, M.F., Farina, D., Caltagirone, C. (2006). Cognitive dysfunction in patients with relapsing-remitting multiple sclerosis. Multiple Sclerosis, 12, 7787.CrossRefGoogle ScholarPubMed
Olivares, T., Sanchez, M.P., Wollmann, T., Hernandez, M.A., Barroso, J. (2005). Pattern of neuropsychological impairment in early phases of relapsing-remitting multiple sclerosis. Multiple Sclerosis, 11, 191197.CrossRefGoogle ScholarPubMed
Papadopoulos, D., Sumayya, D., Patel, R., Nicholas, R., Vora, A., Reynolds, R. (2009). Substantial archaeocortical atrophy and neuronal loss in multiple sclerosis. Brain Pathology, 19, 238253.CrossRefGoogle ScholarPubMed
Paulesu, E., Perani, D., Fazio, F., Comi, G., Pozzilli, C., Martinelli, V., Fieschi, C. (1996). Functional basis of memory impairment in multiple sclerosis: A[18F]FDG PET study. Neuroimage, 4, 8796.CrossRefGoogle ScholarPubMed
Polman, C.H., Reingold, S.C., Edan, G., Filippi, M., Hartung, H., Kappos, L., Wolinsky, J.S. (2005). Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald criteria.”. Annals of Neurology, 58, 840846.CrossRefGoogle Scholar
Ramasamy, D.P., Benedict, R.H.B., Cox, J.L., Fritz, D., Abdelrahman, N., Hussein, S., Zivadinov, R. (2009). Extent of cerebellum, subcortical and cortical atrophy in patients with MS: A case-control study. Journal of the Neurological Sciences, 282, 4754.CrossRefGoogle ScholarPubMed
Rao, S.M., Leo, G.J., St. Aubin-Faubert, P. (1989). On the nature of memory disturbance in multiple sclerosis. Journal of Clinical and Experimental Neuropsychology, 11(5), 699712.CrossRefGoogle ScholarPubMed
Reynolds, C.R., Kamphaus, R.W. (2004). In Assessments P. (Ed.), Behavior assessment system for children, second edition (BASC-2). Bloomington, MN: AGS Publishing.Google Scholar
Reynolds, C.R., Voress, J.K. (2007). Test of memory and learning–second edition (TOMAL-2). Texas: Pro-Ed.Google Scholar
Roosendaal, S.D., Hulst, H.E., Vrenken, H., Feenstra, H.E., Castellins, J.A., Pouwels, P.J., Geurts, J.J. (2010). Structural and functional hippocampal changes in multiple sclerosis patients with intact memory function. Radiology, 225, 595604.CrossRefGoogle Scholar
Sicotte, N.L., Kern, K.C., Giesser, B.S., Arshanapalli, A., Schultz, M., Montag, M., Boohheimer, S.Y. (2008). Regional hippocampal atrophy in multiple sclerosis. Brain, 131, 11341141.CrossRefGoogle ScholarPubMed
Sled, J.G., Zijdenbos, A.P., Evans, A.C. (1998). A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Transactions on Medical Imaging, 17, 8797.CrossRefGoogle ScholarPubMed
Smith, S.M., Zhang, Y., Jenkinson, M., Chen, J., Matthews, P.M., Federico, A., De Stefano, N. (2002). Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage, 17, 479489.CrossRefGoogle ScholarPubMed
Squire, L.R., Stark, C.E., Clark, R.E. (2004). The medial temporal lobe. Annual Review of Neuroscience, 27, 279306.CrossRefGoogle ScholarPubMed
Till, C., Ghassemi, R., Aubert-Broche, B., Narayanan, S., Arnold, D.L., Desrocher, M., Banwell, B. (2011). MRI correlates of cognitive impairment in childhood onset multiple sclerosis. Neuropsychology, 25(3), 319332.CrossRefGoogle ScholarPubMed
Van Der Werf, Y.D., Jolles, J., Witter, M.P., Uylings, H.B. (2003). Contributions of thalamic nuclei to declarative memory functioning. Cortex, 39, 10471062.CrossRefGoogle ScholarPubMed
Wechsler, D. (1999). Wechsler abbreviated scale of intelligence (WASI). San Antonio, TX: The Psychological Corporation.Google Scholar
Zola-Morgan, S., Squire, L.R. (1993). Neuroanatomy of memory. Annual Review of Neuroscience, 16, 547563.CrossRefGoogle ScholarPubMed