Social brain activation during mentalizing in a large autism cohort: the Longitudinal European Autism Project.


Journal

Molecular autism
ISSN: 2040-2392
Titre abrégé: Mol Autism
Pays: England
ID NLM: 101534222

Informations de publication

Date de publication:
22 02 2020
Historique:
received: 02 04 2019
accepted: 23 01 2020
entrez: 24 2 2020
pubmed: 24 2 2020
medline: 1 1 2021
Statut: epublish

Résumé

Autism spectrum disorder (ASD) is a neurodevelopmental condition with key deficits in social functioning. It is widely assumed that the biological underpinnings of social impairment are neurofunctional alterations in the "social brain," a neural circuitry involved in inferring the mental state of a social partner. However, previous evidence comes from small-scale studies and findings have been mixed. We therefore carried out the to-date largest study on neural correlates of mentalizing in ASD. As part of the Longitudinal European Autism Project, we performed functional magnetic resonance imaging at six European sites in a large, well-powered, and deeply phenotyped sample of individuals with ASD (N = 205) and typically developing (TD) individuals (N = 189) aged 6 to 30 years. We presented an animated shapes task to assess and comprehensively characterize social brain activation during mentalizing. We tested for effects of age, diagnosis, and their association with symptom measures, including a continuous measure of autistic traits. We observed robust effects of task. Within the ASD sample, autistic traits were moderately associated with functional activation in one of the key regions of the social brain, the dorsomedial prefrontal cortex. However, there were no significant effects of diagnosis on task performance and no effects of age and diagnosis on social brain responses. Besides a lack of mean group differences, our data provide no evidence for meaningful differences in the distribution of brain response measures. Extensive control analyses suggest that the lack of case-control differences was not due to a variety of potential confounders. Contrary to prior reports, this large-scale study does not support the assumption that altered social brain activation during mentalizing forms a common neural marker of ASD, at least with the paradigm we employed. Yet, autistic individuals show socio-behavioral deficits. Our work therefore highlights the need to interrogate social brain function with other brain measures, such as connectivity and network-based approaches, using other paradigms, or applying complementary analysis approaches to assess individual differences in this heterogeneous condition.

Sections du résumé

BACKGROUND
Autism spectrum disorder (ASD) is a neurodevelopmental condition with key deficits in social functioning. It is widely assumed that the biological underpinnings of social impairment are neurofunctional alterations in the "social brain," a neural circuitry involved in inferring the mental state of a social partner. However, previous evidence comes from small-scale studies and findings have been mixed. We therefore carried out the to-date largest study on neural correlates of mentalizing in ASD.
METHODS
As part of the Longitudinal European Autism Project, we performed functional magnetic resonance imaging at six European sites in a large, well-powered, and deeply phenotyped sample of individuals with ASD (N = 205) and typically developing (TD) individuals (N = 189) aged 6 to 30 years. We presented an animated shapes task to assess and comprehensively characterize social brain activation during mentalizing. We tested for effects of age, diagnosis, and their association with symptom measures, including a continuous measure of autistic traits.
RESULTS
We observed robust effects of task. Within the ASD sample, autistic traits were moderately associated with functional activation in one of the key regions of the social brain, the dorsomedial prefrontal cortex. However, there were no significant effects of diagnosis on task performance and no effects of age and diagnosis on social brain responses. Besides a lack of mean group differences, our data provide no evidence for meaningful differences in the distribution of brain response measures. Extensive control analyses suggest that the lack of case-control differences was not due to a variety of potential confounders.
CONCLUSIONS
Contrary to prior reports, this large-scale study does not support the assumption that altered social brain activation during mentalizing forms a common neural marker of ASD, at least with the paradigm we employed. Yet, autistic individuals show socio-behavioral deficits. Our work therefore highlights the need to interrogate social brain function with other brain measures, such as connectivity and network-based approaches, using other paradigms, or applying complementary analysis approaches to assess individual differences in this heterogeneous condition.

Identifiants

pubmed: 32087753
doi: 10.1186/s13229-020-0317-x
pii: 10.1186/s13229-020-0317-x
pmc: PMC7036196
doi:

Types de publication

Journal Article Multicenter Study Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

17

Subventions

Organisme : Medical Research Council
ID : MR/N026063/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/T003057/1
Pays : United Kingdom

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Auteurs

Carolin Moessnang (C)

Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim / University of Heidelberg, Mannheim, Germany. carolin.moessnang@zi-mannheim.de.

Sarah Baumeister (S)

Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim / University of Heidelberg, Mannheim, Germany.

Julian Tillmann (J)

Department of Psychology, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.
Department of Applied Psychology: Health, Development, Enhancement, and Intervention, University of Vienna, Vienna, Australia.

David Goyard (D)

Neurospin Centre CEA, Saclay, Gif sur Yvette, France.

Tony Charman (T)

Department of Psychology, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.

Sara Ambrosino (S)

Department of Psychiatry, UMC Utrecht Brain Center, Utrecht, The Netherlands.

Simon Baron-Cohen (S)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK.

Christian Beckmann (C)

Donders Institute for Brain, Cognition and Behavior, Radboud University, Nijmegen, The Netherlands.
Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, The Netherlands.

Sven Bölte (S)

Center of Neurodevelopmental Disorders (KIND), Centre for Psychiatry Research, Department of Women's and Children's Health, Karolinska Institutet and Child and Adolescent Psychiatry, Stockholm Health Care Services, Stockholm County Council, Stockholm, Sweden.
Curtin Autism Research Group, School of Occupational Therapy, Social Work and Speech Pathology, Curtin University, Perth, Western Australia, Australia.

Carsten Bours (C)

Donders Institute for Brain, Cognition and Behavior, Radboud University, Nijmegen, The Netherlands.
Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, The Netherlands.

Daisy Crawley (D)

Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.

Flavio Dell'Acqua (F)

Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.
Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.

Sarah Durston (S)

Department of Psychiatry, UMC Utrecht Brain Center, Utrecht, The Netherlands.

Christine Ecker (C)

Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital Frankfurt am Main, Goethe University, Frankfurt, Germany.

Vincent Frouin (V)

Neurospin Centre CEA, Saclay, Gif sur Yvette, France.

Hannah Hayward (H)

Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.

Rosemary Holt (R)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK.

Mark Johnson (M)

Centre for Brain and Cognitive Development, Birkbeck, University of London, London, UK.

Emily Jones (E)

Centre for Brain and Cognitive Development, Birkbeck, University of London, London, UK.

Meng-Chuan Lai (MC)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK.
Centre for Addiction and Mental Health and The Hospital for Sick Children, Department of Psychiatry, University of Toronto, Toronto, Canada.
Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei, Taiwan.

Michael V Lombardo (MV)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK.
Department of Psychology, University of Cyprus, Nicosia, Cyprus.

Luke Mason (L)

Centre for Brain and Cognitive Development, Birkbeck, University of London, London, UK.

Marianne Oldenhinkel (M)

Donders Institute for Brain, Cognition and Behavior, Radboud University, Nijmegen, The Netherlands.
Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, The Netherlands.

Antonio Persico (A)

Child and Adolescent Neuropsychiatry Unit, "Gaetano Martino" University Hospital, University of Messina, Messina, Italy.
Mafalda Luce Center for Pervasive Developmental Disorders, University Campus Bio-Medico, Milan, Italy.

Antonia San José Cáceres (ASJ)

Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.

Will Spooren (W)

Roche Pharmaceutical Research and Early Development, NORD Discovery and Translational Area, Roche Innovation Center Basel, Basel, Switzerland.

Eva Loth (E)

Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.
Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.

Declan G M Murphy (DGM)

Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.
Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.

Jan K Buitelaar (JK)

Donders Institute for Brain, Cognition and Behavior, Radboud University, Nijmegen, The Netherlands.
Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, The Netherlands.
Karakter Child and Adolescent Psychiatry University Centre, Nijmegen, The Netherlands.

Tobias Banaschewski (T)

Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim / University of Heidelberg, Mannheim, Germany.

Daniel Brandeis (D)

Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim / University of Heidelberg, Mannheim, Germany.
Neuroscience Center Zurich, University of Zurich and ETH Zurich, Zurich, Switzerland.
Center for Integrative Human Physiology Zurich, University of Zurich, Zurich, Switzerland.

Heike Tost (H)

Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim / University of Heidelberg, Mannheim, Germany.

Andreas Meyer-Lindenberg (A)

Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim / University of Heidelberg, Mannheim, Germany.

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