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Social Cognition Abilities in Patients With Different Multiple Sclerosis Subtypes

Published online by Cambridge University Press:  28 June 2017

Audrey Henry*
Affiliation:
Cognition, Health and Socialization lab, University of Reims Champagne-Ardenne, Reims, France Psychopathology and Neuropsychology lab, University of Paris 8, Saint-Denis, France
Ayman Tourbah
Affiliation:
Psychopathology and Neuropsychology lab, University of Paris 8, Saint-Denis, France Reims University Hospital and Reims Faculty of Medicine, University of Reims Champagne-Ardenne, Reims, France
Marie-Pierre Chaunu
Affiliation:
Reims University Hospital and Reims Faculty of Medicine, University of Reims Champagne-Ardenne, Reims, France
Serge Bakchine
Affiliation:
Reims University Hospital and Reims Faculty of Medicine, University of Reims Champagne-Ardenne, Reims, France
Michèle Montreuil
Affiliation:
Psychopathology and Neuropsychology lab, University of Paris 8, Saint-Denis, France
*
Correspondence and reprint requests to: Audrey Henry, Université Reims Champagne-Ardenne, B.P. 30, 57 Rue Pierre Taittinger, 51 571, Reims Cedex, France. E-mail: [email protected]

Abstract

Objectives: Multiple sclerosis (MS) can be associated with impaired social cognition. However, social cognition skills have never been explored in the different subtypes of MS. The first aim of this study was to examine whether MS subtypes differ on the course of social cognition. The second aim was to explore the relationship between social cognition performances and executive abilities and mood variables. Methods: Sixty-two patients with MS and 33 healthy matched controls performed experimental tasks assessing facial emotion recognition, theory of mind (ToM), and cognitive functioning, in particular executive functions. Results: Patients differed from controls on both measures of social cognition. On the ToM measures, patients with progressive MS scored significantly lower than healthy participants. Patients with primary progressive MS performed worse than both healthy participants and patients with relapsing-remitting MS on the recognition of fearful facial expressions, while patients with secondary progressive MS performed worse on the recognition of facial expressions of sadness. Patients’ social cognition difficulties were correlated with processing speed, working memory, and verbal fluency. Conclusions: These preliminary results suggested that there may be qualitative differences in social cognition difficulties among the phenotypes. Furthermore, these impairments were related to executive functions, but unrelated to patients’ disability or level of depression. These data highlight the need for research to determine the real impact of these deficits on interpersonal relationships among patients and to confirm these disorders in a larger population with progressive forms of MS. (JINS, 2017, 23, 653–664)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2017 

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References

REFERENCES

Adolphs, R. (2002). Recognizing emotion from facial expressions: Psychological and neurological mechanisms. Behavioral and Cognitive Neuroscience Reviews, 1(1), 2162.CrossRefGoogle ScholarPubMed
Adolphs, R. (2009). The social brain: Neural basis of social knowledge. Annual Review of Psychology, 60, 693716. doi: 10.1146/annurev.psych.60.110707.163514 CrossRefGoogle ScholarPubMed
Banati, M., Sandor, J., Mike, A., Illes, E., Bors, L., Feldmann, A., & Illes, Z. (2010). Social cognition and theory of mind in patients with relapsing-remitting multiple sclerosis. European Journal of Neurology, 17(3), 426433. doi: 10.1111/j.1468-1331.2009.02836.x CrossRefGoogle ScholarPubMed
Baron-Cohen, S., O’Riordan, M., Stone, V., Jones, R., & Plaisted, K. (1999). Recognition of faux pas by normally developing children and children with Asperger syndrome or high-functioning autism. Journal of Autism and Developmental Disorders, 29(5), 407418.CrossRefGoogle ScholarPubMed
Benton, A.L., Sivan, A.B., Hamsher, K., Varney, N.R., & Spreen, O. (1983). Contribution to neuropsychological assessment. New York: Oxford University Press.Google Scholar
Benton, A.L., Sivan, A.B., Hamsher, K., Varney, N.R., & Spreen, O. (1994). Contributions to neuropsychological assessment. New York: Oxford University Press.Google Scholar
Berneiser, J., Wendt, J., Grothe, M., Kessler, C., Hamm, A.O., & Dressel, A. (2014). Impaired recognition of emotional facial expressions in patients with multiple sclerosis. Multiple Sclerosis and Related Disorders, 3(4), 482488. doi: 10.1016/j.msard.2014.02.001 CrossRefGoogle ScholarPubMed
Brothers, L. (1990). The social brain: A project for integrating primate behavior and neurophysiology in a new domain. Concepts in Neuroscience, 1, 2751.Google Scholar
Brune, M., & Brune-Cohrs, U. (2006). Theory of mind--Evolution, ontogeny, brain mechanisms and psychopathology. Neuroscience & Biobehavioral Review, 30(4), 437455. doi: 10.1016/j.neubiorev.2005.08.001 CrossRefGoogle ScholarPubMed
Buchanan, R.J., Minden, S.L., Chakravorty, B.J., Hatcher, W., Tyry, T., & Vollmer, T. (2010). A pilot study of young adults with multiple sclerosis: Demographic, disease, treatment, and psychosocial characteristics. Disability and Health Journal, 3(4), 262270. doi: 10.1016/j.dhjo.2009.09.003 CrossRefGoogle ScholarPubMed
Bull, R., Phillips, L.H., & Conway, C.A. (2008). The role of control functions in mentalizing: Dual-task studies of Theory of Mind and executive function. Cognition, 107(2), 663672. doi: http://dx.doi.org/10.1016/j.cognition.2007.07.015 CrossRefGoogle ScholarPubMed
Calder, A.J., Keane, J., Lawrence, A.D., & Manes, F. (2004). Impaired recognition of anger following damage to the ventral striatum. Brain, 127(Pt, 9, 19581969. doi: 10.1093/brain/awh214 CrossRefGoogle Scholar
Cardebat, D., Doyon, B., Puel, M., Goulet, P., & Joanette, Y. (1990). [Formal and semantic lexical evocation in normal subjects. Performance and dynamics of production as a function of sex, age and educational level]. Acta Neurologica Belgica, 90(4), 207217.Google ScholarPubMed
Cecchetto, C., Aiello, M., D’Amico, D., Cutuli, D., Cargnelutti, D., Eleopra, R., & Rumiati, R.I. (2014). Facial and bodily emotion recognition in multiple sclerosis: The role of alexithymia and other characteristics of the disease. Journal of the International Neuropsychological Society, 20(10), 10041014. doi: 10.1017/s1355617714000939 CrossRefGoogle ScholarPubMed
Chiaravalloti, N.D., & DeLuca, J. (2008). Cognitive impairment in multiple sclerosis. The Lancet Neurology, 7(12), 11391151. doi: 10.1016/s1474-4422(08)70259-x CrossRefGoogle ScholarPubMed
Comi, G., Filippi, M., Martinelli, V., Campi, A., Rodegher, M., Alberoni, M., & Canal, N. (1995). Brain MRI correlates of cognitive impairment in primary and secondary progressive multiple sclerosis. Journal of the Neurological Sciences, 132(2), 222227.CrossRefGoogle ScholarPubMed
Compston, A., & Coles, A. (2002). Multiple sclerosis. The Lancet, 359(9313), 12211231. doi: 10.1016/s0140-6736(02)08220-x CrossRefGoogle ScholarPubMed
Debouverie, M., Pittion-Vouyovitch, S., Louis, S., & Guillemin, F. (2007). Validity of a French version of the fatigue impact scale in multiple sclerosis. Multiple Sclerosis, 13(8), 10261032. doi: 10.1177/1352458507077942 CrossRefGoogle ScholarPubMed
Denney, D.R., Lynch, S.G., Parmenter, B.A., & Horne, N. (2004). Cognitive impairment in relapsing and primary progressive multiple sclerosis: Mostly a matter of speed. Journal of the International Neuropsychological Society, 10(7), 948956.CrossRefGoogle ScholarPubMed
Denney, D.R., Sworowski, L.A., & Lynch, S.G. (2005). Cognitive impairment in three subtypes of multiple sclerosis. Archives of Clinical Neuropsychology, 20(8), 967981. doi: 10.1016/j.acn.2005.04.012 CrossRefGoogle ScholarPubMed
Di Bitonto, L., Longato, N., Jung, B., Fleury, M., Marcel, C., Collongues, N., & Blanc, F. (2011). [Reduced emotional reactivity to negative stimuli in multiple sclerosis, preliminary results]. Revue Neurologique (Paris), 167(11), 820826. doi: 10.1016/j.neurol.2011.01.024 CrossRefGoogle ScholarPubMed
Ehrle, N., Henry, A., Pesa, A., & Bakchine, S. (2011). [Assessment of sociocognitive functions in neurological patients: Presentation of a French adaptation of two tools and implementation in frontal dementia]. Geriatrie, Psychologie et Neuropsychiatrie du Vieillissement, 9(1), 117128. doi: 10.1684/pnv.2010.0252 Google ScholarPubMed
Ekman, P., & Friesen, W.V. (1976). Pictures of facial affect. Palo Alto, CA: Consulting Psychologists Press.Google Scholar
Feinstein, A., DeLuca, J., Baune, B.T., Filippi, M., & Lassman, H. (2013). Cognitive and neuropsychiatric disease manifestations in MS. Multiple Sclerosis and Related Disorders, 2(1), 412. doi: 10.1016/j.msard.2012.08.001 CrossRefGoogle ScholarPubMed
Fett, A.K., Viechtbauer, W., Dominguez, M.D., Penn, D.L., van Os, J., & Krabbendam, L. (2011). The relationship between neurocognition and social cognition with functional outcomes in schizophrenia: A meta-analysis. Neuroscience & Biobehavioral Reviews, 35(3), 573588. doi: 10.1016/j.neubiorev.2010.07.001 CrossRefGoogle ScholarPubMed
Fisk, J.D., Pontefract, A., Ritvo, P.G., Archibald, C.J., & Murray, T.J. (1994). The impact of fatigue on patients with multiple sclerosis. Canadian Journal of Neurological Sciences, 21(1), 914.CrossRefGoogle ScholarPubMed
Foong, J., Rozewicz, L., Chong, W.K., Thompson, A.J., Miller, D.H., & Ron, M.A. (2000). A comparison of neuropsychological deficits in primary and secondary progressive multiple sclerosis. Journal of Neurology, 247(2), 97101.CrossRefGoogle ScholarPubMed
Fusar-Poli, P., Placentino, A., Carletti, F., Landi, P., Allen, P., Surguladze, S., & Politi, P. (2009). Functional atlas of emotional faces processing: A voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry & Neuroscience, 34(6), 418432.Google ScholarPubMed
Green, M.F., Penn, D.L., Bentall, R., Carpenter, W.T., Gaebel, W., Gur, R.C., &Heinssen, R. (2008). Social cognition in schizophrenia: An NIMH workshop on definitions, assessment, and research opportunities. Schizophrenia Bulletin, 34(6), 12111220. doi: 10.1093/schbul/sbm145 CrossRefGoogle ScholarPubMed
Gregory, C., Lough, S., Stone, V., Erzinclioglu, S., Martin, L., Baron-Cohen, S., & Hodges, J.R. (2002). Theory of mind in patients with frontal variant frontotemporal dementia and Alzheimer’s disease: Theoretical and practical implications. Brain, 125(Pt 4), 752764.CrossRefGoogle ScholarPubMed
Heaton, S.K., Chelune, G.J., Talley, J.L., Kay, G.G., & Curtiss, G. (1993). Wisconsin Card Sorting Test manual: Revised and expanded. Odessa, FL: Psychological Assessment Resources.Google Scholar
Henry, A., Bakchine, S., Maarouf, A., Chaunu, M.P., Rumbach, L., Magnin, E., & Montreuil, M. (2015). Facial emotion recognition and faux pas interpretation in multiple sclerosis. Brain Impairment, 16(3), 158172. doi: 10.1017/BrImp.2015.33 CrossRefGoogle Scholar
Henry, A., Tourbah, A., Chaunu, M.P., Rumbach, L., Montreuil, M., & Bakchine, S. (2011). Social cognition impairments in relapsing-remitting multiple sclerosis. Journal of the International Neuropsychological Society, 17(6), 11221131. doi: 10.1017/s1355617711001147 CrossRefGoogle ScholarPubMed
Henry, J.D., & Beatty, W.W. (2006). Verbal fluency deficits in multiple sclerosis. Neuropsychologia, 44(7), 11661174. doi: 10.1016/j.neuropsychologia.2005.10.006 CrossRefGoogle ScholarPubMed
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(2), 277285. doi: 10.1017/s1355617709090195 CrossRefGoogle ScholarPubMed
Honan, C.A., McDonald, S., Gowland, A., Fisher, A., & Randall, R.K. (2015). Deficits in comprehension of speech acts after TBI: The role of theory of mind and executive function. Brain and Language, 150, 6979. doi: http://dx.doi.org/10.1016/j.bandl.2015.08.007 CrossRefGoogle ScholarPubMed
Huijbregts, S.C., Kalkers, N.F., de Sonneville, L.M., de Groot, V., & Polman, C.H. (2006). Cognitive impairment and decline in different MS subtypes. Journal of the Neurological Sciences, 245(1-2), 187194. doi: 10.1016/j.jns.2005.07.018 CrossRefGoogle ScholarPubMed
Jehna, M., Neuper, C., Petrovic, K., Wallner-Blazek, M., Schmidt, R., Fuchs, S., & Enzinger, C. (2010). An exploratory study on emotion recognition in patients with a clinically isolated syndrome and multiple sclerosis. Clinical Neurology and Neurosurgery, 112(6), 482484. doi: 10.1016/j.clineuro.2010.03.020 CrossRefGoogle Scholar
Kipps, C.M., Duggins, A.J., McCusker, E.A., & Calder, A.J. (2007). Disgust and happiness recognition correlate with anteroventral insula and amygdala volume respectively in preclinical Huntington’s disease. Journal of Cognitive Neuroscience, 19(7), 12061217. doi: 10.1162/jocn.2007.19.7.1206 CrossRefGoogle ScholarPubMed
Krause, M., Wendt, J., Dressel, A., Berneiser, J., Kessler, C., Hamm, A.O., & Lotze, M. (2009). Prefrontal function associated with impaired emotion recognition in patients with multiple sclerosis. Behavioural Brain Research, 205(1), 280285. doi: 10.1016/j.bbr.2009.08.009 CrossRefGoogle ScholarPubMed
Kurtzke, J. F. (1983). Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS). Neurology, 33(11), 14441452.CrossRefGoogle ScholarPubMed
Lenne, B., Barthelemy, R., Nandrino, J.L., Sequeira, H., Pinti, A., Mecheri, H., & Hautecoeur, P. (2014). Impaired recognition of facial emotion expressions in multiple sclerosis. Neuropsychological Trends, 15, 6783. doi: 10.7358/neur-2014-015-lenn CrossRefGoogle Scholar
Lough, S., Gregory, C., & Hodges, J.R. (2001). Dissociation of social cognition and executive function in frontal variant frontotemporal dementia. Neurocase, 7(2), 123130. doi: 10.1093/neucas/7.2.123 CrossRefGoogle ScholarPubMed
Lough, S., Kipps, C.M., Treise, C., Watson, P., Blair, J.R., & Hodges, J.R. (2006). Social reasoning, emotion and empathy in frontotemporal dementia. Neuropsychologia, 44(6), 950958. doi: 10.1016/j.neuropsychologia.2005.08.009 CrossRefGoogle ScholarPubMed
Lublin, F.D., & Reingold, S.C. (1996). Defining the clinical course of multiple sclerosis: Results of an international survey. National Multiple Sclerosis Society (USA) Advisory Committee on Clinical Trials of New Agents in Multiple Sclerosis. Neurology, 46(4), 907911.CrossRefGoogle ScholarPubMed
Lublin, F.D., Reingold, S.C., Cohen, J.A., Cutter, G.R., Sørensen, P.S., Thompson, A.J., & Polman, C.H. (2014). Defining the clinical course of multiple sclerosis: The 2013 revisions. Neurology, 83(3), 278286. doi: 10.1212/WNL.0000000000000560 CrossRefGoogle ScholarPubMed
Mancuso, F., Horan, W.P., Kern, R.S., & Green, M.F. (2011). Social cognition in psychosis: Multidimensional structure, clinical correlates, and relationship with functional outcome. Schizophrenia Research, 125(2-3), 143151. doi: 10.1016/j.schres.2010.11.007 CrossRefGoogle ScholarPubMed
Ouellet, J., Scherzer, P.B., Rouleau, I., Metras, P., Bertrand-Gauvin, C., Djerroud, N., & Duquette, P. (2010). Assessment of social cognition in patients with multiple sclerosis. Journal of the International Neuropsychological Society, 16(2), 287296. doi: 10.1017/s1355617709991329 CrossRefGoogle ScholarPubMed
Perner, J., & Wimmer, H. (1985). ‘John thinks that Mary thinks that...’: Attribution of second-order beliefs by 5- to 10-year-old children. Journal of Experimental Child Psychology, 39, 437471.CrossRefGoogle 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(1), 131136. doi: 10.1037/a0020752 CrossRefGoogle ScholarPubMed
Pickup, G.J. (2008). Relationship between Theory of Mind and executive function in schizophrenia: A systematic review. Psychopathology, 41(4), 206213. doi: 10.1159/000125554 CrossRefGoogle ScholarPubMed
Pilgrim, B.M., Meyers, J.E., Bayless, J., & Whetstone, M.M. (1999). Validity of the Ward seven-subtest WAIS-III short form in a neuropsychological population. Applied Neuropsychology, 6(4), 243246. doi: 10.1207/s15324826an0604_7 CrossRefGoogle Scholar
Pinto, C., Gomes, F., Moreira, I., Rosa, B., Santos, E., & Silva, A.M. (2012). Emotion recognition in Multiple Sclerosis. Journal of Eye Tracking, Visual Cognition and Emotion, 2, 7681.Google Scholar
Polman, C.H., Reingold, S.C., Banwell, B., Clanet, M., Cohen, J.A., Filippi, M., & …Wolinsky, J.S. (2011). Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Annals of Neurology, 69, 292302.CrossRefGoogle Scholar
Pottgen, J., Dziobek, I., Reh, S., Heesen, C., & Gold, S.M. (2013). Impaired social cognition in multiple sclerosis. Journal of Neurology, Neurosurgery, & Psychiatry, 84(5), 523528. doi: 10.1136/jnnp-2012-304157 CrossRefGoogle ScholarPubMed
Prochnow, D., Donell, J., Schafer, R., Jorgens, S., Hartung, H.P., Franz, M., & Seitz, R.J. (2011). Alexithymia and impaired facial affect recognition in multiple sclerosis. Journal of Neurology, 258(9), 16831688. doi: 10.1007/s00415-011-6002-4 CrossRefGoogle ScholarPubMed
Rao, S.M., Leo, G.J., Bernardin, L., & Unverzagt, F. (1991). Cognitive dysfunction in multiple sclerosis. I. Frequency, patterns, and prediction. Neurology, 41(5), 685691.CrossRefGoogle ScholarPubMed
Roca, M., Manes, F., Gleichgerrcht, E., Ibanez, A., Gonzalez de Toledo, M.E., Marenco, V., & Sinay, V. (2014). Cognitive but not affective theory of mind deficits in mild relapsing-remitting multiple sclerosis. Cognitive and Behavioral Neurology, 27(1), 2530. doi: 10.1097/wnn.0000000000000017 CrossRefGoogle Scholar
Rowe, A.D., Bullock, P.R., Polkey, C.E., & Morris, R.G. (2001). “Theory of mind” impairments and their relationship to executive functioning following frontal lobe excisions. Brain, 124(Pt 3), 600616.CrossRefGoogle ScholarPubMed
Samson, D., Apperly, I.A., Kathirgamanathan, U., & Humphreys, G.W. (2005). Seeing it my way: A case of a selective deficit in inhibiting self-perspective. Brain, 128(Pt 5), 11021111. doi: 10.1093/brain/awh464 CrossRefGoogle Scholar
Stone, V.E., Baron-Cohen, S., & Knight, R.T. (1998). Frontal lobe contributions to theory of mind. Journal of Cognitive Neuroscience, 10(5), 640656.CrossRefGoogle ScholarPubMed
Van Kleef, G.A. (2009). How emotions regulate social life: The Emotions as Social Information (EASI) model. Current Directions in Psychological Science, 18(3), 184188. doi: 10.1111/j.1467-8721.2009.01633.x CrossRefGoogle Scholar
Wechsler, D. (1997). WAIS‐III administration and scoring manual. San Antonio, TX: Psychological Corporation.Google Scholar
Wimmer, H., & Perner, J. (1983). Beliefs about beliefs: Representation and constraining function of wrong beliefs in young children’s understanding of deception. Cognition, 13(1), 103128.CrossRefGoogle ScholarPubMed
Zigmond, A.S., & Snaith, R.P. (1983). The hospital Anxiety and Depression Scale. Acta Psychiatrica Scandinavica, 67(6), 361370.CrossRefGoogle ScholarPubMed
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