Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-09T14:09:45.524Z Has data issue: false hasContentIssue false
  • English
  • Français

The Nature of Verbal Memory Impairment in Multiple Sclerosis: A List-Learning and Meta-analytic Study

Published online by Cambridge University Press:  23 September 2013

Jose M. Lafosse ,
Sandra M. Mitchell ,
John R. Corboy  and
Christopher M. Filley
Jose M. Lafosse*
Affiliation:
Department of Psychology & Neuroscience, Regis University, Denver, Colorado
Sandra M. Mitchell
Affiliation:
New Mexico Veterans Affairs Healthcare System, Albuquerque, New Mexico
John R. Corboy
Affiliation:
Department of Neurology, University of Colorado School of Medicine, Denver, Colorado Denver Veterans Affairs Medical Center, Denver, Colorado
Christopher M. Filley
Affiliation:
Department of Neurology, University of Colorado School of Medicine, Denver, Colorado Denver Veterans Affairs Medical Center, Denver, Colorado Department of Psychiatry, University of Colorado School of Medicine, Denver, Colorado
*
Correspondence and reprint requests to: Jose M. Lafosse, Department of Psychology & Neuroscience, Regis University, 3333 Regis Boulevard, D-12, Denver, CO 80221-1099. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The primary purpose of this study was to test the hypothesis that multiple sclerosis (MS) patients have impaired acquisition rather than a retrieval deficit. Verbal memory impairment in MS was examined in 53 relapsing-remitting MS patients and 31 healthy controls (HC), and in a meta-analysis of studies that examined memory functioning in MS with list-learning tasks. The MS group demonstrated significantly lower acquisition and delayed recall performance than the HC group, and the meta-analysis revealed that the largest effect sizes were obtained for acquisition measures relative to delayed recall and recognition. Our data argue against a retrieval deficit as the sole explanation for verbal memory impairment in MS, and make a consistent case for the position that deficient acquisition contributes to the memory dysfunction of MS patients. Deficient acquisition may result from demyelination in relevant white matter tracts that reduces encoding efficiency as a result of impaired speed of information processing. (JINS, 2013, 19, 995–1008)

Keywords

Multiple sclerosisMemoryLearningWhite matter diseaseNeuropsychological testsMeta analysis
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 19 , Issue 9 , October 2013 , pp. 995 - 1008
Copyright
Copyright © The International Neuropsychological Society 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

*References marked with an asterisk indicate studies included in the meta-analysis.Google Scholar
Archibald, C.J., Fisk, J.D. (2000). Information processing efficiency in patients with multiple sclerosis. Journal of Clinical and Experimental Neuropsychology, 22, 686–701.CrossRefGoogle ScholarPubMed
*Armstrong, C., Onishi, K., Robinson, K., D'Esposito, M., Thompson, H., Rostami, A., Grossman, M. (1996). Serial position and temporal cue effects in multiple sclerosis: Two subtypes of defective memory mechanisms. Neuropsychologia, 34, 853–862.CrossRefGoogle ScholarPubMed
Arnett, P.A. (2004). Speed of presentation influences story recall in college students and persons with multiple sclerosis. Archives of Clinical Neuropsychology, 19, 507–523.CrossRefGoogle ScholarPubMed
*Basso, M.R., Candilis, P.J., Johnson, J., Ghormley, C., Combs, D.R., Ward, T. (2010). Capacity to make medical treatment decisions in multiple sclerosis: A potentially remediable deficit. Journal of Clinical and Experimental Neuropsychology, 32, 1050–1061. doi:10.1080/13803391003683062CrossRefGoogle ScholarPubMed
Beatty, W.W., Blanco, C.R., Wilbanks, S.L., Paul, R.H., Hames, K.A. (1995). Demographic, clinical and cognitive characteristics of multiple sclerosis patients who continue to work. Journal of Neurologic Rehabilitation, 9, 167–173.Google Scholar
Beck, A.T., Steer, R.A., Brown, G.K. (1996). Beck Depression Inventory (2nd ed.). Manual. San Antonio, TX: The Psychological Corporation.Google Scholar
*Benedict, R.H.B., Weinstock-Guttman, B., Fishman, I., Sharma, J., Tjoa, C.W., Bakshi, R. (2004). Prediction of neuropsychological impairment in multiple sclerosis: Comparison of conventional magnetic resonance imaging measures of atrophy and lesion burden. Archives of Neurology, 61, 226–230. doi:10.1001/archneur.61.2.226CrossRefGoogle ScholarPubMed
*Bomboi, G., Ikonomidou, V.N., Pellegrini, S., Stern, S.K., Gallo, A., Auh, S., Bagnato, F. (2011). Quality and quantity of diffuse of focal white matter disease and cognitive disability of patients with multiple sclerosis. Journal of Neuroimaging, 21, e57–e63. doi:10.1111/j.1552-6569.2010.00488CrossRefGoogle ScholarPubMed
Brooks, B.L., Weaver, L.E., Scialfa, C.T. (2006). Does impaired executive functioning differentially impact verbal memory measures in older adults with suspected dementia? The Clinical Neuropsychologist, 20(2), 230–242.CrossRefGoogle ScholarPubMed
*Bruce, J.M., Bruce, A.S., Hancock, L., Lynch, S. (2010). Self-reported memory problems in multiple sclerosis: Influence of psychiatric status and normative dissociative experiences. Archives of Clinical Neuropsychology, 25, 39–48. doi:10.1093/arclin/acp092CrossRefGoogle ScholarPubMed
*Brunner, R., Schaefer, D., Hess, K., Parzer, P., Resch, F., Schwab, S. (2005). Effect of corticosteroids on short-term and long-term memory. Neurology, 64, 335–337.CrossRefGoogle ScholarPubMed
Buschke, H., Fuld, P.A. (1974). Evaluating storage, retention, and retrieval in disordered memory and learning. Neurology, 24, 1019–1025.CrossRefGoogle ScholarPubMed
*Caine, E.D., Bamford, K.A., Schiffer, R.B., Shoulson, I., Levy, S. (1986). A controlled neuropsychological comparison of Huntington's disease and multiple sclerosis. Archives of Neurology, 43, 249–254.CrossRefGoogle ScholarPubMed
*Carone, D.A., Benedict, R.H.B., Munschauer, F.E. III, Fishman, I., Weinstock-Guttman, B. (2005). Interpreting patient/informant discrepancies of reported cognitive symptoms in MS. Journal of the International Neuropsychological Society, 11, 574–583. doi:10.1017/S135561770505068XCrossRefGoogle ScholarPubMed
Chiaravalloti, N.D., Balzano, J., Moore, N.B., DeLuca, J. (2008). The Open-Trial Selective Reminding Test (OT-SRT) as a tool for the assessment of learning and memory. The Clinical Neuropsychologist, 23, 231–254.CrossRefGoogle Scholar
Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Erlbaum.Google Scholar
Coolidge, F.L., Middleton, P.A., Griego, J.A. (1996). The effects of interference on verbal learning in multiple sclerosis. Archives of Clinical Neuropsychology, 11, 605–611.CrossRefGoogle ScholarPubMed
Cooper, H., Hedges, L.V. (1994). The handbook of research synthesis. New York: Russell Sage Foundation.Google Scholar
Delis, D.C., Kramer, J.H., Kaplan, E., Ober, B.A. (1987). Manual for the California Verbal Learning Test - Adult Version. San Antonio, TX: The Psychological Corporation.Google Scholar
Delis, D.C., Kramer, J.H., Kaplan, E., Ober, B.A. (2000). Manual for the Revised California Verbal Learning Test - Adult Version (2nd ed.). San Antonio, TX: The Psychological Corporation.Google Scholar
DeLuca, J., Barbieri-Berger, S., Johnson, S.K. (1994). The nature of memory impairments in multiple sclerosis: Acquisition versus retrieval. Journal of Clinical and Experimental Neuropsychology, 16, 183–189.CrossRefGoogle ScholarPubMed
DeLuca, J., Chelune, G.J., Tulsky, D.S., Lengenfelder, J., Chiaravolloti, N.D. (2004). Is speed of processing or working memory the primary information processing deficit in multiple sclerosis? Journal of Clinical and Experimental Neuropsychology, 26, 550–562.CrossRefGoogle ScholarPubMed
DeLuca, J., Gaudino, E.A., Diamond, B.J., Christodoulou, C., Engel, R.A. (1998). Acquisition and storage deficits in multiple sclerosis. Journal of Clinical and Experimental Neuropsychology, 20, 376–390.CrossRefGoogle ScholarPubMed
*DeLuca, J., Genova, H.M., Hillary, F.G., Wylie, G. (2008). Neural correlates of cognitive fatigue in multiple sclerosis using functional MRI. Journal of the Neurological Sciences, 270, 28–39. doi:10.1016/j.jns.2008.01.018CrossRefGoogle ScholarPubMed
*DeLuca, J., Johnson, S.K., Beldowicz, D., Natelson, B.H. (1995). Neuropsychological impairments in chronic fatigue syndrome, multiple sclerosis, and depression. Journal of Neurology, Neurosurgery, and Psychiatry, 58, 38–43. doi:10.1136/jnnp.58.1.38CrossRefGoogle ScholarPubMed
Demaree, H.A., DeLuca, J., Gaudino, E.A., Diamond, B.J. (1999). Speed of information processing as a key deficit in multiple sclerosis: Implications for rehabilitation. Journal of Neurology, Neurosurgery, and Psychiatry, 67, 661–663.CrossRefGoogle ScholarPubMed
Demaree, H.A., Gaudino, E.A., DeLuca, J., Ricker, J.H. (2000). Learning impairment is associated with recall ability in multiple sclerosis. Journal of Clinical and Experimental Neuropsychology, 22, 865–873.CrossRefGoogle ScholarPubMed
*Diamond, B.J., DeLuca, J., Johnson, S.K., Kelley, S.M. (1997). Verbal learning in amnesic anterior communicating artery aneurysm patients and in patients with multiple sclerosis. Applied Neuropsychology, 4, 89–98.CrossRefGoogle ScholarPubMed
*Diamond, B.J., Johnson, S.K., Kaufman, M., Graves, L. (2008). Relationship between information processing, depression, fatigue and cognition in multiple sclerosis. Archives of Clinical Neuropsychology, 23, 189–199. doi:10.1016/j.acn.2007.10.002CrossRefGoogle ScholarPubMed
Diaz-Olavarrieta, C., Cummings, J.L., Velazquez, J., Garcia de la Cadena, C. (1999). Neuropsychiatric manifestations of multiple sclerosis. Journal of Neuropsychiatry & Clinical Neurosciences, 11, 51–57.CrossRefGoogle ScholarPubMed
Durlak, J.A. (1998). Understanding meta-analysis. In L. G. Grimm & P. R. Yarnold (Eds.), Reading and understanding multivariate statistics (pp. 319–352). Washington, DC: American Psychological Association.Google Scholar
*Fielding, J., Kilpatrick, T., Millist, L., White, O. (2009). Multiple sclerosis: Cognition and saccadic eye movements. Journal of the Neurological Sciences, 277, 32–36. doi:10.1016/j.jns.2008.10.001CrossRefGoogle ScholarPubMed
Filley, C.M. (1998). The behavioral neurology of cerebral white matter. Neurology, 50, 1535–1540.CrossRefGoogle ScholarPubMed
Filley, C.M. (2012). The behavioral neurology of white matter (2nd ed.). New York: Oxford University Press.CrossRefGoogle ScholarPubMed
Filley, C.M., Franklin, G.M., Heaton, R.K., Rosenberg, N.L. (1988). White matter dementia: Clinical disorders and implications. Neuropsychiatry, Neuropsychology, and Behavioral Neurology, 1, 239–254.Google Scholar
Fischer, J.S., Priore, R.L., Jacobs, L.D., Cookfair, D.L., Rudick, R.A., Herndon, R.M., Kooijmans-Coutinho, M.F. (2000). Neuropsychological effects of interferon beta-1a in relapsing multiple sclerosis. Annals of Neurology, 48, 885–892.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
*Fisk, J.D., Archibald, C.J. (2001). Limitations of the Paced Auditory Serial Addition Test as a measure of working memory in patients with multiple sclerosis. Journal of the International Neuropsychological Society, 7, 363–372.CrossRefGoogle ScholarPubMed
Folstein, M.F., Folstein, S.E., McHugh, P.R. (1975). “Mini-Mental State”: A practical method of grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198.CrossRefGoogle ScholarPubMed
Foong, J., Rozewicz, L., Quaghebeur, G., Davie, C.A., Kartsounis, L.D., Thompson, A.J., Ron, A. (1997). Executive function in multiple sclerosis. The role of frontal lobe pathology. Brain, 120, 15–26.CrossRefGoogle ScholarPubMed
*Forn, C., Barros-Loscertales, A., Escudero, J., Benlloch, V., Campos, S., Parcet, M.A., Avila, C. (2007). Compensatory activations with patients with multiple sclerosis during preserved performance on the N-Back task. Human Brain Mapping, 28, 424–430.CrossRefGoogle ScholarPubMed
*Fuso, S.F., Callegaro, D., Pompéia, S., Bueno, O.F.A. (2010). Working memory impairment in multiple sclerosis relapsing-remitting patients with episodic memory deficits. Arquivos de Neuro-Psiquiatria, 68, 205–211. doi:10.1590/S0004-282×2012000400021CrossRefGoogle ScholarPubMed
*Gaines, J.J., Gavett, R.A., Lynch, J.J., Bakshi, R., Benedict, R.H.B. (2008). New error type and recall consistency indices for the Brief Visuospatial Memory Test – Revised: Performance in healthy adults and multiple sclerosis patients. The Clinical Neuropsychologist, 22, 851–863. doi:10.1080/13854040701565216CrossRefGoogle ScholarPubMed
Gaudino, E.A., Chiaravalloti, N.D., DeLuca, J., Diamond, B.J. (2001). A comparison of memory performance in relapsing-remitting, primary progressive and secondary progressive, multiple sclerosis. Neuropsychiatry, Neuropsychology, and Behavioral Neurology, 14, 32–44.Google ScholarPubMed
*Goverover, Y., Chiaravalloti, N., DeLuca, J. (2008). Self-generation to improve learning and memory of functional activities in persons with multiple sclerosis: Meal preparation and managing finances. Archives of Physical Medicine and Rehabilitation, 89, 1514–1521. doi:10.1016/j.apmr.2007.11.059CrossRefGoogle ScholarPubMed
*Griffiths, S.Y., Yamamoto, A., Boudreau, V.G., Ross, L.K., Kozora, E., Thornton, A.E. (2005). Memory interference in multiple sclerosis. Journal of the International Neuropsychological Society, 11, 737–746. doi:10.1017/S135561770505085XCrossRefGoogle ScholarPubMed
Hedges, L.V., Olkin, I. (1985). Statistical methods for meta-analysis. San Diego, CA: Academic Press, Inc.Google Scholar
*Henry, J.D., Phillips, L.H., Beatty, W.W., McDonald, S., Longley, W.A., Joscelyne, A., Rendell, P.G. (2009). Evidence for deficits in facial affect recognition and theory of mind in multiple sclerosis. Journal of the International Neuropsychological Society, 15, 277–285. doi:10.1017/S1355617709090195CrossRefGoogle ScholarPubMed
Higgins, J.P.T., Thompson, S.G. (2002). Quantifying heterogeneity in a meta-analysis. Statistics in Medicine, 21, 1539–1558.CrossRefGoogle ScholarPubMed
Higgins, J.P.T., Thompson, S.G., Deeks, J.J., Altman, D.G. (2003). Measuring inconsistency in meta-analyses. British Medical Journal, 327, 557–560.CrossRefGoogle ScholarPubMed
*Houtchens, M.K., Benedict, R.H.B., Killiany, R., Sharma, J., Jaisani, Z., Singh, B., Bakshi, R. (2007). Thalamic atrophy and cognition in multiple sclerosis. Neurology, 69, 1213–1223. doi:10.1212/01.wnl.0000276992.17011.b5CrossRefGoogle ScholarPubMed
Hulst, H.E., Schoonheim, M.M., Roosendaal, S.D., Popescu, V., Schweren, L.J.S., van der Werf, Y.D., Geurts, J.J.G. (2012). Functional adaptive changes within the hippocampal memory system of patients with multiple sclerosis. Human Brain Mapping, 33, 2268–2280.CrossRefGoogle ScholarPubMed
*Iwasaki, Y., Kinoshita, M., Ikeda, K., Takamiya, K. (1989). Cognitive function in multiple sclerosis and its relation to functional abilities. International Journal of Neuroscience, 48, 219–223.CrossRefGoogle ScholarPubMed
*Jennekens-Schinkel, A., van der Velde, E.A., Sanders, E.A., Lanser, J.B. (1990). Memory and learning in outpatients with quiescent multiple sclerosis. Journal of the Neurological Sciences, 95, 311–325.CrossRefGoogle ScholarPubMed
King, D.A., Caine, E.D. (1996). Cognitive impairment and major depression: Beyond the pseudodementia syndrome. In I. Grant & K.M. Adams (Eds.), Neuropsychological assessment of neuropsychiatric disorders (2nd ed., Chapt. 9, pp. 200–217). New York: Oxford.CrossRefGoogle Scholar
*Lafosse, J.M., Corboy, J.R., Leehey, M.A., Seeberger, L.C., Filley, C.M. (2007). MS vs. HD: Can white matter and subcortical gray matter pathology be distinguished neuropsychologically? Journal of Clinical and Experimental Neuropsychology, 29, 142–154. doi:10.1080/13803390600582438CrossRefGoogle ScholarPubMed
*Ling, N.D., Selby, M.J. (1998). Assessment of memory in multiple sclerosis patients using the Memory Assessment Scale. Perceptual and Motor Skills, 86, 987–998.CrossRefGoogle ScholarPubMed
Lipsey, M.W., Wilson, D.B. (2000). Practical meta-analysis. Thousand Oaks, CA: Sage Publications.Google Scholar
*Litvan, I., Grafman, J., Vendrell, P., Martinez, J.M. (1988). Slowed information processing in multiple sclerosis. Archives of Neurology, 45, 281–285.CrossRefGoogle ScholarPubMed
Longenecker, J., Kohn, P., Liu, S., Zoltick, B., Weinberger, D.R., Elvevag, B. (2010). Data-driven methodology illustrating mechanisms underlying word list recall: Applications to clinical research. Neuropsychology, 24(5), 625–636.Google ScholarPubMed
Lucchinetti, C.F., Popescu, B.F., Bunyan, R.F., Moll, N.M., Roemer, S.F., Lassmann, H., Ransohoff, R.M. (2011). Inflammatory cortical demyelination in early multiple sclerosis. New England Journal of Medicine, 365(23), 2188–2197.CrossRefGoogle ScholarPubMed
Macartney-Filgate, M.S., Vriezen, E.R. (1988). Intercorrelation of clinical tests of verbal memory. Archives of Clinical Neuropsychology, 3, 121–126.CrossRefGoogle ScholarPubMed
*Maurelli, M., Marchioni, E., Cerretano, R., Bosone, D., Bergamaschi, R., Citterio, A., Savoldi, F. (1992). Neuropsychological assessment in MS: Clinical, neurophysiological and neuroradiological relationships. Acta Neurologica Scandinavica, 86, 124–128.Google ScholarPubMed
Mesulam, M.M. (1990). Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Annals of Neurology, 28, 597–613.CrossRefGoogle ScholarPubMed
*Middleton, L.S., Denney, D.R., Lynch, S.G., Parmenter, B. (2006). The relationship between perceived and objective cognitive functioning in multiple sclerosis. Archives of Clinical Neuropsychology, 21, 487–494. doi:10.1016/j.acn.2006.06.008CrossRefGoogle ScholarPubMed
*Minden, S.L., Moes, E.J., Orav, J., Kaplan, E., Reich, P. (1990). Memory impairment in multiple sclerosis. Journal of Clinical and Experimental Neuropsychology, 12, 566–586.CrossRefGoogle ScholarPubMed
*Nocentini, U., Rossini, P.M., Carlesimo, G.A., Graceffa, A., Grasso, M.G., Lupoi, D., Caltagirone, C. (2001). Patterns of cognitive impairment in secondary progressive stable phase of multiple sclerosis: Correlations with MRI findings. European Neurology, 45, 11–18.CrossRefGoogle ScholarPubMed
*Olivares, T., Nieto, A., Sanchez, M.P., Wollmann, T., Hernandez, M.A., Barroso, J. (2005). Pattern of neuropsychological impairment in the early phase of relapsing-remitting multiple sclerosis. Multiple Sclerosis, 11, 191–197. doi:10.1191/1352458505ms1139oaCrossRefGoogle ScholarPubMed
Onwuegbuzie, A.J., Leech, N.L. (2012). Meta-analysis research: Cautions and limitations. Manuscript in preparation.Google Scholar
Orwin, R.G. (1983). A fail-safe N for effect size. Journal of Educational Statistics, 8, 157–159.Google Scholar
*Phillips, L.H., Henry, J.D., Scott, C., Summers, F., Whyte, M., Cook, M. (2011). Specific impairments of emotion perception in multiple sclerosis. Neuropsychology, 25, 131–136. doi:10.1037/A0020752CrossRefGoogle ScholarPubMed
Pliskin, N.H., Hamer, D.P., Goldstein, D.S., Towle, V.L., Reder, A.T., Noronha, A., Arnason, B.B. (1996). Improved delayed visual reproduction test performance in multiple sclerosis patients receiving interferon beta-1b. Neurology, 47, 1463–1468.CrossRefGoogle ScholarPubMed
Poser, C.M., Paty, D.W., Scheinberg, L., McDonald, W.I., Davis, F.A., Ebers, G.C., Tourtellotte, W.W. (1983). New diagnostic criteria for multiple sclerosis: Guidelines for research protocols. Annals of Neurology, 13, 227–231.CrossRefGoogle ScholarPubMed
*Pozzilli, C., Passafiume, D., Bernardi, S., Pantano, P., Incoccia, C., Bastianello, S., Fieschi, C. (1991). SPECT, MRI and cognitive functions in multiple sclerosis. Journal of Neurology, Neurosurgery and Psychiatry, 54, 110–115.CrossRefGoogle ScholarPubMed
Prakash, R.S., Snook, E.M., Lewis, J.M., Motl, R.W., Kramer, A.F. (2008). Cognitive impairments in relapsing-remitting multiple sclerosis: A meta-analysis. Multiple Sclerosis, 14, 1250–1261.CrossRefGoogle ScholarPubMed
Randolph, C., Gold, J.M., Kozora, E., Cullum, C.M., Hermann, B.P., Wyler, A.R. (1994). Estimating memory function: Disparity of Wechsler Memory Scale-Revised and California Verbal Learning Test indices in clinical and normal samples. The Clinical Neuropsychologist, 8, 99–108.CrossRefGoogle Scholar
*Randolph, J.J., Wishart, H.A., Saykin, A.J., McDonald, B.C., Schuschu, K.R., MacDonald, J.W., Kasper, L.H. (2005). FLAIR lesion volume in multiple sclerosis: Relation to processing speed and verbal memory. Journal of the International Neuropsychological Society, 11, 205–209. doi:10.1017/S1355617705050253CrossRefGoogle ScholarPubMed
*Rao, S.M., Hammeke, T.A., McQuillen, M.P., Khatri, B.O., Lloyd, D. (1984). Memory disturbance in chronic progressive multiple sclerosis. Archives of Neurology, 41, 625–631.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, 699–712.CrossRefGoogle ScholarPubMed
*Rendell, P.G., Jensen, F., Henry, J.D. (2007). Prospective memory in multiple sclerosis. Journal of the International Neuropsychological Society, 13, 410–416. doi:10.1017/S1355617707070579CrossRefGoogle ScholarPubMed
*Rosti, E., Hämäläinen, P., Koivisto, K., Hokkanen, L. (2007). PASAT in detecting cognitive impairment in relapsing-remitting MS. Applied Neuropsychology, 14, 101–112.CrossRefGoogle ScholarPubMed
Ruggieri, R.M., Palermo, R., Vitello, G., Gennuso, M., Settipani, N., Piccoli, (2003). Cognitive impairment in patients suffering from relapsing-remitting multiple sclerosis with EDSS < or = 3.5. Acta Neurological Scandinavica, 108, 323–326. doi:10.1034/j.1600-0404.2003.00157CrossRefGoogle ScholarPubMed
*Sanfilipo, M.P., Benedict, R.H.B., Weinstock-Guttman, B., Bakshi, R. (2006). Gray and white matter brain atrophy and neuropsychological impairment in multiple sclerosis. Neurology, 66, 685–692.CrossRefGoogle ScholarPubMed
Scarrabelotti, M., Carroll, M. (1999). Memory dissociation and metamemory in multiple sclerosis. Neuropsychologia, 37, 1335–1350.CrossRefGoogle ScholarPubMed
*Scarrabelotti, M., Carroll, M. (1998). Awareness of remembering achieved through automatic and conscious processes in multiple sclerosis. Brain and Cognition, 38, 183–201.CrossRefGoogle ScholarPubMed
*Schulz, D., Kopp, B., Kunkel, A., Faiss, J.H. (2006). Cognitive in the early stage of multiple sclerosis. Journal of Neurology, 253, 1002–1010. doi:10.1007/s00415-006-0145-8CrossRefGoogle ScholarPubMed
Sicotte, N.L., Kern, K.C., Giesser, B.S., Arshanapalli, A., Schultz, A., Montag, M., Bookheimer, S.Y. (2008). Regional hippocampal atrophy in multiple sclerosis. Brain, 131, 1134–1141.CrossRefGoogle ScholarPubMed
*Solari, A., Mancuso, L., Motta, A., Mendozzi, L., Serrati, C. (2002). Comparison of two brief neuropsychological batteries in people with multiple sclerosis. Multiple Sclerosis, 8, 169–176.CrossRefGoogle ScholarPubMed
*Stegen, S., Stepanov, I., Cookfair, D., Schwartz, E., Hojnacki, D., Weinstock-Guttman, B., Benedict, R.H.B. (2010). Validity of the California Verbal Learning Test-II in multiple sclerosis. The Clinical Neuropsychologist, 24, 189–202. doi:10.1080/13854040903266910CrossRefGoogle ScholarPubMed
*Strober, L., Englert, J., Munschauer, F., Weinstock-Guttman, B., Rao, S., Benedict, R.H.B. (2009). Sensitivity of conventional memory tests in multiple sclerosis: Comparing the Rao Brief Repeatable Neuropsychological Battery and the Minimal Assessment of Cognitive Function in MS. Multiple Sclerosis, 15, 1077–1084.CrossRefGoogle ScholarPubMed
Thornton, A.E., Raz, N. (1997). Memory impairment in multiple sclerosis: A quantitative review. Neuropsychology, 11, 357–366.CrossRefGoogle ScholarPubMed
Thornton, A.E., Raz, N., Tucker, K.A. (2002). Memory in multiple sclerosis: Contextual encoding deficits. Journal of the International Neuropsychological Society, 8, 395–409.CrossRefGoogle ScholarPubMed
*Tinnefeld, M., Treitz, F.H., Haase, C.G., Wilhelm, H., Daum, I., Faustmann, P.M. (2005). Attention and memory dysfunctions in mild multiple sclerosis. European Archives of Psychiatry and Clinical Neuroscience, 255, 319–326. doi:10.1007/S00406-005-0565-YCrossRefGoogle ScholarPubMed
*Tong, B.S.K., Yip, J.T.H., Lee, T.M.C., Li, L.S.W. (2002). Frontal fluency and memory functioning among multiple sclerosis patients in Hong Kong. Brain Injury, 16, 987–995.Google ScholarPubMed
*van den Burg, W., van Zomeren, A.H., Minderhoud, J.M., Prange, A.J., Meijer, N.S. (1987). Cognitive impairment in patients with multiple sclerosis and mild physical disability. Archives of Neurology, 44, 494–501.CrossRefGoogle ScholarPubMed
*Wachowius, U., Talley, M., Silver, N., Heinze, H.J., Sailer, M. (2005). Cognitive impairment in primary and secondary progressive multiple sclerosis. Journal of Clinical and Experimental Neuropsychology, 27, 65–77. doi:10.1080/138033990513645CrossRefGoogle ScholarPubMed
*Wallace, G.L., Holmes, S. (1993). Cognitive-linguistic assessment of individuals with multiple sclerosis. Archives of Physical Medicine and Rehabilitation, 74, 637–643.CrossRefGoogle ScholarPubMed
Wishart, H., Sharpe, D. (1997). Neuropsychological aspects of multiple sclerosis: A quantitative review. Journal of Clinical and Experimental Neuropsychology, 19, 810–824.CrossRefGoogle ScholarPubMed
Wolf, F.M. (1986). Meta-analysis: Quantitative methods for research synthesis. Newbury, London: Sage.CrossRefGoogle Scholar
Zakzanis, K.K. (2001). Statistics to tell the truth, the whole truth, and nothing but the truth: Formulae, illustrative numerical examples, and heuristic interpretation of effect size analyses for neuropsychological researchers. Archives of Clinical Neuropsychology, 16, 653–667.CrossRefGoogle ScholarPubMed
Zakzanis, K.K. (2000). Distinct neurocognitive profiles in multiple sclerosis subtypes. Archives of Clinical Neuropsychology, 15, 115–136.CrossRefGoogle ScholarPubMed