Social dysfunction is associated with altered facial emotion neural processing across diverse neuropsychiatric disorders
Neuroscience Applied, vol. 3, pp. 103977
Abstract
Objective: Social dysfunction is a common symptom across neuropsychiatric disorders, including schizophrenia (SZ), Alzheimer’s disease (AD), depression (DEP) and anxiety (ANX) [1]. Although these disorders differ in core symptoms, they show overlap in social dysfunction, indicating possible shared neurobiological mechanisms [1,2,3]. Social dysfunction is typified by clear alterations in socio-affective neural processing, yet transdiagnostic neurobiological properties of social dysfunction remain unclear. This study examines whether alterations in neural processing of negative and positive emotional valence is coupled to social dysfunction across SZ and AD patients and whether these results can be generalized to DEP and ANX disorders. Methods: Data from the PRISM (Psychiatric Ratings using Intermediate Stratified Markers) and NESDA (Netherlands Study of Depression and Anxiety) studies were used [4,5]. PRISM included SZ (N=46), AD (N=40) and age-matched healthy controls (HC) (N=53). NESDA included DEP (N=46), ANX (N=45), comorbid DEP and ANX (COM) (N=57) and HC (N=52). All participants performed an implicit facial emotion processing (iFEP) fMRI task. During the iFEP task, participants are presented with sad, happy, fearful and angry (NESDA) faces, while asked to indicate the gender of the depicted faces through a button-press to ensure task-engagement. In PRISM, social dysfunction was indexed using the Social Functioning Scale (SFS), while the World Health Organization Disability Assessment Schedule 2.0 (WHODAS) was used in NESDA. Additionally, the Jong Gierveld Loneliness (LON) scale was used as another measure of social dysfunction in both studies. From the fMRI data, subject-level statistical maps were created for each emotion. These were fed into group-level GLM analyses (whole-brain) that included social functioning measures while correcting for clinical and demographic variables. Statistical thresholding was set at z=3.1, p < 0.05 corrected for multiple comparisons. Results: Analyses on PRISM data revealed an association across SZ/AD/HC participants wherein higher SFS social dysfunction scores were coupled to greater activation within fronto-parieto-limbic brain systems when processing sad emotions (p < 0.05); but less activation in these brain systems in response to happy emotions (p < 0.05). In NESDA- and consistent with PRISM results, higher WHODAS social dysfunction scores across DEP/ANX/COM/HC participants were associated with greater activation within the left angular gyrus in response to sad emotions (p < 0.05). However, no association was found between WHODAS scores and neural activation in response to other emotions across the participants. No diagnosis by social dysfunction interaction effects were observed for the findings. Finally, no relationship was found for total LON scores in either dataset. Conclusions: Results suggest that social dysfunction across neuropsychiatric disorders converges specifically on sad emotional valence processing of the brain, with less evidence for commonality in the response to other emotions. The findings cautiously pinpoint altered socio-affective neural processing as a putative marker for social dysfunction in persons with diverse neuropsychiatric disorders, and could aid personalized care initiatives grounded in social behaviour. References [1] Porcelli, S., N. Van Der Wee, S. van der Werff, M. Aghajani, J. C. Glennon, S. van Heukelum, F. Mogavero, A. Lobo, F. J. Olivera, E. Lobo, M. Posadas, J. Dukart, R. Kozak, E. Arce, A. Ikram, J. Vorstman, A. Bilderbeck, I. Saris, M. J. Kas, A. Serretti., 2019. Social Brain, Social Dysfunction and Social Withdrawal. Neurosci Biobehav Rev 97, 10-33. [2] Saris, I. M. J., M. Aghajani, N. Jongs, L. M. Reus, N. J. A. van der Wee, A. C. Bilderbeck, I. W. van Rossum, C. Arango, A. de la Torre-Luque, A. Malik, A. Raslescu, G. R. Dawson, J. L. Ayuso-Mateos, M. J. Kas, B. W. J. H. Penninx., 2022. Cross-Disorder and Disorder-Specific Deficits in Social Functioning among Schizophrenia and Alzheimer's Disease Patients. PLoS One 17 (4). [3] Saris, I. M. J., M. Aghajani, S. J. A. van der Werff, N. J. A. van der Wee, Bwjh Penninx., 2017. Social Functioning in Patients with Depressive and Anxiety Disorders. Acta Psychiatr Scand 136 (4), 352-61. [4] Bilderbeck, A. C., Bwjh Penninx, C. Arango, N. van der Wee, R. Kahn, I. Winter-van Rossum, A. Hayen, M. J. Kas, A. Post, G. R. Dawson., 2019. Overview of the Clinical Implementation of a Study Exploring Social Withdrawal in Patients with Schizophrenia and Alzheimer's Disease. Neurosci Biobehav Rev 97, 87-93. [5] Penninx, Bwjh, M. Eikelenboom, E. J. Giltay, A. M. van Hemert, H. Riese, R. A. Schoevers, A. T. F. Beekman., 2021. Cohort Profile of the Longitudinal Netherlands Study of Depression and Anxiety (Nesda) on Etiology, Course and Consequences of Depressive and Anxiety Disorders. J Affect Disord 287, 69-77.
Authors 17
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Amsterdam Neuroscience · Amsterdam UMC Location Vrije Universiteit Amsterdam
Affiliation as printed
Amsterdam Neuroscience, Mood- Anxiety- Psychosis- Sleep & Stress and Neurodegeneration programs, Amsterdam, Netherlands
Amsterdam UMC- location VUmc, Department of Psychiatry, Amsterdam, Netherlands
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Affiliation as printed
Amacrine, Scientific Consulting, Amsterdam, Netherlands
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Amsterdam Neuroscience · Amsterdam UMC Location Vrije Universiteit Amsterdam
Affiliation as printed
Amsterdam Neuroscience, Mood- Anxiety- Psychosis- Sleep & Stress and Neurodegeneration programs, Amsterdam, Netherlands
Amsterdam UMC- location VUmc, Department of Psychiatry, Amsterdam, Netherlands
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Affiliation as printed
Alzheimer Centre Amsterdam, Neurology, Amsterdam, Netherlands
Amsterdam Neuroscience, Neurodegeneration, Amsterdam, Netherlands
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Centro de Investigación Biomédica en Red de Salud Mental · Hospital Universitario de La Princesa
Affiliation as printed
Centre of Biomedical Research in Mental Health, Cibersam, Madrid, Spain
Hospital Universitario de la Princesa, Memory Unit. Department of Neurology, Madrid, Spain
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Universidad Complutense de Madrid · Centro de Investigación Biomédica en Red de Salud Mental
Affiliation as printed
Centre of Biomedical Research in Mental Health, Cibersam, Madrid, Spain
Complutense University of Madrid, Department of Legal Medicine- Psychiatry and Pathology, Madrid, Spain
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Affiliation as printed
P1vital Products Ltd., Manor House- Howbery Park, Wallingford, United Kingdom
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Affiliation as printed
P1vital Ltd., Manor House- Howbery Park, Wallingford, United Kingdom
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Affiliation as printed
P1vital Ltd., Manor House- Howbery Park, Wallingford, United Kingdom
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Boehringer Ingelheim (Germany)
Affiliation as printed
Boehringer Ingelheim, Pharma, Biberach, Germany
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Centro de Investigación Biomédica en Red de Salud Mental · Instituto de Investigación Sanitaria del Hospital Universitario de La Princesa · Universidad Autónoma de Madrid
Affiliation as printed
Centre of Biomedical Research in Mental Health, Cibersam, Madrid, Spain
Universidad Autonoma de Madrid- Instituto de Investigación Sanitaria Princesa, Department of Psychiatry, Madrid, Spain
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Universidad Complutense de Madrid · Hospital General Universitario Gregorio Marañón · Centro de Investigación Biomédica en Red de Salud Mental
Affiliation as printed
Centre of Biomedical Research in Mental Health, Cibersam, Madrid, Spain
Institute of Psychiatry and Mental Health- Gregorio Marañon University Hospital, Department of Child and Adolescent Psychiatry, Madrid, Spain
Universidad Complutense de Madrid, Department of Psychiatry, Madrid, Spain
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University Medical Center Groningen · University of Groningen
Affiliation as printed
University Medical Centre Groningen- University of Groningen, Cognitive Neuroscience Centre, Groningen, Netherlands
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Leiden University · Leiden University Medical Center
Affiliation as printed
Leiden University Medical Centre, Department of Psychiatry, Leiden, Netherlands
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Affiliation as printed
University of Groningen, Groningen Institute for Evolutionary Life Sciences, Groningen, Netherlands
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Leiden University · Amsterdam UMC Location Vrije Universiteit Amsterdam
Affiliation as printed
Amsterdam UMC- location VUmc, Department of Psychiatry, Amsterdam, Netherlands
Leiden University, Institute of Education & Child Studies- Section Forensic Family & Youth Care, Leiden, Netherlands
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Amsterdam Neuroscience · Amsterdam UMC Location Vrije Universiteit Amsterdam
Affiliation as printed
Amsterdam Neuroscience, Mood- Anxiety- Psychosis- Sleep & Stress and Neurodegeneration programs, Amsterdam, Netherlands
Amsterdam UMC- location VUmc, Department of Psychiatry, Amsterdam, Netherlands
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