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Abstract

Background:

Patients with multiple sclerosis (MS) frequently reveal social behavior disturbance. Nevertheless, little is known regarding the impact of MS on social cognition, particularly theory of mind (ToM), and its neural basis.

Objectives:

To explore how ToM is affected in MS and its neural correlates.

Methods:

Enrolled 60 consecutive MS patients and 60 healthy controls (HC) matched on age, sex, and education. Participants underwent ToM testing (Eyes Test, Videos Test) and 3 T brain magnetic resonance imaging (MRI). Using Freesurfer software, cortical and subcortical gray matter (GM) volumes were calculated.

Results:

MS patients performed worse on Eyes Test (58.7% ± 13.8% vs 81.9% ± 10.4%, p < 0.001) and Videos Test (75.3% ± 9.3% vs 88.1% ± 7.1%, p < 0.001). Eyes Test performance in MS was positively correlated with the volume of subcortical structures (amygdala, putamen) and cortical regions (entorhinal cortex, fusiform gyrus, superior temporal gyrus, superior parietal gyrus, supramarginal gyrus, medial orbitofrontal cortex, anterior and posterior cingulate gyrus). In regression analysis, amygdala volume was the single predictor of performance (R² change = 0.064, p = 0.031), and a mediation analysis indicated that it contributes for the differences observed between MS and HC.

Conclusion:

Patients with MS have impairment on social cognition. Amygdala atrophy was the main predictor probably due to its central position within the “social brain” network.

Keywords

Multiple sclerosis social cognition theory of mind social brain amygdala

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References

Fishman

Benedict

Bakshi

et al . Construct validity and frequency of euphoria sclerotica in multiple sclerosis. J Neuropsychiatry Clin Neurosci 2004; 16: 350–356.

Adolphs

. Cognitive neuroscience of human social behaviour. Nat Rev Neurosci 2003; 4: 165–178.

Banati

Sandor

Mike

et al . Social cognition and Theory of Mind in patients with relapsing-remitting multiple sclerosis. Eur J Neurol 2010; 17: 426–433.

Ouellet

Scherzer

Rouleau

et al . Assessment of social cognition in patients with multiple sclerosis. J Int Neuropsychol Soc 2010; 16: 287–296.

Pottgen

Dziobek

Reh

et al . Impaired social cognition in multiple sclerosis. J Neurol Neurosurg Psychiatry 2013; 84: 523–528.

Henry

Tourbah

Chaunu

et al . Social cognition impairments in relapsing-remitting multiple sclerosis. J Int Neuropsychol Soc 2011; 17: 1122–1131.

Mike

Strammer

Aradi

et al . 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 2013; 8: e82422.

Polman

Reingold

Banwell

et al . Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 2011; 69: 292–302.

Kurtzke

. Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS). Neurology 1983; 33: 1444–1452.

10.

Baron-Cohen

Wheelwright

Hill

et al . The “Reading the Mind in the Eyes” Test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. J Child Psychol Psychiatry 2001; 42: 241–251.

11.

Sullivan

Ruffman

. Social understanding: How does it fare with advancing years? Br J Psychol 2004; 95: 1–18.

12.

Benedict

RHB

Fischer

Archibald

et al . Minimal neuropsychological assessment of MS patients: A consensus approach. Clin Neuropsychol 2002; 16: 381–397.

13.

Smith

. Symbol digit modalities test: Manual. Los Angeles: Western Psychological Services, 1982.

14.

Rao

. A manual for the brief, repeatable battery of neuropsychological tests in multiple sclerosis. New York: National Multiple Sclerosis Society, 1991.

15.

Gronwall

. Paced auditory serial-addition task: A measure of recovery from concussion. Percept Mot Skills 1977; 44: 367–373.

16.

Benedict

RHB

. Brief visuospatial memory test-revised: Professional manual. Odessa, FL: Psychological Assessment Resources, 1997.

17.

Delis

Kramer

Kaplan

et al . California verbal learning test manual (adult version). 2nd ed. San Antonio, TX: Psychological Corporation, 2000.

18.

Benton

Sivan

Hamsher

et al . Contributions to neuropsychological assessment. New York: Oxford University Press, 1994.

19.

Heaton

. Wisconsin card sorting test manual. Odessa, FL: Psychological Assessment Resources, 1981.

20.

Parmenter

Zivadinov

Kerenyi

et al . Validity of the Wisconsin card sorting and Delis–Kaplan executive function system (DKEFS) sorting tests in multiple sclerosis. J Clin Exp Neuropsychol 2007; 29: 215–223.

21.

Benedict

Cookfair

Gavett

et al . Validity of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). J Int Neuropsychol Soc 2006; 12: 549–558.

22.

Alves

Simoes

Martins

. The estimation of premorbid intelligence levels among Portuguese speakers: The Irregular Word Reading Test (TeLPI). Arch Clin Neuropsychol 2012; 27: 58–68.

23.

Vaz Serra

Pio Abreu

. Aferição dos quadros depressivos. I—Ensaio de aplicação do Inventário Depressivo de Beck a uma amostra portuguesa de doentes deprimidos. Coimbra Méd 1973; 20: 623–644.

24.

Fisk

Pontefract

Ritvo

et al . The impact of fatigue on patients with multiple sclerosis. Can J Neurol Sci 1994; 21: 9–14.

25.

Gomes

. Validação da versão portuguesa da escala de impacto da fadiga modificada e da escala de severidade da fadiga na esclerose múltipla. Braga: University of Minho, 2011.

26.

Fischl

Sereno

Dale

. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 1999; 9: 195–207.

27.

Dale

Fischl

Sereno

. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 1999; 9: 179–194.

28.

Schmidt

Gaser

Arsic

et al . An automated tool for detection of FLAIR-hyperintense white-matter lesions in Multiple Sclerosis. Neuroimage 2012; 59: 3774–3783.

29.

Cohen

. Statistical power analysis for the behavioral sciences. New York: Routledge, 1977.

30.

Bickart

Dickerson

Barrett

. The amygdala as a hub in brain networks that support social life. Neuropsychologia 2014; 63: 235–248.

31.

Siegal

Varley

. Neural systems involved in “theory of mind.” Nat Rev Neurosci 2002; 3: 463–471.

32.

Kennedy

Glascher

Tyszka

et al . Personal space regulation by the human amygdala. Nat Neurosci 2009; 12: 1226–1227.

33.

Adolphs

. Is the human amygdala specialized for processing social information? Ann N Y Acad Sci 2003; 985: 326–340.

34.

Dineen

Vilisaar

Hlinka

et al . Disconnection as a mechanism for cognitive dysfunction in multiple sclerosis. Brain 2009; 132: 239–249.

35.

Baron-Cohen

Jolliffe

Mortimore

et al . Another advanced test of theory of mind: Evidence from very high functioning adults with autism or asperger syndrome. J Child Psychol Psychiatry 1997; 38: 813–822.

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Impairment of social cognition in multiple sclerosis: Amygdala atrophy is the main predictor

Abstract

Background:

Objectives:

Methods:

Results:

Conclusion:

Keywords

Get full access to this article

References

Supplementary Material