Impaired Self-Other Distinction and Subcortical Gray-Matter Alterations Characterize Socio-Cognitive Disturbances in Multiple Sclerosis
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection
Document type Journal Article
PubMed
31164860
PubMed Central
PMC6536606
DOI
10.3389/fneur.2019.00525
Knihovny.cz E-resources
- Keywords
- automatic imitation, gray-matter volume, multiple sclerosis, self-other distinction, social cognition, visual perspective taking, voxel-based morphometry,
- Publication type
- Journal Article MeSH
Introduction: Recent studies of patients with multiple sclerosis (MS) have revealed disturbances in distinct components of social cognition, such as impaired mentalizing and empathy. The present study investigated this socio-cognitive profile in MS patients in more detail, by examining their performance on tasks measuring more fundamental components of social cognition and any associated disruptions to gray-matter volume (GMV). Methods: We compared 43 patients with relapse-remitting MS with 43 age- and sex-matched healthy controls (HCs) on clinical characteristics (depression, fatigue), cognitive processing speed, and three aspects of low-level social cognition; specifically, imitative tendencies, visual perspective taking, and emotion recognition. Using voxel-based morphometry, we then explored relationships between GMV and these clinical and behavioral measures. Results: Patients exhibited significantly slower processing speed, poorer perspective taking, and less imitation compared with HCs. These impairments were related to reduced GMV throughout the putamen, thalami, and anterior insula, predominantly in the left hemisphere. Surprisingly, differences between the groups in emotion recognition were not significant. Conclusion: Less imitation and poorer perspective taking indicate a cognitive self-bias when faced with conflicting self- and other-representations. This suggests that impaired self-other distinction, and an associated subcortical pattern of GM atrophy, might underlie the socio-cognitive disturbances observed in MS.
Department of Imaging Methods Masaryk University and St Anne's University Hospital Brno Czechia
Institute of Psychology Czech Academy of Sciences Brno Czechia
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Chiaravalloti ND, DeLuca J. Cognitive impairment in multiple sclerosis. Lancet Neurol. (2008) 7:1139–51. 10.1016/S1474-4422(08)70259-X PubMed DOI
Sumowski JF, Benedict R, Enzinger C, Filippi M, Geurts JJ, Hamalainen P, et al. . Cognition in multiple sclerosis: state of the field and priorities for the future. Neurology. (2018) 90:278–88. 10.1212/WNL.0000000000004977 PubMed DOI PMC
Bora E, Özakbaş S, Velakoulis D, Walterfang M. Social cognition in multiple sclerosis: a meta-analysis. Neuropsychol Rev. (2016) 26:160–72. 10.1007/s11065-016-9320-6 PubMed DOI
Happé F, Cook JL, Bird G. The structure of social cognition: in(ter)dependence of sociocognitive processes. Ann Rev Psychol. (2017) 68:243–67. 10.1146/annurev-psych-010416-044046 PubMed DOI
Frith CD, Frith U. Mechanisms of social cognition. Ann Rev Psychol. (2012) 63:287–313. 10.1146/annurev-psych-120710-100449 PubMed DOI
Henry JD, Von Hippel W, Molenberghs P, Lee T, Sachdev PS. Clinical assessment of social cognitive function in neurological disorders. Nat Rev Neurol. (2016) 12:28–39. 10.1038/nrneurol.2015.229 PubMed DOI
Cotter J, Firth J, Enzinger C, Elliott R, Drake RJ. Social cognition in multiple sclerosis A systematic review and meta-analysis. Neurology. (2016) 87:1727–36. 10.1212/WNL.0000000000003236 PubMed DOI PMC
Neuhaus M, Bagutti S, Yaldizli Ö, Zwahlen D, Schaub S, Frey B, et al. . Characterization of social cognition impairment in multiple sclerosis. Eur J Neurol. (2018) 25:90–6. 10.1111/ene.13457 PubMed DOI
Raimo S, Trojano L, Pappacena S, Alaia R, Spitaleri D, Grossi D, et al. . Neuropsychological correlates of theory of mind deficits in patients with multiple sclerosis. Neuropsychology. (2017) 31:811–21. 10.1037/neu0000372 PubMed DOI
Isernia S, Baglio F, D'Arma A, Groppo E, Marchetti A, Massaro D. Social mind and long-lasting disease: focus on affective and cognitive theory of mind in multiple sclerosis. Front Psychol. (2019) 10:218. 10.3389/fpsyg.2019.00218 PubMed DOI PMC
Roca M, Manes F, Gleichgerrcht E, Ibáñez A, González De Toledo ME, Marenco V, et al. . Cognitive but not affective theory of mind deficits in mild relapsing-remitting multiple sclerosis. Cogn Behav Neurol. (2014) 27:25–30. 10.1097/WNN.0000000000000017 PubMed DOI
Schurz M, Aichhorn M, Martin A, Perner J. Common brain areas engaged in false belief reasoning and visual perspective taking: a meta-analysis of functional brain imaging studies. Front Hum Neurosci. (2013) 7:1–14. 10.3389/fnhum.2013.00712 PubMed DOI PMC
Fan Y, Duncan NW, de Greck M, Northoff G. Is there a core neural network in empathy? An fMRI based quantitative meta-analysis. Neurosci Biobehav Rev. (2011) 35:903–11. 10.1016/j.neubiorev.2010.10.009 PubMed DOI
Fusar-Poli P, Placentino A, Carletti F, Landi P, Allen P, Surguladze S, et al. . Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci. (2009) 34:418–32. PubMed PMC
Lamm C, Bukowski H, Silani G. From shared to distinct self–other representations in empathy: evidence from neurotypical function and socio-cognitive disorders. Philos Transac R Soc B Biol Sci. (2016) 371:20150083. 10.1098/rstb.2015.0083 PubMed DOI PMC
Shaw DJ, Czekóová K, Pennington CR, Qureshi AW, Špiláková B, Salazar M, et al. You ≠ Me: individual differences in the structure of social cognition. Psychol Res. (2018). 10.1007/s00426-018-1107-3 PubMed DOI PMC
Steinbeis N. The role of self–other distinction in understanding others' mental and emotional states: neurocognitive mechanisms in children and adults. Philos Transac R Soc B Biol Sci. (2016) 371:20150074 10.1098/rstb.2015.0074 PubMed DOI PMC
Silani G, Lamm C, Ruff CC, Singer T. Right supramarginal gyrus is crucial to overcome emotional egocentricity bias in social judgments. J Neurosci. (2013) 33:15466–76. 10.1523/JNEUROSCI.1488-13.2013 PubMed DOI PMC
Epley N, Keysar B, Van Boven L, Gilovich T. Perspective taking as egocentric anchoring and adjustment. J Pers Soc Psychol. (2004) 87:327–39. 10.1037/0022-3514.87.3.327 PubMed DOI
Chartrand TL, Lakin JL. The antecedents and consequences of human behavioral mimicry. Ann Rev Psychol. (2013) 64:285–308. 10.1146/annurev-psych-113011-143754 PubMed DOI
Catmur C, Walsh V, Heyes C. Associative sequence learning: the role of experience in the development of imitation and the mirror system. Philos Transac R Soc B Biol Sci. (2009) 364:2369–80. 10.1098/rstb.2009.0048 PubMed DOI PMC
de Guzman M, Bird G, Banissy MJ, Catmur C. Self–other control processes in social cognition: from imitation to empathy. Philos Transac R Soc B Biol Sci. (2016) 371:20150079. 10.1098/rstb.2015.0079 PubMed DOI PMC
Santiesteban I, Banissy MJ, Catmur C, Bird G. Enhancing social ability by stimulating right temporoparietal junction. Curr Biol. (2012) 22:2274–7. 10.1016/j.cub.2012.10.018 PubMed DOI
Shaw DJ, Czekóová K, Porubanová M. Orthogonal-compatibility effects confound automatic imitation: implications for measuring self–other distinction. Psychol Res. (2017) 81:1152–65. 10.1007/s00426-016-0814-x PubMed DOI
Batista S, D'Almeida O, Afonso A, Freitas S, Macário C, Sousa L, et al. . Impairment of social cognition in multiple sclerosis: amygdala atrophy is the main predictor. Mult Scler. (2017a) 23:1358–66. 10.1177/1352458516680750 PubMed DOI
Audoin B, Zaaraoui W, Reuter F, Rico A, Malikova I, Confort-Gouny S, et al. . Atrophy mainly affects the limbic system and the deep grey matter at the first stage of multiple sclerosis. J Neurol Neurosurg Psychiatry. (2010) 81:690–5. 10.1136/jnnp.2009.188748 PubMed DOI
Eshaghi A, Prados F, Brownlee W, Altmann DR, Tur C, Cardoso MJ. Deep grey matter volume loss drives disability worsening in multiple sclerosis. Ann Neurol. (2017) 83:210–22. 10.1002/ana.25145 PubMed DOI PMC
Datta S, Staewen TD, Cofield SS, Cutter GR, Lublin FD, Wolinsky JS, et al. . Regional gray matter atrophy in relapsing remitting multiple sclerosis: Baseline analysis of multi-center data. Mult Scler Relat Disord. (2015) 4:124–36. 10.1016/j.msard.2015.01.004 PubMed DOI PMC
Abu-Akel A, Shamay-Tsoory S. Neuroanatomical and neurochemical bases of theory of mind. Neuropsychologia. (2011) 49:2971–84. 10.1016/j.neuropsychologia.2011.07.012 PubMed DOI
Poletti M, Enrici I, Adenzato M. Cognitive and affective theory of mind in neurodegenerative diseases: neuropsychological, neuroanatomical and neurochemical levels. Neurosci Biobehav Rev. (2012) 36:2147–64. 10.1016/j.neubiorev.2012.07.004 PubMed DOI
Kraemer M, Herold M, Uekermann J, Kis B, Wiltfang J, Daum I, et al. . Theory of mind and empathy in patients at an early stage of relapsing remitting multiple sclerosis. Clin Neurol Neurosurg. (2013) 115:1016–22. 10.1016/j.clineuro.2012.10.027 PubMed DOI
Batista S, Dineen R, Vilisaar J, Hlinka J, Bradshaw C, Morgan P, et al. Disconnection as a mechanism for cognitive dysfunction in multiple sclerosis. Neurology. (2017b) 89:38–45. 10.1212/WNL.0000000000004060 PubMed DOI
Chalah MA, Kauv P, Lefaucheur JP, Hodel J, Créange A, Ayache SS. Theory of mind in multiple sclerosis: a neuropsychological and MRI study. Neurosci Lett. (2017) 658:108–13. 10.1016/j.neulet.2017.08.055 PubMed DOI
Milenkovic S, Dragovic M. Modification of the Edinburgh Handedness inventory: a replication study. Laterality. (2013) 18:340–8. 10.1080/1357650X.2012.683196 PubMed DOI
Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. (1983) 33:1444. 10.1212/WNL.33.11.1444 PubMed DOI
Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, et al. . Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald criteria. Ann Neurol. (2011) 69:292–302. 10.1002/ana.22366 PubMed DOI PMC
Winkler AM, Ridgway GR, Webster MA, Smith SM, Nichols TE. Permutation inference for the general linear model. NeuroImage. (2014) 92:381–97. 10.1016/j.neuroimage.2014.01.060 PubMed DOI PMC
Benedict RHB, DeLuca J, Phillips G, LaRocca N, Hudson LD, Rudick R, et al. . Validity of the Symbol Digit Modalities Test as a cognition performance outcome measure for multiple sclerosis. Mult Scler J. (2017) 23:721–33. 10.1177/1352458517690821 PubMed DOI PMC
Langdon D, Amato M, Boringa I, Brochet B, Foley F, Fredrikson S, et al. . Recommendations for a Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS). Mult Scler J. (2012) 18:891–8. 10.1177/1352458511431076 PubMed DOI PMC
Brass M, Bekkering H, Wohlschläger A, Prinz W. Compatibility between observed and executed finger movements: comparing symbolic, spatial, and imitative cues. Brain Cogn. (2000) 44:124–43. 10.1006/brcg.2000.1225 PubMed DOI
Genschow O, Van Den Bossche S, Cracco E, Bardi L, Rigoni D, Brass M. Mimicry and automatic imitation are not correlated. PLoS ONE. (2017) 12:1–21. 10.1371/journal.pone.0183784 PubMed DOI PMC
Keysar B, Barr DJ, Balin JA, Brauner JS. Taking perspective in conversation: the role of mutual knowledge in comprehension. Psychol Sci. (2000) 11:32–8. 10.1111/1467-9280.00211 PubMed DOI
Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I. 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 Psychiat Assoc Child Psychol Psychiatry. (2001) 42:241–51. 10.1111/1469-7610.00715 PubMed DOI
Oakley BFM, Brewer R, Bird G, Catmur C. Theory of mind is not theory of emotion. J Abnorm Psychol. (2016) 125:1–25. 10.1037/abn0000182 PubMed DOI PMC
Beck AT, Steer RA, Brown GK. Beck Depression Inventory-II: Manual. San Antonio, TX: Psychological Corporation; (1996).
Sacco R, Santangelo G, Stamenova S, Bisecco A, Bonavita S, Lavorgna L, et al. . Psychometric properties and validity of Beck Depression Inventory II in multiple sclerosis. Eur J Neurol. (2016) 23:744–50. 10.1111/ene.12932 PubMed DOI
Kos D, Kerckhofs E, Carrea I, Verza R, Ramos M, Jansa J. Evaluation of the modified fatigue impact scale in four different European countries. Mult Scler J. (2005) 11:76–80. 10.1191/1352458505ms1117oa PubMed DOI
Good CD, Scahill RI, Fox NC, Ashburner J, Friston KJ, Chan D, et al. . Automatic differentiation of anatomical patterns in the human brain: validation with studies of degenerative dementias. NeuroImage. (2002) 17:29–46. 10.1006/nimg.2002.1202 PubMed DOI
Douaud G, Smith S, Jenkinson M, Behrens T, Johansen-Berg H, Vickers J, et al. . Anatomically related grey and white matter abnormalities in adolescent-onset schizophrenia. Brain. (2007) 130:2375–86. 10.1093/brain/awm184 PubMed DOI
Zhang Y, Brady M, Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Transac Med Imaging. (2001) 20:45–57. 10.1109/42.906424 PubMed DOI
Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage. (2002) 17:825–41. 10.1006/nimg.2002.1132 PubMed DOI
Andersson JLR, Jenkinson M, Smith S. Non-linear registration, aka spatial normalisation. In: FMRIB Technial Report TR07JA2. Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, Department of Clinical Neurology, Oxford University, Oxford (2007).
Good CD, Johnsrude IS, Ashburner J, Henson RNA, Friston KJ, Frackowiak RSJ. A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage. (2001) 14:21–36. 10.1006/nimg.2001.0786 PubMed DOI
Smith SM, Nichols TE. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage. (2009) 44:83–98. 10.1016/j.neuroimage.2008.03.061 PubMed DOI
Bukowski H, Samson D. New insights into the inter-individual variability in perspective taking. Vision. (2017) 1:8 10.3390/vision1010008 PubMed DOI PMC
Bird G, Viding E. The self to other model of empathy: Providing a new framework for understanding empathy impairments in psychopathy, autism, and alexithymia. Neurosci Biobehav Rev. (2014) 47:520–32. 10.1016/j.neubiorev.2014.09.021 PubMed DOI
Banati M, Sandor J, Mike A, Illes E, Bors L, Feldmann A, et al. . Social cognition and Theory of Mind in patients with relapsing-remitting multiple sclerosis. Eur J Neurol. (2010) 17:426–33. 10.1111/j.1468-1331.2009.02836.x PubMed DOI
Zhang R, Geng X, Lee TMC. Large-scale functional neural network correlates of response inhibition: an fMRI meta-analysis. Brain Struct Function. (2017) 222:3973–90. 10.1007/s00429-017-1443-x PubMed DOI PMC
Batista S, Freitas S, Afonso A, Macário C, Sousa L, Cunha L, et al. . Theory of mind and executive functions are dissociated in multiple sclerosis. Arch Clin Neuropsychol. (2018) 33:541–51. 10.1093/arclin/acx101 PubMed DOI
Di Filippo M, Portaccio E, Mancini A, Calabresi P. Multiple sclerosis and cognition: synaptic failure and network dysfunction. Nat Rev Neurosci. (2018) 19:599–609. 10.1038/s41583-018-0053-9 PubMed DOI
Báez-Mendoza R, Schultz W. The role of the striatum in social behavior. Front Neurosci. (2013) 7:233. 10.3389/fnins.2013.00233 PubMed DOI PMC
Hwang K, Bertolero MA, Liu WB, D'Esposito M. The human thalamus is an integrative hub for functional brain networks. J Neurosci. (2017) 37:5594–607. 10.1523/JNEUROSCI.0067-17.2017 PubMed DOI PMC
Saalmann YB, Kastner S. The cognitive thalamus. Front Syst Neurosci. (2015) 9:39. 10.3389/fnsys.2015.00039 PubMed DOI PMC
Uddin LQ, Nomi JS, Hébert-Seropian B, Ghaziri J, Boucher O. Structure and function of the human insula. J Clini Neurophysiol. (2017) 34:300–6. 10.1097/WNP.0000000000000377 PubMed DOI PMC
Mike A, Strammer E, Aradi M, Orsi G, Perlaki G, Hajnal 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. 10.1371/journal.pone.0082422 PubMed DOI PMC
Barbey AK, Colom R, Grafman J. Architecture of cognitive flexibility revealed by lesion mapping. NeuroImage. (2013) 82:547–54. 10.1016/j.neuroimage.2013.05.087 PubMed DOI PMC
Uddin LQ, Iacoboni M, Lange C, Keenan JP. The self and social cognition: the role of cortical midline structures and mirror neurons. Trends Cogn Sci. (2007) 11:153–7. 10.1016/j.tics.2007.01.001 PubMed DOI
Geurts JJG, Calabrese M, Fisher E, Rudick RA. Measurement and clinical effect of grey matter pathology in multiple sclerosis. Lancet Neurol. (2012) 11:1082–92. 10.1016/S1474-4422(12)70230-2 PubMed DOI
Plata-Bello J, Pérez-Martín Y, Castañón-Pérez A, Modroño C, Fariña H, Hernández-Martín E, et al. . The mirror neuron system in relapsing remitting multiple sclerosis patients with low disability. Brain Topogr. (2017) 30:548–59. 10.1007/s10548-017-0558-y PubMed DOI
Modica CM, Bergsland N, Dwyer MG, Ramasamy DP, Carl E, Zivadinov R, et al. . Cognitive reserve moderates the impact of subcortical gray matter atrophy on neuropsychological status in multiple sclerosis. Mult Scler. (2016) 22:36–42. 10.1177/1352458515579443 PubMed DOI
Schmidt P, Gaser C, Arsic M, Buck D, Förschler A, Berthele A, et al. . An automated tool for detection of FLAIR-hyperintense white-matter lesions in multiple sclerosis. NeuroImage. (2012) 59:3774–83. 10.1016/j.neuroimage.2011.11.032 PubMed DOI