Emotionserkennung, Theory of Mind und Empathie bei Multipler Sklerose

Zusammenfassung

Die Multiple Sklerose (MS), eine chronisch-entzündliche Erkrankung des zentralen Nervensystems, verursacht häufig körperliche Einschränkung, Affektstörungen, Fatigue und kognitive Störungen. Ein Teil der Letzten ist die soziale Kognition, die bei MS Patienten häufig beeinträchtigt ist. Sie umfasst die Theory of Mind, die Empathie und die soziale Wahrnehmung von Emotionen, die von Stimuli aus Gesichts-, Körper- und Stimmwahrnehmung geboten werden. Sozialkognitive Defizite verschlechtern die Affektdekodierung, die interpersonelle Kommunikation und die Lebensqualität. Trotz des Einflusses dieser Einschränkungen auf das Globalbefinden haben nur wenige Studien die Zusammenhänge und Überlappungen mit anderen MS Symptomen untersucht. Diese Übersichtsarbeit zielt auf die Definition und Anatomie sozialer Kognition ab und stellt die neuropsychologischen und bildgebenden Studien zur sozialen Kognition bei MS dar. Die Ergebnisse der verfügbaren Studien zeigen, dass sozialkognitive Defizite bereits in frühen Stadien der MS sichtbar sind. Über den Erkrankungsverlauf zeigen neuropsychologische und bildgebende Studien eine Zunahme der Krankheitsschwere und der Einschränkung der sozialen und nicht sozialen Kognition. Dies folgt der Hypothese eines Diskonnektionssyndroms bei zunehmender Zerstörung grauer und weißer Substanz. Diese strukturellen Läsionen übersteigen eine Schwelle an kompensatorischen und neuroplastischen Mechanismen und führen letztlich zum Auftreten der kognitiven Defizite. Angesichts der Belastung durch die Erkrankung ist eine weitere Untersuchung sozial-kognitiver Defizite bei MS dringend erforderlich, um Patienten spezifische therapeutische Ansätze zu bieten und die Lebensqualität zu verbessern.

Abstract

Multiple sclerosis (MS), a chronic progressive inflammatory disease of the central nervous system, causes frequent disability, mood disorders, fatigue, and cognitive dysfunction. As a part of the last, social cognition is frequently disturbed in MS patients. It comprises empathy and social perception of emotions from facial, bodily and vocal cues. Social cognitive deficits worsen affect decoding, interpersonal relationship, and quality of life. Despite the impact of these deficits on global functioning, only a small number of studies have investigated its correlations and overlaps with MS symptoms. This review focuses on the definition and anatomy of social cognition and draws attention to findings of neuropsychological and neuroimaging studies on social cognitive performance in MS.

Results of the available studies show that social cognitive deficits are already measurable in early stages of MS. Over time course of the disease, neuropsychological and neuroimaging studies show an increase of disease burden and social and non-social cognitive impairment following the hypothesis of a disconnection syndrome resulting from gray and white matters lesions. These structural changes might exceed a threshold of compensatory restorative and neuroplasticity mechanisms and finally lead to deficits in social cognition. Considering this burden in social functioning, a further assessment of sociocognitive deficits in MS is urgently needed to provide specific therapeutic approaches and to improve quality of life.

Schlüsselwörter

Emotion - Empathie - Multiple Sklerose - Prosodie - soziale Kognition - Theory of Mind

Key words

emotions - empathy - multiple sclerosis - prosody - social cognition - theory of mind

• Literatur

• 1 Compston A, Coles A. Multiple sclerosis. Lancet 2008; 372: 1502-1517
• 2 Gajofatto A, Benedetti MD. Treatment strategies for multiple sclerosis: When to start, when to change, when to stop?. World J Clin Cas 2015; 3: 545-555
• 3 Segal BM, Stüve O. Primary progressive multiple sclerosis – why we are failing. Lancet 2016; 387: 1032-1034
• 4 Rao SM, Leo GJ, Bernardin L. et al. Cognitive dysfunction in multiple sclerosis. I. Frequency, patterns, and prediction. Neurology 1991; 41: 685-691
• 5 Benedict RH, Cookfair D, Gavett R. et al. Validity of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). J Int Neuropsychol Soc 2009; 12: 549-558
• 6 Sanfilipo MP, Benedict RH, Weinstock-Guttman B. et al. Gray and white matter brain atrophy and neuropsychological impairment in multiple sclerosis. Neurology 2006; 66: 685-692
• 7 American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5. Aufl.. Washington: APA; 2013
• 8 Mohr DC, Cox D. Multiple sclerosis: empirical literature for the clinical health psychologist. J Clin Psychol 2001; 57: 479-499
• 9 Uekermann J, Channon S, Winkel K. et al. Theory of Mind, humour processing and executive functioning in alcoholism. Addiction 2007; 102: 232-240
• 10 Uekermann J, Daum I. Social cognition in alcoholism: A link to prefrontal cortex dysfunction?. Addiction 2008; 103: 726-735
• 11 Uekermann J, Kraemer M, Abdel-Hamid M. et al. Social cognition in attention-deficit hyperactivity disorder (ADHD). Neurosci Biobehav Rev 2010; 34: 734-743
• 12 Vistoli D, Brunet-Gouet E, Baup-Bobin E. et al. Anatomical and temporal architecture of Theory of Mind: A MEG insight into the early stages. Neuroimage 2011; 54: 1406-1414
• 13 Wolkenstein L, Schonenberg M, Schirm E. et al. I can see what you feel, but I can’t deal with it: Impaired Theory of Mind in depression. J Affect Disord 2011; 132: 104-111
• 14 Sebastian CL, Fontaine NM, Bird G. et al. Neural processing associated with cognitive and affective Theory of Mind in adolescents and adults. Soc Cogn Affect Neurosci 2012; 7: 53-63
• 15 Koelkebeck K, Abdel-Hamid M, Ohrmann P. et al. Theory of Mind in schizophrenia: Clinical aspects and empirical research. Fortschr Neurol Psychiatr 2008; 76: 573-582
• 16 Abdel-Hamid M, Lehmkämper C, Sonntag C. et al. Theory of mind in schizophrenia: the role of clinical symptomatology and neurocognition in understanding other people’s thoughts and intentions. Psychiatry Res 2009; 165: 19-26
• 17 Carr L, Iacoboni M, Dubeau MC. et al. Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proc Natl Acad Sci U S A 2003; 100: 5497-5502
• 18 Decety J, Jackson PL. The functional architecture of human empathy. Behav Cogn Neurosci Rev 2004; 3: 71-100
• 19 Leslie KR, Johnson-Frey SH, Grafton ST. Functional imaging of face and hand imitation: towards a motor theory of empathy. Neuroimage 2004; 21: 601-607
• 20 Seitz RJ, Nickel J, Azari NP. Functional modularity of the medial prefrontal cortex: involvement in human empathy. Neuropsychol 2006; 20: 743-751
• 21 Vollm BA, Taylor AN, Richardson P. et al. Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task. Neuroimage 2006; 29: 90-98
• 22 Ross ED, Thompson RD, Yenkosky J. Lateralization of affective prosody in brain and the callosal integration of hemispheric language functions. Brain Lang 1997; 56: 27-54
• 23 Wheaton KJ, Thompson JC, Syngeniotis A. et al. Viewing the motion of human body parts activates different regions of premotor, temporal, and parietal cortex. Neuroimage 2004; 22: 277-288
• 24 Calder AJ, Young AW. Understanding the recognition of facial identity and facial expression. Nat Rev Neurosci 2005; 6: 641-651
• 25 Ethofer T, Anders S, Erb M. et al. Cerebral pathways in processing of affective prosody: A dynamic causal modeling study. Neuroimage 2006; 30: 580-587
• 26 Uekermann J, Abdel-Hamid M, Lehmkamper C. et al. Perception of affective prosody in major depression: A link to executive functions?. J Int Neuropsychol Soc 2008; 14: 552-561
• 27 Heikkinen J, Jansson-Verkasalo E, Toivanen J. et al. Perception of basic emotions from speech prosody in adolescents with Asperger’s syndrome. Logoped Phoniat Vocol 2010; 35: 113-120
• 28 Montel SR, Bungener C. Coping and quality of life in one hundred and thirty-five subjects with multiple sclerosis. Mult Scler 2007; 13: 393-401
• 29 Rao SM, Leo GJ, Ellington L. et al. Cognitive dysfunction in multiple sclerosis. II. Impact on employment and social functioning. Neurology 1991; 41: 692-696
• 30 Kesselring J, Klement U. Cognitive and affective disturbances in multiple sclerosis. J Neurol 2001; 248: 180-183
• 31 Buhse M. Assessment of caregiver burden in families of persons with multiple sclerosis. J Neurosci Nurs 2008; 40: 25-31
• 32 Julian LJ, Vella L, Vollmer T. et al. Employment in multiple sclerosis. Exiting and reentering the work force. J Neurol 2008; 255: 1354-1360
• 33 Pfleger CC, Flachs EM, Koch-Henriksen N. Social consequences of multiple sclerosis. Part 2. Divorce and separation: a historical prospective cohort study. Mult Scler 2010; 16: 878-882
• 34 Langdon DW. Cognition in multiple sclerosis. Curr Opin Neurol 2011; 24: 244-249
• 35 Poder K, Ghatavi K, Fisk JD. et al. Social anxiety in a multiple sclerosis clinic population. Mult Scler 2009; 15: 393-398
• 36 Brothers L. The social brain: a project for integrating primate behavior and neurophysiology in a new domain. Concepts Neurosci 1990; 1: 27-51
• 37 Van Kleef GA. How emotions regulate social life. The Emotions as Social Information (EASI) model. Curr Dir Psychol Sci 2009; 18: 184-188
• 38 LaBar KS, Crupain MJ, Voyvodic JT. et al. Dynamic perception of facial affect and identity in the human brain. Cereb Cortex 2003; 13: 1023-1033
• 39 Palermo R, Rhodes G. Are you always on my mind? A review of how face perception and attention interact. Neuropsychologia 2007; 45: 75-92
• 40 Vuilleumier P, Pourtois G. Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia 2007; 45: 174-194
• 41 Kanwisher N, Yovel G. The fusiform face area: a cortical region specialized for the perception of faces. Philos Trans B Biol Sci 2006; 361: 2109-2128
• 42 Allison T, Puce A, McCarthy G. Social perception from visual cues: role of the STS region. Trends Cogn Sci 2000; 4: 267-278
• 43 Adolphs R. Neural systems for recognizing emotion. Curr Opin Neurobiol 2002; 12: 169-77
• 44 Krause M, Wendt J, Dressel A. et al. Prefrontal function associated with impaired emotion recognition in patients with multiple sclerosis. Behav Brain Res 2009; 205: 280-285
• 45 Tamietto M, de Gelder B. Neural bases of the non-conscious perception of emotional signals. Nat Rev Neurosci 2010; 11: 697-709
• 46 Critchley HD. Neural mechanisms of autonomic, affective, and cognitive integration. J Comp Neurol 2005; 493: 154-166
• 47 Wildgruber D, Ackermann H, Kreifelts B. et al. Cerebral processing of linguistic and emotional prosody: fMRI studies. Prog Brain Res 2006; 156: 249-268
• 48 Stone VE, Baron-Cohen S, Knight RT. Frontal lobe contribution to theory of mind. J Cogn Neurosci 1998; 10: 640-656
• 49 Uekermann J, Channon S, Lehmkamper C. et al. Executive function, mentalizing and humor in major depression. J Int Neuropsychol Soc 2008; 14: 55-62
• 50 Baron-Cohen S. Theory of mind and autism: a review. Int Rev Res Ment Retard 2000; 23: 169-184
• 51 Frith CD. Schizophrenia and theory of mind. Psychol Med 2004; 34: 385-389
• 52 Adolphs R, Baron-Cohen S, Tranel D. Impaired recognition of social emotions following amygdala damage. J Cogn Neurosci 2002; 14: 1264-1274
• 53 Kuperberg GR, Broome MR, McGuire PK. et al. Regionally localized thinning of the cerebral cortex in schizophrenia. Arch Gen Psychiatry 2003; 60: 878-888
• 54 Frith CD, Frith U. The neural basis of mentalizing. Neuron 2006; 50: 531-534
• 55 Herold R, Feldmann A, Simon M. et al. Regional gray matter reduction and theory of mind deficit in the early phase of schizophrenia: a voxel-based morphometric study. Acta Psychiatr Scand 2009; 119: 199-208
• 56 Schulte-Rüther M, Greimel E, Markowitsch HJ. et al. Dysfunctions in brain networks supporting empathy: an fMRI study in adults with autism spectrum disorders. Soc Neurosci 2011; 6: 1-21
• 57 Shamay-Tsoory SG, Aharon-Peretz J. Dissociable prefrontal networks for cognitive and affective theory of mind: a lesion study. Neuropsychologia 2007; 45: 3054-3067
• 58 Ruby P, Decety J. How would you feel versus how do you think she would feel? A neuroimaging study of perspective-taking with social emotions. J Cogn Neurosci 2004; 16: 988-999
• 59 Davis MH. Measuring individual differences in empathy: evidence for a multidimensional approach. J Pers Soc Psychol 1983; 44: 113-126
• 60 Tangney JP, Stuewig J, Mashek DJ. Moral emotions and moral behavior. Ann Rev Psychol 2007; 58: 345-372
• 61 Gallese V, Keysers C, Rizzolatti G. A unifying view of the basis of social cognition. Trends Cogn Sci 2004; 8: 396-403
• 62 Fan Y, Duncan NW, de Greck M. et al. Is there a core neural network in empathy? An fMRI based quantitative meta-analysis. Neurosci Biobehav Rev 2011; 35: 903-911
• 63 Vogeley K. Two social brains: neural mechanisms of intersubjectivity. Philos Trans R Soc Lond B Biol Sci 2017; 372 pii: 20160245. doi: 10.1098/rstb.2016.0245
• 64 Beatty WW, Goodkin DE, Weir WS. et al. Affective judgments by patients with Parkinson’s disease or chronic progressive multiple sclerosis. Bull Psychonom Soc 1989; 27: 361-364
• 65 Benton AL, Sivan AB, Hamsher K. et al. Contributions to neuropsychological assessment. New York: Oxford University Press; 1994
• 66 Ekman P, Friesen WV. Pictures of facial affect. Palo Alto: Consulting Psychologists Press; 1976
• 67 Parada-Fernández P, Oliva-Macias M, Amayra I. et al. Accuracy and reaction time in recognition of facial emotions in people with multiple sclerosis. Rev Neurol 2015; 61: 433-440
• 68 Kessler H, Bayerl P, Deighton R. et al. Facially Expressed Emotion Labeling (FEEL): PC-gestützer Test zur Emotionserkennung. Verhaltensther Verhaltensmed 2002; 23: 297-306
• 69 Berneiser J, Wendt J, Grothe M. et al. Impaired recognition of emotional facial expressions in patients with multiple sclerosis. Mult Scler Rel Disord 2014; 3: 482-488
• 70 Bowers D, Blonder LX, Heilman KM. The Florida Affect Battery. Gainsville: Center for Neuropsychological Studies; 1991
• 71 Bowers D, Blonder LX, Heilman KM. The Florida Affect Battery, manual (revised). Gainesville: Center for Neuropsychological Studies, University of Florida; 2011
• 72 Cecchetto C, Aiello M, D’Amico D. et al. Facial and bodily emotion recognition in multiple sclerosis: the role of alexithymia and other characteristics of the disease. J Int Neuropsychol Soc 2014; 20: 1004-1014
• 73 Phillips L, Henry J, Scott C. et al. Specific impairments of emotion perception in multiple sclerosis. Neuropsychol 2011; 25: 131-136
• 74 Sullivan S, Ruffman T. Social understanding: How does it fare with advancing years?. Br J Psychol 2004; 95: 1-18
• 75 Phillips LH, Saldias A, McCarrey A. et al. Attentional lapses, emotional regulation and quality of life in multiple sclerosis. Br J Clin Psychol 2009; 48: 101-106
• 76 Henry JD, Phillips LH, Beatty WW. et al. Evidence for deficits in facial affect recognition and Theory of Mind in multiple sclerosis. J Int Neuropsychol Soc 2009; 15: 277-285
• 77 Henry A, Tourbah A, Chaunu MP. et al. Social cognition impairments in relapsing remitting multiple sclerosis. J Int Neuropsychol Soc 2011; 17: 1122-1131
• 78 Prochnow D, Donell J, Schäfer R. et al. Alexithymia and impaired facial affect recognition in multiple sclerosis. J Neurol 2011; 258: 1683-1688
• 79 Skowronski JJ, Carlston DE. Negativity and extremity biases in impression formation: a review of explanations. Psychol Bull 1989; 105: 131-142
• 80 Di Bitonto L, Longato N, Jung B. et al. Reduced emotional reactivity to negative stimuli in multiple sclerosis, preliminary results. Rev Neurol 2011; 167: 820-826
• 81 Jehna M, Neuper C, Ischebeck A. et al. The functional correlates of face perception and recognition of emotional facial expressions as evidenced by fMRI. Brain Res 2011; 1393: 73-83
• 82 Habel U, Klein M, Kellermann T. et al. Same or different? Neural correlates of happy and sad mood in healthy males. Neuroimage 2006; 26: 206-214
• 83 Passamonti L, Cerasa A, Liguori M. et al. Neurobiological mechanisms underlying emotional processing in relapsing-remitting multiple sclerosis. Brain 2009; 132: 3380-3391
• 84 Jehna M, Neuper C, Petrovic K. et al. An exploratory study on emotion recognition in patients with a clinically isolated syndrome and multiple sclerosis. Clin Neurol Neurosurg 2010; 112: 482-484
• 85 Jehna M, Langkammer C, Wallner-Blazek M. et al. Cognitively preserved MS patients demonstrate functional differences in processing neutral and emotional faces. Brain Imaging Behav 2011; 5: 241-251
• 86 Pinto C, Gomes F, Moreira I. et al. Emotion recognition in multiple sclerosis. J Eye Track Vis Cogn Emot 2012; 2: 76-81
• 87 Vázquez-Marrufo M, Galvao-Carmona A, González-Rosa JJ. et al. Neural correlates of alerting and orienting impairment in multiple sclerosis patients. PLoS One 2014; 12 e97226
• 88 Knight M, Mather M. Look out-it’s your off-peak time of day! Time of day matters more for alerting than for orienting or executive attention. Exp Aging Res 2013; 39: 305-321
• 89 Ayache SS, Chalah MA, Kümpfel T. et al. Fatigue bei Multipler Sklerose: Neuronale Korrelate und Möglichkeiten nicht-invasiver Hirnstimulation mit tDCS. Fortschr Neurol Psychiatr 2017; 85: 260-269
• 90 Leppanen JM. Emotional information processing in mood disorders: a review of behavioral and neuroimaging findings. Curr Opin Psychiatry 2006; 19: 34-39
• 91 Grynberg D, Chang B, Corneille O. et al. Alexithymia and the processing of emotional facial expressions (EFEs): systematic review, unanswered questions and further perspectives. PloS One 2012; 7 e42429
• 92 Franz M, Popp K, Schaefer R. et al. Alexithymia in the German general population. Soc Psychiatry Psychiatr Epidemiol 2008; 43: 54-62
• 93 Beatty WW, Orbelo DM, Sorocco KH. et al. Comprehension of affective prosody in multiple sclerosis. Mult Scler 2003; 9: 148-153
• 94 Kraemer M, Herold M, Uekermann J. et al. Perception of affective prosody in patients at an early stage of relapsing-remitting multiple sclerosis. J Neuropsychol 2013; 7: 91-106
• 95 Baron-Cohen S, Jolliffe T, Mortimore C. et al. A further 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
• 96 Baron-Cohen S, Wheelwright S, Hill J. 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
• 97 Baron-Cohen S, O’Riordan M, Stone V. et al. Recognition of faux pas by normally developing children and children with Asperger syndrome or high-functioning autism. J Autism Dev Disord 1999; 29: 407-418
• 98 Banati M, Sandor J, Mike A. et al. Social cognition and Theory of Mind in patients with relapsing-remitting multiple sclerosis. Eur J Neurol 2010; 17: 426-433
• 99 Mike A, Strammer E, Aradi M. 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
• 100 Roca M, Manes F, Gleichgerrcht E. et al. Cognitive but not affective theory of mind deficits in mild relapsing-remitting multiple sclerosis. Cogn Behav Neurol 2014; 27: 25-30
• 101 Ouellet J, Scherzer PB, Rouleau I. et al. Assessment of social cognition in patients with multiple sclerosis. J Int Neuropsychol Soc 2010; 16: 287-296
• 102 Happé FG, Winner E, Brownell H. The getting of wisdom: Theory of mind in old age. Dev Psychol 1998; 34: 358-362
• 103 Kuzmanovic B, Bente G, von Cramon DY. et al. Imaging first impressions: distinct neural processing of verbal and nonverbal social information. Neuroimage 2012; 60: 179-188
• 104 Pöttgen J, Dziobek I, Reh S. et al. Impaired social cognition in multiple sclerosis. J Neurol Neurosurg Psychiatry 2013; 84: 523-528
• 105 Kraemer M, Herold M, Uekermann J. et al. Theory of mind and empathy in patients at an early stage of relapsing remitting multiple sclerosis. Clin Neurol Neurosurg 2013; 115: 1016-1022
• 106 Genova HM, Cagna CJ, Chiaravalloti ND. et al. Dynamic Assessment of Social Cognition in Individuals with Multiple Sclerosis: A Pilot Study. J Int Neuropsychol Soc 2016; 22: 83-88
• 107 Charvet LE, Cleary RE, Vazquez K. et al. Social cognition in pediatric-onset multiple sclerosis (MS). Mult Scler 2014; 20: 1478-1484
• 108 Gleichgerrcht E, Tomashitis B, Sinay V. The relationship between alexithymia, empathy and moral judgment in patients with multiple sclerosis. Eur J Neurol 2015; 22: 1295-1303
• 109 Bird G, Silani G, Brindley R. et al. Empathic brain responses in insula are modulated by levels of alexithymia but not autism. Brain 2010; 133: 1515-1525
• 110 Benedict RH, Priore RL, Miller C. et al. Personality disorder in multiple sclerosis correlates with cognitive impairment. J Neuropsychiatry Clin Neurosci 2001; 13: 70-76
• 111 Pakenham KI, Cox S. The dimensional structure of benefit finding in multiple sclerosis and relations with positive and negative adjustment: a longitudinal study. Psychol Health 2009; 24: 373-393
• 112 Cavada C, Company T, Tejedor J. et al. The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb Cort 2000; 10: 220-242
• 113 Park HJ, Kim JJ, Lee SK. et al. Corpus callosal connection mapping using cortical gray matter parcellation and DT-MRI. Hum Brain Mapp 2008; 29: 503-516
• 114 Haxby JV, Hoffman EA, Gobbini MI. The distributed human neural system for face perception. Trends Cogn Sci 2000; 4: 223-233
• 115 Haxby JV, Hoffman EA, Gobbini MI. Human neural systems for face recognition and social communication. Biol Psychiatry 2002; 51: 59-67
• 116 Zaki J, Hennigan K, Weber J. et al. Social cognitive conflict resolution: contributions of domain-general and domain-specific neural systems. J Neurosci 2010; 30: 8481-8488
• 117 Rovaris M, Comi G, Filippi M. The role of non-conventional MR techniques to study multiple sclerosis patients. J Neurol Sci 2001; 186: S3-S9
• 118 Baas D, Aleman A, Kahn RS. Lateralization of amygdala activation: a systematic review of functional neuroimaging studies. Brain Res Rev 2004; 45: 96-103
• 119 Ghashghaei HT, Hilgetag CC, Barbas H. Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 2007; 34: 905-23
• 120 Maddock RJ, Garrett AS, Buonocore MH. Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task. Hum Brain Mapp 2003; 18: 30-41
• 121 Cavanna AE, Trimble MR. The precuneus: a review of its functional anatomy and behavioural correlates. Brain 2006; 129: 564-583
• 122 Pantano P, Iannetti GD, Caramia F. et al. Cortical motor reorganization after a single clinical attack of multiple sclerosis. Brain 2002; 125: 1607-1615
• 123 Mainero C, Caramia F, Pozzilli C. et al. fMRI evidence of brain reorganization during attention and memory tasks in multiple sclerosis. Neuroimage 2004; 21: 858-867
• 124 Mainero C, Pantano P, Caramia F. et al. Brain reorganization during attention and memory tasks in multiple sclerosis: insights from functional MRI studies. J Neurol Sci 2006; 245: 93-98
• 125 Sweet LH, Rao SM, Primeau M. et al. Functional magnetic resonance imaging response to increased verbal working memory demands among patients with multiple sclerosis. Hum Brain Mapp 2006; 27: 28-36
• 126 Wegner C, Filippi M, Korteweg T. et al. Relating functional changes during hand movement to clinical parameters in patients with multiple sclerosis in a multi-centre fMRI study. Eur J Neurol 2008; 15: 113-122
• 127 Rocca MA, Absinta M, Ghezzi A. et al. Is a preserved functional reserve a mechanism limiting clinical impairment in pediatric MS patients?. Hum Brain Mapp 2009; 30: 2844-2851
• 128 Sumowski JF, Wylie GR, Deluca J. et al. Intellectual enrichment is linked to cerebral efficiency in multiple sclerosis: functional magnetic resonance imaging evidence for cognitive reserve. Brain 2009; 133: 362-374
• 129 Morgen K, Kadom N, Sawaki L. et al. Training-dependent plasticity in patients with multiple sclerosis. Brain 2004; 127: 2506-2517
• 130 Citri A, Malenka RC. Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacol 2008; 33: 18-41
• 131 Bodini B, Mandarelli G, Tomassini V. et al. Alexithymia in multiple sclerosis: Relationship with fatigue and depression. Acta Neurol Scand 2008; 118: 18-23
• 132 Chahraoui K, Duchene C, Rollot F. et al. Longitudinal study of alexithymia and multiple sclerosis. Brain Behav 2014; 4: 75-82
• 133 Chahraoui K, Pinoit JM, Viegas N. et al. Alexithymie et liens avec la dépression et l’anxiété dans la sclérose en plaques. Rev Neurol 2008; 164: 242-245
• 134 Gay MC, Vrignaud P, Garitte C. et al. Predictors of depression in multiple sclerosis patients. Acta Neurol Scand 2010; 121: 161-170
• 135 Kano M, Fukudo S, Gyoba J. et al. Specific brain processing of facial expressions in people with alexithymia: an H2 15O-PET study. Brain 2003; 126: 1474-1484
• 136 Ihme K, Dannlowski U, Lichev V. et al. Alexithymia is related to differences in gray matter volume: a voxelbased morphometry study. Brain Res 2013; 1491: 60-67
• 137 Feinstein A. Multiple sclerosis and depression. Mult Scler 2011; 17: 1276-1281
• 138 Gobbi C, Rocca MA, Riccitelli G. et al. Influence of the topography of brain damage on depression and fatigue in patients with multiple sclerosis. Mult Scler 2014; 20: 192-201
• 139 Persad SM, Polivy J. Differences between depressed and nondepressed individuals in the recognition of and response to facial emotional cues. J Abnorm Psychol 1993; 102: 358-368
• 140 Asthana HS, Mandal MK, Khurana H. et al. Visuospatial and affect recognition deficit in depression. J Affect Disord 1998; 48: 57-62
• 141 Suslow T, Dannlowski U, Lalee-Mentzel J. et al. Spatial processing of facial emotion in patients with unipolar depression: a longitudinal study. J Affect Disord 2004; 83: 59-63
• 142 Gobbi C, Rocca MA, Pagani E. et al. Forceps minor damage and co-occurrence of depression and fatigue in multiple sclerosis. Mult Scler 2014; 20: 1633-1640
• 143 Bisecco A, Caiazzo G, d’Ambrosio A. et al. Fatigue in multiple sclerosis: The contribution of occult white matter damage. Mult Scler. pii: 1352458516628331
• 144 Ayache SS, Palm U, Chalah MA. et al. Orienting network dysfunction in progressive multiple sclerosis. J Neurol Sci 2015; 351: 206-207
• 145 Samson D, Apperly IA, Chiavarino C. et al. Left temporoparietal junction is necessary for representing someone else’s belief. Nat Neurosci 2004; 7: 499-500
• 146 Young L, Camprodon JA, Hauser M. et al. Disruption of the right temporoparietal junction with transcranial magnetic stimulation reduces the role of beliefs in moral judgments. Proc Natl Acad Sci U S A 2010; 107: 6753-6758
• 147 Beattie L, Kyle SD, Espie CA. et al. Social interactions, emotion and sleep: A systematic review and research agenda. Sleep Med Rev 2015; 24: 83-100
• 148 Pantano P, Mainero C, Lenzi D. et al. A longitudinal fMRI study on motor activity in patients with multiple sclerosis. Brain 2005; 128: 2146-2153
• 149 Cader S, Cifelli A, Abu-Omar Y. et al. Reduced brain functional reserve and altered functional connectivity in patients with multiple sclerosis. Brain 2006; 129: 527-537
• 150 Stern Y. Cognitive reserve in ageing and Alzheimer’s disease. Lancet Neurol 2012; 11: 1006-1012
• 151 Sumowski JF, Leavitt VM. Cognitive reserve in multiple sclerosis. Mult Scler 2013; 19: 1122-1127
• 152 Dziobek I, Fleck S, Kalbe E. et al. Introducing MASC: A movie for the assessment of social cognition. J Autism Dev Disord 2006; 36: 623-636