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

Abstract 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 th...

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Main Authors: Carolin Moessnang, Sarah Baumeister, Julian Tillmann, David Goyard, Tony Charman, Sara Ambrosino, Simon Baron-Cohen, Christian Beckmann, Sven Bölte, Carsten Bours, Daisy Crawley, Flavio Dell’Acqua, Sarah Durston, Christine Ecker, Vincent Frouin, Hannah Hayward, Rosemary Holt, Mark Johnson, Emily Jones, Meng-Chuan Lai, Michael V. Lombardo, Luke Mason, Marianne Oldenhinkel, Antonio Persico, Antonia San José Cáceres, Will Spooren, Eva Loth, Declan G. M. Murphy, Jan K. Buitelaar, Tobias Banaschewski, Daniel Brandeis, Heike Tost, Andreas Meyer-Lindenberg, the EU-AIMS LEAP group
Format: Article
Language:English
Published: BMC 2020-02-01
Series:Molecular Autism
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13229-020-0317-x
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author Carolin Moessnang
Sarah Baumeister
Julian Tillmann
David Goyard
Tony Charman
Sara Ambrosino
Simon Baron-Cohen
Christian Beckmann
Sven Bölte
Carsten Bours
Daisy Crawley
Flavio Dell’Acqua
Sarah Durston
Christine Ecker
Vincent Frouin
Hannah Hayward
Rosemary Holt
Mark Johnson
Emily Jones
Meng-Chuan Lai
Michael V. Lombardo
Luke Mason
Marianne Oldenhinkel
Antonio Persico
Antonia San José Cáceres
Will Spooren
Eva Loth
Declan G. M. Murphy
Jan K. Buitelaar
Tobias Banaschewski
Daniel Brandeis
Heike Tost
Andreas Meyer-Lindenberg
the EU-AIMS LEAP group
author_facet Carolin Moessnang
Sarah Baumeister
Julian Tillmann
David Goyard
Tony Charman
Sara Ambrosino
Simon Baron-Cohen
Christian Beckmann
Sven Bölte
Carsten Bours
Daisy Crawley
Flavio Dell’Acqua
Sarah Durston
Christine Ecker
Vincent Frouin
Hannah Hayward
Rosemary Holt
Mark Johnson
Emily Jones
Meng-Chuan Lai
Michael V. Lombardo
Luke Mason
Marianne Oldenhinkel
Antonio Persico
Antonia San José Cáceres
Will Spooren
Eva Loth
Declan G. M. Murphy
Jan K. Buitelaar
Tobias Banaschewski
Daniel Brandeis
Heike Tost
Andreas Meyer-Lindenberg
the EU-AIMS LEAP group
author_sort Carolin Moessnang
collection DOAJ
description Abstract 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.
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spelling doaj.art-f48a8574767d4ae79e94aec9107f7ec32022-12-21T23:40:53ZengBMCMolecular Autism2040-23922020-02-0111111710.1186/s13229-020-0317-xSocial brain activation during mentalizing in a large autism cohort: the Longitudinal European Autism ProjectCarolin Moessnang0Sarah Baumeister1Julian Tillmann2David Goyard3Tony Charman4Sara Ambrosino5Simon Baron-Cohen6Christian Beckmann7Sven Bölte8Carsten Bours9Daisy Crawley10Flavio Dell’Acqua11Sarah Durston12Christine Ecker13Vincent Frouin14Hannah Hayward15Rosemary Holt16Mark Johnson17Emily Jones18Meng-Chuan Lai19Michael V. Lombardo20Luke Mason21Marianne Oldenhinkel22Antonio Persico23Antonia San José Cáceres24Will Spooren25Eva Loth26Declan G. M. Murphy27Jan K. Buitelaar28Tobias Banaschewski29Daniel Brandeis30Heike Tost31Andreas Meyer-Lindenberg32the EU-AIMS LEAP groupDepartment of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim / University of HeidelbergDepartment of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim / University of HeidelbergDepartment of Psychology, Institute of Psychiatry, Psychology & Neuroscience, King’s College LondonNeurospin Centre CEADepartment of Psychology, Institute of Psychiatry, Psychology & Neuroscience, King’s College LondonDepartment of Psychiatry, UMC Utrecht Brain CenterAutism Research Centre, Department of Psychiatry, University of CambridgeDonders Institute for Brain, Cognition and Behavior, Radboud UniversityCenter 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 CouncilDonders Institute for Brain, Cognition and Behavior, Radboud UniversityDepartment of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King’s College LondonDepartment of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King’s College LondonDepartment of Psychiatry, UMC Utrecht Brain CenterDepartment of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital Frankfurt am Main, Goethe UniversityNeurospin Centre CEADepartment of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King’s College LondonAutism Research Centre, Department of Psychiatry, University of CambridgeCentre for Brain and Cognitive Development, Birkbeck, University of LondonCentre for Brain and Cognitive Development, Birkbeck, University of LondonAutism Research Centre, Department of Psychiatry, University of CambridgeAutism Research Centre, Department of Psychiatry, University of CambridgeCentre for Brain and Cognitive Development, Birkbeck, University of LondonDonders Institute for Brain, Cognition and Behavior, Radboud UniversityChild and Adolescent Neuropsychiatry Unit, “Gaetano Martino” University Hospital, University of MessinaDepartment of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King’s College LondonRoche Pharmaceutical Research and Early Development, NORD Discovery and Translational Area, Roche Innovation Center BaselDepartment of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King’s College LondonDepartment of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King’s College LondonDonders Institute for Brain, Cognition and Behavior, Radboud UniversityDepartment of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim / University of HeidelbergDepartment of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim / University of HeidelbergDepartment of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim / University of HeidelbergDepartment of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim / University of HeidelbergAbstract 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.http://link.springer.com/article/10.1186/s13229-020-0317-xAutismAutism spectrum disorderSocial brainfMRIMentalizingTheory of mind
spellingShingle Carolin Moessnang
Sarah Baumeister
Julian Tillmann
David Goyard
Tony Charman
Sara Ambrosino
Simon Baron-Cohen
Christian Beckmann
Sven Bölte
Carsten Bours
Daisy Crawley
Flavio Dell’Acqua
Sarah Durston
Christine Ecker
Vincent Frouin
Hannah Hayward
Rosemary Holt
Mark Johnson
Emily Jones
Meng-Chuan Lai
Michael V. Lombardo
Luke Mason
Marianne Oldenhinkel
Antonio Persico
Antonia San José Cáceres
Will Spooren
Eva Loth
Declan G. M. Murphy
Jan K. Buitelaar
Tobias Banaschewski
Daniel Brandeis
Heike Tost
Andreas Meyer-Lindenberg
the EU-AIMS LEAP group
Social brain activation during mentalizing in a large autism cohort: the Longitudinal European Autism Project
Molecular Autism
Autism
Autism spectrum disorder
Social brain
fMRI
Mentalizing
Theory of mind
title Social brain activation during mentalizing in a large autism cohort: the Longitudinal European Autism Project
title_full Social brain activation during mentalizing in a large autism cohort: the Longitudinal European Autism Project
title_fullStr Social brain activation during mentalizing in a large autism cohort: the Longitudinal European Autism Project
title_full_unstemmed Social brain activation during mentalizing in a large autism cohort: the Longitudinal European Autism Project
title_short Social brain activation during mentalizing in a large autism cohort: the Longitudinal European Autism Project
title_sort social brain activation during mentalizing in a large autism cohort the longitudinal european autism project
topic Autism
Autism spectrum disorder
Social brain
fMRI
Mentalizing
Theory of mind
url http://link.springer.com/article/10.1186/s13229-020-0317-x
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