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Facial and Bodily Emotion Recognition in Multiple Sclerosis: The Role of Alexithymia and Other Characteristics of the Disease

Published online by Cambridge University Press:  06 November 2014

Cinzia Cecchetto ,
Marilena Aiello ,
Delia D’Amico ,
Daniela Cutuli ,
Daniela Cargnelutti ,
Roberto Eleopra  and
Raffaella Ida Rumiati
Cinzia Cecchetto*
Affiliation:
Cognitive Neuroscience Sector, SISSA, Trieste, Italy, Udine, Italy
Marilena Aiello
Affiliation:
Cognitive Neuroscience Sector, SISSA, Trieste, Italy, Udine, Italy
Delia D’Amico
Affiliation:
S.O.C. Neurologia, Azienda Ospedaliero Universitaria “Santa Maria della Misericordia”
Daniela Cutuli
Affiliation:
S.O.C. Neurologia, Azienda Ospedaliero Universitaria “Santa Maria della Misericordia”
Daniela Cargnelutti
Affiliation:
S.O.C. Neurologia, Azienda Ospedaliero Universitaria “Santa Maria della Misericordia”
Roberto Eleopra
Affiliation:
S.O.C. Neurologia, Azienda Ospedaliero Universitaria “Santa Maria della Misericordia”
Raffaella Ida Rumiati
Affiliation:
Cognitive Neuroscience Sector, SISSA, Trieste, Italy, Udine, Italy
*
Correspondence and reprint requests to: Cinzia Cecchetto, Neuroscience and Society Lab, SISSA - International School for Advanced Studies, via Bonomea 265, 34100 Trieste Italy. E-mail: ccecchet@sissa.it
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Abstract

Multiple sclerosis (MS) may be associated with impaired perception of facial emotions. However, emotion recognition mediated by bodily postures has never been examined in these patients. Moreover, several studies have suggested a relation between emotion recognition impairments and alexithymia. This is in line with the idea that the ability to recognize emotions requires the individuals to be able to understand their own emotions. Despite a deficit in emotion recognition has been observed in MS patients, the association between impaired emotion recognition and alexithymia has received little attention. The aim of this study was, first, to investigate MS patient’s abilities to recognize emotions mediated by both facial and bodily expressions and, second, to examine whether any observed deficits in emotions recognition could be explained by the presence of alexithymia. Thirty patients with MS and 30 healthy matched controls performed experimental tasks assessing emotion discrimination and recognition of facial expressions and bodily postures. Moreover, they completed questionnaires evaluating alexithymia, depression, and fatigue. First, facial emotion recognition and, to a lesser extent, bodily emotion recognition can be impaired in MS patients. In particular, patients with higher disability showed an impairment in emotion recognition compared with patients with lower disability and controls. Second, their deficit in emotion recognition was not predicted by alexithymia. Instead, the disease’s characteristics and the performance on some cognitive tasks significantly correlated with emotion recognition. Impaired facial emotion recognition is a cognitive signature of MS that is not dependent on alexithymia. (JINS, 2014, 19, 1–11)

Keywords

Multiple sclerosisAlexithymiaEmotionDepressionFacial expressionbodily postures
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 20 , Supplement 10 , November 2014 , pp. 1004 - 1014
Copyright
Copyright © The International Neuropsychological Society 2014 

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References

Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. (1994). Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature, 372(6507), 669–672.Google Scholar
Adolphs, R., Tranel, D., Hamann, S., Young, A.W., Calder, A.J., Phelps, E.A., … Damasio, A.R. (1999). Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia, 37(10), 1111–1117.Google Scholar
Aiello, M., Eleopra, R., Lettieri, C., Mondani, M., D’Auria, S., Belgrado, E., … Rumiati, R. (2014). Emotion recognition in Parkinson’s disease after subthalamic deep brain stimulation: Differential effects of microlesion and STN stimulation. Cortex, 51, 35–45.Google Scholar
Amato, M., Portaccio, E., Goretti, B., Zipoli, V., Ricchiuti, L., De Caro, M., … Trojano, M. (2006). The Rao’s Brief Repeatable Battery and Stroop Test: Normative values with age, education and gender corrections in an Italian population. Multiple Sclerosis, 12(6), 787–793.CrossRefGoogle Scholar
Assogna, F., Pontieri, F.E., Caltagirone, C., & Spalletta, G. (2008). The recognition of facial emotion expressions in Parkinson's disease. European Neuropsychopharmacology, 18(11), 835–848.Google Scholar
Assogna, F., Pontieri, F.E., Cravello, L., Peppe, A., Pierantozzi, M., Stefani, A., … Spalletta, G. (2010). Intensity-dependent facial emotion recognition and cognitive functions in Parkinson's disease. Journal of the International Neuropsychological Society, 16(5), 867–876.CrossRefGoogle ScholarPubMed
Baggio, H., Segura, B., Ibarretxe-Bilbao, N., Valldeoriola, F., Marti, M., Compta, Y., … Junque, C. (2012). Structural correlates of facial emotion recognition deficits in Parkinson's disease patients. Neuropsychologia, 50(8), 2121–2128.CrossRefGoogle ScholarPubMed
Bakshi, R., Shaikh, Z., Miletich, R., Czarnecki, D., Dmochowski, J., Henschel, K., … Kinkel, P. (2000). Fatigue in multiple sclerosis and its relationship to depression and neurologic disability. Multiple Sclerosis, 6(3), 181–185.CrossRefGoogle ScholarPubMed
Barsalou, L. (2008). Grounded cognition. Annual Review of Psychology, 59, 617–645.Google Scholar
Beck, A.T., & Beck, R. W. (1972). Screening depressed patients in a family practive: A rapid technique. Postgraduate Medicine, 52, 4.Google Scholar
Benton, A., Hamsher, K., Varney, N., & Spreen, O. (1983). Contributions to neuropsychology assessment: A clinical manual. New York, NY: Oxford University Press.Google Scholar
Besharat, M.A., Pourhosein, R., Rostami, R., & Bazzazian, S. (2011). Perfectionism and fatigue in multiple sclerosis. Psychology & Health, 26(4), 419–432.CrossRefGoogle ScholarPubMed
Bodini, B., Mandarelli, G., Tomassini, V., Tarsitani, L., Pestalozza, I., Gasperini, C., … Pozzilli, C. (2008). Alexithymia in multiple sclerosis: Relationship with fatigue and depression. Acta Neurologica Scandinavica, 118(1), 18–23.CrossRefGoogle ScholarPubMed
Bressi, C., Taylor, G., Parker, J., Bressi, S., Brambilla, V., Aguglia, E., … Bucca, M. (1996). Cross validation of the factor structure of the 20-item Toronto Alexithymia Scale: an Italian multicenter study. Journal of Psychosomatic Research, 41(6), 551–559.Google Scholar
Brown, R., Tennant, C., Sharrock, M., Hodgkinson, S., Dunn, S., & Pollard, J. (2006). Relationship between stress and relapse in multiple sclerosis: Part II. Direct and indirect relationships. Multiple Sclerosis, 12(4), 465–475.CrossRefGoogle ScholarPubMed
Chahraoui, K., Pinoit, J.-M., Viegas, N., Adnet, J., Bonin, B., & Moreau, T. (2008). Alexithymie et liens avec la dépression et l’anxiété dans la sclérose en plaques. Revue Neurologique, 164(3), 242–245.CrossRefGoogle Scholar
Chiaravalloti, N., & DeLuca, J. (2008). Cognitive impairment in multiple sclerosis. Lancet Neurology, 7(12), 1139–1151.CrossRefGoogle ScholarPubMed
Compston, A., & Coles, A. (2002). Multiple sclerosis. Lancet, 359(9313), 1221–1231.CrossRefGoogle ScholarPubMed
de Gelder, B. (2006). Towards the neurobiology of emotional body language. Nature reviews, 7(3), 242–249.Google Scholar
de Gelder, B., Snyder, J., Greve, D., Gerard, G., & Hadjikhani, N. (2004). Fear fosters flight: a mechanism for fear contagion when perceiving emotion expressed by a whole body. Proceedings of the National Academy of Sciences of the United States of America, 101(47), 16701–16706.Google Scholar
de Gelder, B., Van den Stock, J., Balaguer, R. d. D., & Bachoud-Lévi, A.C. (2008). Huntington’s disease impairs recognition of angry and instrumental body language. Neuropsychologia, 46(1), 369–373.Google Scholar
de Gelder, B., & Van den Stock, J. (2011). The Bodily Expressive Action Stimulus Test (BEAST). Construction and validation of a stimulus basis for measuring perception of whole body expression of emotions. Frontiers in Psychology, 2, 181.Google Scholar
de Gelder, B., Van den Stock, J., Meeren, H., Sinke, C., Kret, M., & Tamietto, M. (2010). Standing up for the body. Recent progress in uncovering the networks involved in the perception of bodies and bodily expressions. Neuroscience and Biobehavioral Reviews, 34(4), 513–527.CrossRefGoogle ScholarPubMed
Di Bitonto, L., Longato, N., Jung, B., Fleury, M., Marcel, C., Collongues, N., … Blanc, F. (2011). [Reduced emotional reactivity to negative stimuli in multiple sclerosis, preliminary results]. Revue Neurologique, 167(11), 820–826.Google Scholar
Feinstein, A., DeLuca, J., Baune, B.T., Filippi, M., & Lassman, H. (2013). Cognitive and neuropsychiatric disease manifestations in MS. Multiple Sclerosis and Related Disorders, 2(1), 4–12.CrossRefGoogle ScholarPubMed
Gay, M.C., Vrignaud, P., Garitte, C., & Meunier, C. (2010). Predictors of depression in multiple sclerosis patients. Acta Neurologica Scandinavica, 121(3), 161–170.Google Scholar
Ghosh, B., Rowe, J., Calder, A., Hodges, J., & Bak, T. (2009). Emotion recognition in progressive supranuclear palsy. Journal of Neurology, Neurosurgery, & Psychiatry, 80(10), 1143–1145.Google Scholar
Giovagnoli, A.R., Del Pesce, M., Mascheroni, S., Simoncelli, M., Laiacona, M., & Capitani, E. (1996). Trail making test: normative values from 287 normal adult controls. The Italian Journal of Neurological Sciences, 17(4), 305–309.Google Scholar
Goldman, A., & Sripada, C. (2005). Simulationist models of face-based emotion recognition. Cognition, 94(3), 193–213.Google Scholar
Grynberg, D., Chang, B., Corneille, O., Maurage, P., Vermeulen, N., Berthoz, S., & Luminet, O. (2012). Alexithymia and the processing of emotional facial expressions (EFEs): systematic review, unanswered questions and further perspectives. PloS One, 7(8), e42429.Google Scholar
Hadjikhani, N., Joseph, R.M., Manoach, D.S., Naik, P., Young, A., Snyder, J., Dominick, K., Hoge, R., Van den Stock, J., … de Gelder, B. (2009). Body expressions of emotion do not trigger fear contagion in autism spectrum disorder. Social cognitive and affective neuroscience, 4(1), 70–78.Google Scholar
Hall, J., Harris, J., Sprengelmeyer, R., Sprengelmeyer, A., Young, A., Santos, I., … Lawrie, S. (2004). Social cognition and face processing in schizophrenia. The British Journal of Psychiatry, 185, 169–170.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 the International Neuropsychological Society, 17(6), 1122–1131.CrossRefGoogle ScholarPubMed
Henry, J., Phillips, L., Beatty, W., McDonald, S., Longley, W., Joscelyne, A., & Rendell, P. (2009). Evidence for deficits in facial affect recognition and theory of mind in multiple sclerosis. Journal of the International Neuropsychological Society, 15(2), 277–285.CrossRefGoogle ScholarPubMed
Jehna, M., Langkammer, C., Wallner-Blazek, M., Neuper, C., Loitfelder, M., Ropele, S., … Enzinger, C. (2011). Cognitively preserved MS patients demonstrate functional differences in processing neutral and emotional faces. Brain Imaging and Behavior, 5(4), 241–251.CrossRefGoogle ScholarPubMed
Jehna, M., Neuper, C., Petrovic, K., Wallner-Blazek, M., Schmidt, R., Fuchs, S., … Enzinger, C. (2010). An exploratory study on emotion recognition in patients with a clinically isolated syndrome and multiple sclerosis. Clinical Neurology and Neurosurgery, 112(6), 482–484.CrossRefGoogle Scholar
Kessler, H., Schwarze, M., Filipic, S., Traue, H.C., & von Wietersheim, J. (2006). Alexithymia and facial emotion recognition in patients with eating disorders. International Journal of Eating Disorders, 39(3), 245–251.CrossRefGoogle ScholarPubMed
Krause, M., Wendt, J., Dressel, A., Berneiser, J., Kessler, C., Hamm, A., & Lotze, M. (2009). Prefrontal function associated with impaired emotion recognition in patients with multiple sclerosis. Behavioural Brain Research, 205(1), 280–285.Google Scholar
Kret, M., Stekelenburg, J., Roelofs, K., & de Gelder, B. (2013). Perception of face and body expressions using electromyography, pupillometry and gaze measures. Frontiers in psychology, 4, 28.CrossRefGoogle ScholarPubMed
Krupp, L.B., LaRocca, N.G., Muir-Nash, J., & Steinberg, A.D. (1989). The fatigue severity scale: application to patients with multiple sclerosis and systemic lupus erythematosus. Archives of Neurology, 46(10), 1121–1123.CrossRefGoogle ScholarPubMed
Kurtzke, J. (1983). Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS). Neurology, 33(11), 1444–1452.CrossRefGoogle ScholarPubMed
Levant, R.F., Good, G.E., Cook, S.W., O’Neil, J.M., Smalley, K.B., Owen, K., & Richmond, K. (2006). The normative Male Alexithymia Scale: Measurement of a gender-linked syndrome. Psychology of Men & Masculinity, 7(4), 212.Google Scholar
Levant, R.F., Hall, R.J., Williams, C.M., & Hasan, N.T. (2009). Gender differences in alexithymia. Psychology of Men & Masculinity, 10(3), 190.Google Scholar
Mann, L.S., Wise, T.N., Trinidad, A., & Kohansky, R. (1995). Alexithymia, affect recognition, and five factors of personality in substance abusers. Perceptual and Motor Skills, 81(1), 35–40.Google Scholar
McCade, D., Savage, G., & Naismith, S.L. (2012). Review of emotion recognition in mild cognitive impairment. Dementia and geriatric cognitive disorders, 32(4), 257–266.Google Scholar
McDonald, W.I., Compston, A., Edan, G., Goodkin, D., Hartung, H., Lublin, F.D., … Wolinsky, J.S. (2001). Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Annals of Neurology, 50(1), 121–127.Google Scholar
Mike, A., Strammer, E., Aradi, M., Orsi, G., Perlaki, G., Hajnal, A., … Illes, Z. (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(12), e82422.Google Scholar
Milo, R., & Kahana, E. (2010). Multiple sclerosis: geoepidemiology, genetics and the environment. Autoimmunity Reviews, 9(5), A387–A394.CrossRefGoogle ScholarPubMed
Monaco, M., Costa, A., Caltagirone, C., & Carlesimo, G. (2013). Forward and backward span for verbal and visuo-spatial data: standardization and normative data from an Italian adult population. Neurological Sciences, 34(5), 749–754.CrossRefGoogle ScholarPubMed
Namiki, C., Hirao, K., Yamada, M., Hanakawa, T., Fukuyama, H., Hayashi, T., & Murai, T. (2007). Impaired facial emotion recognition and reduced amygdalar volume in schizophrenia. Psychiatry Research, 156(1), 23–32.CrossRefGoogle ScholarPubMed
Narme, P., Mouras, H., Roussel, M., Duru, C., Krystkowiak, P., & Godefroy, O. (2013). Emotional and cognitive social processes are impaired in Parkinson's disease and are related to behavioral disorders. Neuropsychology, 27(2), 182–192.Google Scholar
Nemiah, J., Freyberger, H., & Sifneos, P. (1976). Alexithymia: a view of the psychosomatic process. Modern Trends in Psychosomatic Medicine, 3, 430–439.Google Scholar
Novelli, G., Papagno, C., Capitani, E., & Laiacona, M. (1986). Tre test clinici di ricerca e produzione lessicale. Taratura su sogetti normali. Archivio di Psicologia, Neurologia e Psichiatria, 47(4), 477–506.Google Scholar
Nyenhuis, D.L., Rao, S.M., Zajecka, J.M., Luchetta, T., Bernardin, L., & Garron, D.C. (1995). Mood disturbance versus other sympthoms of depression in multiple sclerosis. Journal of the International Neuropsychological Society, 1(3), 291–296.Google Scholar
Orsini, A., Grossi, D., Capitani, E., Laiacona, M., Papagno, C., & Vallar, G. (1987). Verbal and spatial immediate memory span: normative data from 1355 adults and 1112 children. The Italian Journal of Neurological Sciences, 8(6), 537–548.Google Scholar
Parmenter, B., Weinstock-Guttman, B., Garg, N., Munschauer, F., & Benedict, R.H. (2007). Screening for cognitive impairment in multiple sclerosis using the Symbol Digit Modalities Test. Multiple Sclerosis, 13(1), 52–57.Google Scholar
Passamonti, L., Cerasa, A., Liguori, M., Gioia, M., Valentino, P., Nisticò, R., … Fera, F. (2009). Neurobiological mechanisms underlying emotional processing in relapsing-remitting multiple sclerosis. Brain, 132(Pt 12), 3380–3391.Google Scholar
Phillips, L., Henry, J., Scott, C., Summers, F., Whyte, M., & Cook, M. (2011). Specific impairments of emotion perception in multiple sclerosis. Neuropsychology, 25(1), 131–136.Google Scholar
Pinto, C., Gomes, F., Moreira, I., Rosa, B., Santos, E., Silva, A.M., & Cavaco, S. (2012). Emotion recognition in multiple sclerosis. Journal of Eye Tracking, Visual Cognition and Emotion, 2(1), 76–81.Google Scholar
Pittion-Vouyovitch, S., Debouverie, M., Guillemin, F., Vandenberghe, N., Anxionnat, R., & Vespignani, H. (2006). Fatigue in multiple sclerosis is related to disability, depression and quality of life. Journal of the Neurological Sciences, 243(1--2), 39–45.CrossRefGoogle ScholarPubMed
Pontieri, F.E., Assogna, F., Stefani, A., Pierantozzi, M., Meco, G., Benincasa, D., & Spalletta, G. (2012). Sad and happy facial emotion recognition impairment in progressive supranuclear palsy in comparison with Parkinson's disease. Parkinsonism & Related Disorders, 18(7), 871–875.Google Scholar
Prochnow, D., Donell, J., Schäfer, R., Jörgens, S., Hartung, H., Franz, M., & Seitz, R. (2011). Alexithymia and impaired facial affect recognition in multiple sclerosis. Journal of Neurology, 258(9), 1683–1688.Google Scholar
Quaranta, D., Marra, C., Zinno, M., Patanella, A.K., Messina, M.J., Piccininni, C., & Gainotti, G. (2012). Presentation and validation of the multiple sclerosis depression rating scale: a test specifically devised to investigate affective disorders in multiple sclerosis patients. The Clinical Neuropsychologist, 26(4), 571–587.Google Scholar
Robotham, L., Sauter, D.A., Bachoud-Lévi, A.-C., & Trinkler, I. (2011). The impairment of emotion recognition in Huntington’s disease extends to positive emotions. Cortex, 47(7), 880–884.CrossRefGoogle ScholarPubMed
Sartori, G., Lombardi, L., & Mattiuzzi, L. (2005). Semantic relevance best predicts normal and abnormal name retrieval. Neuropsychologia, 43(5), 754–770.Google Scholar
Schwartz, C., & Frohner, R. (2005). Contribution of demographic, medical, and social support variables in predicting the mental health dimension of quality of life among people with multiple sclerosis. Health & Social Work, 30(3), 203–212.Google Scholar
Solari, A., Filippini, G., Mendozzi, L., Ghezzi, A., Cifani, S., Barbieri, E., … Mosconi, P. (1999). Validation of Italian multiple sclerosis quality of life 54 questionnaire. Journal of Neurology, Neurosurgery, & Psychiatry, 67(2), 158–162.CrossRefGoogle ScholarPubMed
Spoletini, I., Marra, C., Iulio, F.D., Gianni, W., Sancesario, G., Giubilei, F., … Spalletta, G. (2008). Facial emotion recognition deficit in amnestic mild cognitive impairment and Alzheimer disease. The American Journal of Geriatric Psychiatry, 16(5), 389–398.CrossRefGoogle ScholarPubMed
Sprengelmeyer, R., Schroeder, U., Young, A., & Epplen, J. (2006). Disgust in pre-clinical Huntington's disease: A longitudinal study. Neuropsychologia, 44(4), 518–533.Google Scholar
Sprengelmeyer, R., Young, A., Mahn, K., Schroeder, U., Woitalla, D., Büttner, T., & Przuntek, H. (2003). Facial expression recognition in people with medicated and unmedicated Parkinson’s disease. Neuropsychologia, 41(8), 1047–1057.Google Scholar
Tamietto, M., Geminiani, G., Genero, R., & de Gelder, B. (2007). Seeing fearful body language overcomes attentional deficits in patients with neglect. Journal of cognitive neuroscience, 19(3), 445–454.CrossRefGoogle ScholarPubMed
Tottenham, N., Tanaka, J., Leon, A., McCarry, T., Nurse, M., Hare, T., … Nelson, C. (2009). The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Research, 168(3), 242–249.Google Scholar
Tsui, C.F., Huang, J., Lui, S.S.Y., Au, A.C.W., Leung, M.M.W., Cheung, E.F.C., & Chan, R.C.K. (2013). Facial emotion perception abnormality in patients with early schizophrenia. Schizophrenia Research, 147(2), 230–235.Google Scholar
Van den Stock, J., van de Riet, W., Righart, R., & de Gelder, B. (2008). Neural correlates of perceiving emotional faces and bodies in developmental prosopagnosia: an event-related fMRI-study. PloS one, 3(9), e3195.Google Scholar
Van den Stock, J., de Jong, S. J., Hodiamont, P.P., & de Gelder, B. (2011). Perceiving emotions from bodily expressions and multisensory integration of emotion cues in schizophrenia. Social Neuroscience, 6(5--6), 537–547.CrossRefGoogle ScholarPubMed
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