Skip to main content
Log in

Social Cognition in Multiple Sclerosis: a Meta-Analysis

  • Review
  • Published:
Neuropsychology Review Aims and scope Submit manuscript

Abstract

Multiple sclerosis (MS) is associated with cognitive decline and impairment in social functioning. Accumulating evidence suggests that patients with MS are impaired in social cognition, including theory of mind (ToM) and emotion recognition. In this meta-analysis of 24 studies, facial emotion recognition and ToM performances of 989 patients with MS and 836 healthy controls were compared. MS was associated with significant impairments with medium effect sizes in ToM (d = 0.57) and facial emotion recognition (d = 0.61). Among individual emotions recognition of fear and anger were particularly impaired. The severity of social cognitive deficits was significantly associated with non-social cognitive impairment. These deficits in social cognition may underpin difficulties in social functioning in MS. However, there is a need for further studies investigating the longitudinal evolution of social cognitive deficits and their neural correlates in MS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Banati, M., Sandor, J., Mike, A., et al. (2010). Social cognition and theory of mind in patients with relapsing-remitting multiple sclerosis. European Journal of Neurology, 17, 426–433.

    Article  CAS  PubMed  Google Scholar 

  • Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., & Plumb, I. (2001). The reading the mind in the eyes” test revised version: a study with normal adults, and adults with asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry, 42, 241–251.

    Article  CAS  PubMed  Google Scholar 

  • Bax, L., Yu, L. M., Ikeda, N., Tsuruta, H., & Moons, K. G. (2006). Development and validation of MIX: comprehensive free software for meta-analysis of causal research data. BMC Medical Research Methodology, 6, 50.

    Article  PubMed  PubMed Central  Google Scholar 

  • Beatty, W. W., Goodkin, D. E., Weir, W. S., et al. (1989). Affective judgments by patients with Parkinson’s disease or chronic progressive multiple sclerosis. Bulletin of the Psychonomic Society, 27, 361–364.

    Article  Google Scholar 

  • Beatty, W. W., Orbelo, D. M., Sorocco, K. H., & Ross, E. D. (2003). Comprehension of affective prosody in multiple sclerosis. Multiple Sclerosis, 9, 148–153.

    Article  PubMed  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, 482–488.

    Article  PubMed  Google Scholar 

  • Bora, E., & Berk, M. (2016). Theory of mind in major depressive disorder: a meta-analysis. Journal of Affective Disorders, 191, 49–55.

    Article  PubMed  Google Scholar 

  • Bora, E., & Pantelis, C. (2013). Theory of mind impairments in first-episode psychosis, individuals at ultra-high risk for psychosis and in first-degree relatives of schizophrenia: systematic review and meta-analysis. Schizophrenia Research, 144, 31–36.

    Article  PubMed  Google Scholar 

  • Bora, E., Eryavuz, A., Kayahan, B., Sungu, G., & Veznedaroglu, B. (2006). Social functioning, theory of mind and neurocognition in outpatients with schizophrenia; mental state decoding may be a better predictor of social functioning than mental state reasoning. Psychiatry Research, 145, 95–103.

    Article  PubMed  Google Scholar 

  • Bora, E., Walterfang, M., & Velakoulis, D. (2015a). Theory of mind in behavioural-variant frontotemporal dementia and Alzheimer’s disease: a meta-analysis. Journal of Neurology, Neurosurgery, and Psychiatry, 86, 714–719.

    Article  PubMed  Google Scholar 

  • Bora, E., Walterfang, M., & Velakoulis, D. (2015b). Theory of mind in Parkinson’s disease: a meta-analysis. Behavioural Brain Research, 292, 515–520.

    Article  PubMed  Google Scholar 

  • Bora, E., & Pantelis, C. (2016). Meta-analysis of social cognition in attention-deficit/hyperactivity disorder (ADHD): comparison with healthy controls and autistic spectrum disorder. Psychological Medicine, 46, 699–716.

  • Bora, E., Velakoulis, D., & Walterfang, M. (2016). Social cognition in Huntington’s disease. Behavioural Brain Research, 297, 131–140.

    Article  PubMed  Google Scholar 

  • Brandon, L.R. (2015). Theory of mind in multiple sclerosis: disease subtype differences and association with measures of social functioning. University of Missouri-Kansas City (thesis).

  • Cecchetto, C., Aiello, M., D’Amico, D., et al. (2014). Facial and bodily emotion recognition in multiple sclerosis: the role of alexithymia and other characteristics of the disease. Journal of International Neuropsychological Society, 20, 1004–1014.

    Article  Google Scholar 

  • Chahraoui, K., Duchene, C., Rollot, F., Bonin, B., & Moreau, T. (2014). Longitudinal study of alexithymia and multiple sclerosis. Brain and Behavior, 4, 75–82.

    Article  PubMed  Google Scholar 

  • Charvet, L. E., Cleary, R. E., Vazquez, K., Belman, A. L., Krupp, L. B., & US Network for Pediatric MS. (2014). Social cognition in pediatric-onset multiple sclerosis (MS). Multiple Sclerosis, 20, 1478–1484.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chiaravalloti, N. D., & DeLuca, J. (2008). Cognitive impairment in multiple sclerosis. Lancet Neurology, 7, 1139–1151.

    Article  PubMed  Google Scholar 

  • Compston, A., & Coles, A. (2002). Multiple sclerosis. Lancet, 359(9313), 1221–1231.

    Article  PubMed  Google Scholar 

  • Cruz-Gómez, Á. J., Ventura-Campos, N., Belenguer, A., Ávila, C., & Forn, C. (2014). The link between resting-state functional connectivity and cognition in MS patients. Multiple Sclerosis, 20, 338–348.

    Article  PubMed  Google Scholar 

  • DeLuca, G. C., Yates, R. L., Beale, H., & Morrow, S. A. (2015). Cognitive impairment in multiple sclerosis: clinical, radiologic and pathologic insights. Brain Pathology, 25, 79–98.

    Article  PubMed  Google Scholar 

  • Di Bitonto, L., Longato, N., Jung, B., et al. (2011). Reduced emotional reactivity to negative stimuli in multiple sclerosis, preliminary results. Revue Neurologique (Paris), 167, 820–826.

    Article  Google Scholar 

  • Dulau, C (2014). Existe-t-il vraiment une atteinte de la cognition sociale dans la scl’erose en plaques? Human health and pathology < dumas-01089147 > (Thesis Bordeaux University) http//dumas.ccsd.cnrs.fr/dumas-01089147

  • Ekman, P., & Friesen, W. (1976). Pictures of facial affect. Palo Alto: Consulting Psychologists Press.

    Google Scholar 

  • Filippi, M., Rocca, M. A., Benedict, R. H., et al. (2010). The contribution of MRI in assessing cognitive impairment in multiple sclerosis. Neurology, 75, 2121–2128.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fusar-Poli, P., Placentino, A., Carletti, F., et al. (2009). Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry and Neuroscience, 34, 418–432.

    PubMed  PubMed Central  Google Scholar 

  • Genova, H. M., Cagna, C. J., Chiaravalloti, N. D., DeLuca, J., Lengenfelder, J. (2016). Dynamic assessment of social cognition in individuals with multiple sclerosis: a pilot study. Journal of International Neuropsychological Society 22, 83–88.

  • Geurts, J. J. G., & Barkhof, F. (2008). Grey matter pathology in multiple sclerosis. Lancet Neurology, 7, 841–851.

    Article  PubMed  Google Scholar 

  • Gleichgerrcht, E., Tomashitis, B., & Sinay, V. (2015). The relationship between alexithymia, empathy and moral judgment in patients with multiple sclerosis. European Journal of Neurology, 22, 1295–1303.

    Article  CAS  PubMed  Google Scholar 

  • Hanken, K., Eling, P., & Hildebrandt, H. (2015). Is there a cognitive signature for MS-related fatigue? Multiple Sclerosis, 21, 376–381.

    Article  PubMed  Google Scholar 

  • Henry, J. D., & Beatty, W. W. (2006). Verbal fluency deficits in multiple sclerosis. Neuropsychologia, 44, 1166–1174.

    Article  PubMed  Google Scholar 

  • Henry, J. D., Phillips, L. H., Beatty, W. W., et al. (2009). Evidence for deficits in facial affect recognition and theory of mind in multiple sclerosis. Journal of International Neuropsychological Society, 15, 277–285.

    Article  Google 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 International Neuropsychological Society, 17, 1122–1131.

    Article  Google Scholar 

  • Hsieh, S., Hornberger, M., Piguet, O., & Hodges, J. R. (2012). Brain correlates of musical and facial emotion recognition: evidence from the dementias. Neuropsychologia, 50, 1814–1822.

    Article  CAS  PubMed  Google Scholar 

  • Jehna, M., Neuper, C., Petrovic, K., et al. (2010). An exploratory study on emotion recognition in patients with a clinically isolated syndrome and multiple sclerosis. Clinical Neurology and Neurosurgery, 112, 482–484.

    Article  PubMed  Google Scholar 

  • Jehna, M., Langkammer, C., Wallner-Blazek, M., et al. (2011). Cognitively preserved MS patients demonstrate functional differences in processing neutral and emotional faces. Brain Imaging and Behavior, 5, 241–251.

    Article  PubMed  Google Scholar 

  • Johnston, L., Miles, L., & McKinlay, A. (2008). A critical review of the eyes test as a measure of social-cognitive impairment. Australian Journal of Psychology, 60, 135–141.

    Article  Google Scholar 

  • Kraemer, M., Herold, M., Uekermann, J., et al. (2013a). Theory of mind and empathy in patients at an early stage of relapsing remitting multiple sclerosis. Clinical Neurology and Neurosurgery, 115, 1016–1022.

    Article  PubMed  Google Scholar 

  • Kraemer, M., Herold, M., Uekermann, J., et al. (2013b). Perception of affective prosody in patients at an early stage of relapsing-remitting multiple sclerosis. Journal of Neuropsychology, 7, 91–106.

    Article  PubMed  Google Scholar 

  • Krause, M., Wendt, J., Dressel, A., Berneiser, J., Kessler, C., Hamm, A. O., et al. (2009). Prefrontal function associated with impaired emotion recognition in patients with multiple sclerosis. Behavioural Brain Research, 205, 280–285.

    Article  PubMed  Google Scholar 

  • Krause, I., Kern, S., Horntrich, A., & Ziemssen, T. (2013). Employment status in multiple sclerosis: impact of disease-specific and non-disease-specific factors. Multiple Sclerosis, 19, 1792–1799.

    Article  PubMed  Google Scholar 

  • Langdon, D. W. (2011). Cognition in multiple sclerosis. Current Opinion in Neurology, 24, 244–249.

    Article  PubMed  Google Scholar 

  • Lenne, B., Barthelemy, R., Nandrino, J. L., et al. (2014). Impaired recognition of facial emotional expressions in multiple sclerosis. Neuropsychological Trends, 15, 67–83.

    Article  Google Scholar 

  • Lyros, E., Messinis, L., Papageorgiou, S. G., & Papathanasopoulos, P. (2010). Cognitive dysfunction in multiple sclerosis: the effect of pharmacological interventions. International Review of Psychiatry, 22, 35–42.

    Article  PubMed  Google Scholar 

  • Mike, A., Strammer, E., Aradi, M., Orsi, G., Perlaki, G., Hajnal, A., et al. (2013). Disconnection mechanism and regional cortical atrophy contribute to impaired processing of facial expressions and theory of mind in multiple sclerosis: a structural MRI study. PLoS ONE, 8, e82422.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mitolo, M., Venneri, A., Wilkinson, I. D., & Sharrack, B. (2015). Cognitive rehabilitation in multiple sclerosis: a systematic review. Journal of the Neurological Sciences, 354, 1–9.

    Article  PubMed  Google Scholar 

  • Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & Group PRISMA. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ, 339, b2535.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ouellet, J., Scherzer, P. B., Rouleau, I., et al. (2010). Assessment of social cognition in patients with multiple sclerosis. Journal of International Neuropsychological Society, 16, 287–296.

    Article  Google Scholar 

  • Parada-Fernández, P., Oliva-Macías, M., Amayra, I., López-Paz, J. F., Lázaro, E., Martínez, Ó., Jometón, A., Berrocoso, S., García de Salazar, H., Pérez, M. (2015). Accuracy and reaction time in recognition of facial emotions in people with multiple sclerosis. Revista de Neurologia 61, 433–440.

  • Passamonti, L., Cerasa, A., Liguori, M., Gioia, M. C., Valentino, P., Nisticò, R., et al. (2009). Neurobiological mechanisms underlying emotional processing in relapsing-remitting multiple sclerosis. Brain, 132, 3380–3391.

    Article  PubMed  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.

    Article  PubMed  Google Scholar 

  • Pinto, C., Gomes, F., Moreira, I., et al. (2012). Emotion recognition in multiple sclerosis. The Journal of Eye Tracking, Visual Cognition and Emotion, 2, 76–81.

    Google Scholar 

  • Planche, V., Gibelin, M., Cregut, D., Pereira, B., & Clavelou, P. (2015). Cognitive impairment in a population-based study of patients with multiple sclerosis: differences between late relapsing-remitting, secondary progressive and primary progressive multiple sclerosis. European Journal of Neurology. doi:10.1111/ene.12715.

    PubMed  Google Scholar 

  • Pöttgen, J., Dziobek, I., Reh, S., Heesen, C., & Gold, S. M. (2013). Impaired social cognition in multiple sclerosis. Journal of Neurology, Neurosurgery, and Psychiatry, 84, 523–528.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prochnow, D., Donell, J., Schäfer, R., et al. (2011). Alexithymia and impaired facial affect recognition in multiple sclerosis. Journal of Neurology, 258, 1683–1688.

    Article  CAS  PubMed  Google Scholar 

  • Radlak, B. (2014). Social cognition in multiple scleoris. Effects of social participation and quality of life. University of Aberdeen (Thesis).

  • Rao, S. M., Leo, G. J., Bernardin, L., & Unverzagt, F. (1991a). Cognitive dysfunction in multiple sclerosis. I. Frequency, patterns, and prediction. Neurology, 41, 685–691.

    Article  CAS  PubMed  Google Scholar 

  • Rao, S. M., Leo, G. J., Ellington, L., Nauertz, T., Bernardin, L., & Unverzagt, F. (1991b). Cognitive dysfunction in multiple sclerosis. II. Impact on employment and social functioning. Neurology, 41, 692–696.

    Article  CAS  PubMed  Google Scholar 

  • Roca, M., Manes, F., Gleichgerrcht, E., et al. (2014). Cognitive but not affective theory of mind deficits in mild relapsing-remitting multiple sclerosis. Cognitive and Behavioral Neurology, 27, 25–30.

    Article  PubMed  Google Scholar 

  • Rosenberg, H., McDonald, S., Dethier, M., Kessels, R. P., & Westbrook, R. F. (2014). Facial emotion recognition deficits following moderate-severe traumatic brain injury (TBI): re-examining the valence effect and the role of emotion intensity. Journal of the International Neuropsychological Society, 20, 994–1003.

    Article  PubMed  Google Scholar 

  • Rosti-Otajärvi, E., & Hämäläinen, P. (2013). Behavioural symptoms and impairments in multiple sclerosis: a systematic review and meta-analysis. Multiple Sclerosis, 19, 31–45.

    Article  PubMed  Google Scholar 

  • Sabbagh, M. A. (2004). Understanding orbitofrontal contributions to theory-of-mind reasoning: implications for autism. Brain and Cognition, 55, 209–219.

    Article  PubMed  Google Scholar 

  • Sabbagh, M. A., Moulson, M. C., & Harkness, K. L. (2004). Neural correlates of mental state decoding in human adults: an event-related potential study. Journal of Cognitive Neuroscience, 16, 415–426.

    Article  PubMed  Google Scholar 

  • Schaafsma, S. M., Pfaff, D. W., Spunt, R. P., & Adolphs, R. (2015). Deconstructing and reconstructing theory of mind. Trends in Cognitive Science, 19, 65–72.

    Article  Google Scholar 

  • Schoonheim, M. M., Meijer, K. A., & Geurts, J. J. (2015). Network collapse and cognitive impairment in multiple sclerosis. Frontiers in Neurology, 6, 82.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sripada, C. S., Kessler, D., & Angstadt, M. (2014). Lag in maturation of the brain’s intrinsic functional architecture in attention-deficit/hyperactivity disorder. PNAS U S A, 111, 14259–14264.

    Article  CAS  Google Scholar 

  • Stone, V. E., Baron-Cohen, S., & Knight, R. T. (1998). Frontal lobe contributions to theory of mind. Journal of Cognitive Neuroscience, 10, 640–656.

    Article  CAS  PubMed  Google Scholar 

  • Strober, L. B., Rao, S. M., Lee, J. C., Fischer, E., & Rudick, R. (2014). Cognitive impairment in multiple sclerosis: an 18 year follow-up study. Multiple Sclerosis and Related Disorders, 3, 473–481.

    Article  PubMed  Google Scholar 

  • Stroup, D. F., Berlin, J. A., Morton, S. C., et al. (2000). Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA, 283, 2008–2012.

    Article  CAS  PubMed  Google Scholar 

  • Sumowski, J. F., & Leavitt, V. M. (2013). Cognitive reserve in multiple sclerosis. Multiple Sclerosis, 19, 1122–1127.

    Article  PubMed  Google Scholar 

  • Van Schependom, J., D’hooghe, M. B., Cleynhens, K., et al. (2014). The symbol digit modalities test as sentinel test for cognitive impairment in multiple sclerosis. European Journal of Neurology, 21, 1219–1225. e71-2.

    Article  PubMed  Google Scholar 

  • Vanotti, S., Rojas, G., Allegri, R., Caceres, F., & RELACCEM work group. (2012). How behavioral and quality of life changes affect social cognition in multiple sclerosis patients. Neurology, 178, P02.042.

    Google Scholar 

  • Viechtbauer, W. (2010). Conducting meta-analyses in R with the metafor package. Journal of Statistical Software, 36, 1–48.

    Article  Google Scholar 

  • Wallace, B. C., Dahabreh, I. J., Trikalinos, T. A., Lau, J., Trow, P., & Schmid, C. H. (2012). Closing the gap between methodologists and end-users: R as a computational back-end. Journal of Statistical Software, 49, 1–15.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Emre Bora.

Ethics declarations

Funding

This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

Competing Interests

Authors have no conflicts of interest regarding subject of this manuscript. Dr. Walterfang reports grants from Actelion pharmaceuticals, personal fees from Actelion pharmaceuticals, personal fees from Orphazyme, outside the submitted work; Dr Ozakbas reports non-financial support from Bayer, Novartis, Merck-Serono and Teva.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 139 kb)

ESM 2

(DOC 128 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bora, E., Özakbaş, S., Velakoulis, D. et al. Social Cognition in Multiple Sclerosis: a Meta-Analysis. Neuropsychol Rev 26, 160–172 (2016). https://doi.org/10.1007/s11065-016-9320-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11065-016-9320-6

Keywords

Navigation