Advertisement
Original article| Volume 45, 102333, October 2020

Social cognition in Multiple Sclerosis is associated to changes in brain connectivity: A resting-state fMRI study

      Highlights

      • A specific social cognition impairment is described in Multiple Sclerosis patients.
      • Resting-state functional connectivity has found to be altered in Multiple Sclerosis.
      • Connectivity of fusiform cortex is related with social cognition impairment.
      • Visual processing areas are functionally related to social cognition.
      • Functional connectivity of amygdala is related with social cognition.

      Abstract

      Background: Multiple Sclerosis produces changes in the functional connectivity of the brain. Resting-State fMRI is a useful tool for the study of functional changes in the human brain, and its metrics can be related to clinical findings involved in clinical decline. Social cognition has focused increasing interest because patients are exposed to experiencing social disorganization during the progression of the disease. fMRI has proved to be a useful tool for studying brain connectivity and its relation with social cognition both in resting-state and during socio-cognitive tasks.
      Objective. to identify functional changes during rest in Relapsing-Remitting Multiple Sclerosis patients and look for a correlation with social cognition.
      Methods. 45 patients with Relapsing-Remitting Multiple Sclerosis and 47 control subjects were recruited to perform a neuropsychological evaluation of the social cognition performance and to acquire resting-state fMRI.
      Results. Patients exhibited lower performance in social cognition tasks, mostly related to face emotion recognition. Decreased functional connectivity in patients is seen concerning the right anterior insula, middle frontal, and occipital regions while increased connectivity is mostly related to the occipital and visual areas. The connectivity of the fusiform cortex and the amygdala is related to the performance in emotion recognition and Theory of Mind tasks respectively.
      Conclusion. Social cognition compromise was found in this sample. Functional connectivity changes during rest were detected and correlated with social cognition changes in patients.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Multiple Sclerosis and Related Disorders
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Adolphs R.
        Is the human amygdala specialized for processing social information.
        Annals of the New York. 985. Academy of Sciences, 2006: 326-340
        • Audoin B.
        • Van Au Duong M.
        • Ranjeva J.-P.
        • Ibarrola D.
        • Malikova I.
        • Confort-Gouny S.
        • Soulier E.
        • Viout P.
        • Ali-Chérif A.
        • Pelletier J.
        • et al.
        Magnetic resonance study of the influence of tissue damage and cortical reorganization on PASAT performance at the earliest stage of Multiple Sclerosis.
        Hum. Brain Mapp. 2005; 24: 216-228
        • Benedict R.H.B.
        • Amato M.P.
        • Boringa J.
        • Brochet B.
        • Foley F.
        • Fredrikson S.
        • Hamalainen P.
        • Hartung H.
        • Krupp L.
        • Penner I.
        • et al.
        Brief International Cognitive Assessment for MS (BICAMS): international standards for validation.
        BMC Neurol. 2012; 12
        • Bisecco A.
        • Nardo F.D.
        • Docimo R.
        • Caiazzo G.
        • d'Ambrosio A.
        • Bonavita S.
        • Capuano R.
        • Sinisi L.
        • Cirillo M.
        • Esposito F.
        • et al.
        Fatigue in Multiple Sclerosis: The contribution of resting-state functional connectivity reorganization.
        Mult. Scler. 2018; 24: 1696-1705
        • Bisecco A.
        • Altieri M.
        • Santangelo G.
        • Di Nardo F.
        • Docimo R.
        • Caiazzo G.
        • Capuano R.
        • Pappacena S.
        • d'Ambrosio A.
        • Bonavita S.
        • et al.
        Resting-state functional correlates of social cognition in Multiple Sclerosis: an explorative study.
        Front. Behav. Neurosci. 2019; 13: 276
        • Bonzano L.
        • Pedullà L.
        • Pardini M.
        • Tacchino A.
        • Zaratin P.
        • Battaglia M.A.
        • Brichetto G.
        • Bove M.
        Brain activity pattern changes after adaptive working memory training in Multiple Sclerosis.
        Brain Imaging Behav. 2020; 14: 142-154
        • Castellazzi G.
        • Debernard L.
        • Melzer T.R.
        • Dalrymple-Alford J.C.
        • D'Angelo E.
        • Miller D.H.
        • Gandini Wheeler-Kingshott C.A.M.
        • Mason D.F.
        Functional connectivity alterations reveal complex mechanisms based on clinical and radiological status in mild relapsing remitting Multiple Sclerosis.
        Front. Neurol. 2018; 9: 690
        • Faivre A.
        • Robinet E.
        • Guye M.
        • Rousseau C.
        • Maarouf A.
        • Le Troter A.
        • Zaaraoui W.
        • Rico A.
        • Crespy L.
        • Soulier E.
        • et al.
        Depletion of brain functional connectivity enhancement leads to disability progression in Multiple Sclerosis: a longitudinal resting-state fMRI study.
        Mult. Scler. 2016; 22: 1695-1708
        • Fantoni-Quinton S.
        • Kwiatkowski A.
        • Vermersch P.
        • Roux B.
        • Hautecoeur P.
        • Leroyer A.
        Impact of Multiple Sclerosis on employment and use of job-retention strategies: the situation in France in 2015.
        J. Rehabil. Med. 2016; 48: 535-540
        • Frith C.D.
        The social brain?.
        Philos. Trans. R. Soc. B. 2007; 362: 671-678
        • Green R.
        • Adler A.
        • Banwell B.L.
        • Fabri T.L.
        • Yeh E.A.
        • Collins D.L.
        • Sled J.G.
        • Narayanan S.
        • Till C.
        Involvement of the amygdala in memory and psychosocial functioning in pediatric-onset Multiple Sclerosis.
        Dev. Neuropsychol. 2018; 43: 524-534
        • Jehna M.
        • Neuper C.
        • Petrovic K.
        • Wallner-Blazek M.
        • Schmidt R.
        • Fuchs S.
        • Fazekas F.
        • Enzinger C.
        An exploratory study on emotion recognition in patients with a clinically isolated syndrome and Multiple Sclerosis.
        Clin. Neurol. Neurosurg. 2010; 112: 482-484
        • Jehna M.
        • Langkammer C.
        • Wallner-Blazek M.
        • Neuper C.
        • Loitfelder M.
        • Ropele S.
        • Fuchs S.
        • Khalil M.
        • Pluta-Fuerst A.
        • Fazekas F.
        • et al.
        Cognitively preserved MS patients demonstrate functional differences in processing neutral and emotional faces.
        Brain Imaging Behav. 2011; 5: 241-251
        • Jimenez A.M.
        • Riedel P.
        • Lee J.
        • Reavis E.A.
        • Green M.F.
        Linking resting-state networks and social cognition in schizophrenia and bipolar disorder.
        Hum. Brain Mapp. 2019; 40: 4703-4715
        • Julian L.J.
        • Vella L.
        • Vollmer T.
        • Hadjimichael O.
        • Mohr D.C.
        Employment in Multiple Sclerosis. Exiting and re-entering the work force.
        J. Neurol. 2008; 255: 1354-1360
        • Krause M.
        • Wendt J.
        • Dressel A.
        • Berneiser J.
        • Kessler C.
        • Hamm A.O.
        • Lotze M.
        Prefrontal function associated with impaired emotion recognition in patients with Multiple Sclerosis.
        Behav. Brain Res. 2009; 205: 280-285
        • Lancaster K.
        • Venkatesan U.M.
        • Lengenfelder J.
        • Genova H.M.
        Default mode network connectivity predicts emotion recognition and social integration after traumatic brain injury.
        Front. Neurol. 2019; 10: 825
      1. Maxime-Louis Bertoux, M. (2014). Mini SEA: Évaluation de la démence fronto-temporale (De Boeck Supérieur).

        • Mike A.
        • Strammer E.
        • Aradi M.
        • Orsi G.
        • Perlaki G.
        • Hajnal A.
        • Sandor J.
        • Banati M.
        • Illes E.
        • Zaitsev A.
        • 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
        • Multani N.
        • Taghdiri F.
        • Anor C.J.
        • Varriano B.
        • Misquitta K.
        • Tang-Wai D.F.
        • Keren R.
        • Fox S.
        • Lang A.E.
        • Vijverman A.C.
        • et al.
        Association between social cognition changes and resting state functional connectivity in frontotemporal dementia, Alzheimer's Disease, Parkinson's Disease, and Healthy Controls.
        Front. Neurosci. 2019; 13
        • Nieto-Castañón A.
        • Fedorenko E.
        Subject-specific functional localizers increase sensitivity and functional resolution of multi-subject analyses.
        Neuroimage. 2012; 63: 1646-1669
        • Persechino B.
        • Fontana L.
        • Buresti G.
        • Fortuna G.
        • Valenti A.
        • Iavicoli S.
        Improving the job-retention strategies in Multiple Sclerosis workers: the role of occupational physicians.
        Ind. Health. 2019; 57: 52-69
        • Pitteri M.
        • Genova H.
        • Lengenfelder J.
        • DeLuca J.
        • Ziccardi S.
        • Rossi V.
        • Calabrese M.
        Social cognition deficits and the role of amygdala in relapsing remitting Multiple Sclerosis patients without cognitive impairment.
        Mult. Scler. Relat. Disord. 2019; 29: 118-123
        • Polman C.H.
        • Reingold S.C.
        • Edan G.
        • Filippi M.
        • Hartung H.-P.
        • Kappos L.
        • Lublin F.D.
        • Metz L.M.
        • McFarland H.F.
        • O'Connor P.W.
        • et al.
        Diagnostic criteria for Multiple Sclerosis: 2005 revisions to the “McDonald Criteria.
        Ann. Neurol. 2005; 58: 840-846
        • Schmidt P.
        • Gaser C.
        • Arsic M.
        • Buck D.
        • Förschler A.
        • Berthele A.
        • Hoshi M.
        • Ilg R.
        • Schmid V.J.
        • Zimmer C.
        • et al.
        An automated tool for detection of FLAIR-hyperintense white-matter lesions in Multiple Sclerosis.
        Neuroimage. 2012; 59: 3774-3783
        • Stern Y.
        Brain networks associated with cognitive reserve in healthy young and old adults.
        Cerebral Cortex. 2005; 15: 394-402
        • Tommasin S.
        • De Giglio L.
        • Ruggieri S.
        • Petsas N.
        • Giannì C.
        • Pozzilli C.
        • Pantano P.
        Relation between functional connectivity and disability in Multiple Sclerosis: a non-linear model.
        J. Neurol. 2018; 265: 2881-2892
        • Whitfield-Gabrieli S.
        • Fischer A.S.
        • Henricks A.M.
        • Khokhar J.Y.
        • Roth R.M.
        • Brunette M.F.
        • Green A.I.
        Understanding marijuana's effects on functional connectivity of the default mode network in patients with schizophrenia and co-occurring cannabis use disorder: a pilot investigation.
        Schizophr. Res. 2018; 194: 70-77
        • Yang D.Y.-J.
        • Rosenblau G.
        • Keifer C.
        • Pelphrey K.A.
        An integrative neural model of social perception, action observation, and Theory of Mind.
        Neurosci. Biobehav. Rev. 2015; 51: 263-275
        • Zhou F.
        • Zhuang Y.
        • Gong H.
        • Wang B.
        • Wang X.
        • Chen Q.
        • Wu L.
        • Wan H.
        Altered inter-subregion connectivity of the default mode network in relapsing remitting Multiple Sclerosis: a functional and structural connectivity study.
        PLoS ONE. 2014; 9e101198