Processing of social and monetary rewards in autism spectrum disorders.


Journal

The British journal of psychiatry : the journal of mental science
ISSN: 1472-1465
Titre abrégé: Br J Psychiatry
Pays: England
ID NLM: 0342367

Informations de publication

Date de publication:
03 2023
Historique:
pubmed: 27 1 2023
medline: 16 2 2023
entrez: 26 1 2023
Statut: ppublish

Résumé

Reward processing has been proposed to underpin the atypical social feature of autism spectrum disorder (ASD). However, previous neuroimaging studies have yielded inconsistent results regarding the specificity of atypicalities for social reward processing in ASD. Utilising a large sample, we aimed to assess reward processing in response to reward type (social, monetary) and reward phase (anticipation, delivery) in ASD. Functional magnetic resonance imaging during social and monetary reward anticipation and delivery was performed in 212 individuals with ASD (7.6-30.6 years of age) and 181 typically developing participants (7.6-30.8 years of age). Across social and monetary reward anticipation, whole-brain analyses showed hypoactivation of the right ventral striatum in participants with ASD compared with typically developing participants. Further, region of interest analysis across both reward types yielded ASD-related hypoactivation in both the left and right ventral striatum. Across delivery of social and monetary reward, hyperactivation of the ventral striatum in individuals with ASD did not survive correction for multiple comparisons. Dimensional analyses of autism and attention-deficit hyperactivity disorder (ADHD) scores were not significant. In categorical analyses, Our results do not support current theories linking atypical social interaction in ASD to specific alterations in social reward processing. Instead, they point towards a generalised hypoactivity of ventral striatum in ASD during anticipation of both social and monetary rewards. We suggest this indicates attenuated reward seeking in ASD independent of social content and that elevated ADHD symptoms may attenuate altered reward seeking in ASD.

Sections du résumé

BACKGROUND
Reward processing has been proposed to underpin the atypical social feature of autism spectrum disorder (ASD). However, previous neuroimaging studies have yielded inconsistent results regarding the specificity of atypicalities for social reward processing in ASD.
AIMS
Utilising a large sample, we aimed to assess reward processing in response to reward type (social, monetary) and reward phase (anticipation, delivery) in ASD.
METHOD
Functional magnetic resonance imaging during social and monetary reward anticipation and delivery was performed in 212 individuals with ASD (7.6-30.6 years of age) and 181 typically developing participants (7.6-30.8 years of age).
RESULTS
Across social and monetary reward anticipation, whole-brain analyses showed hypoactivation of the right ventral striatum in participants with ASD compared with typically developing participants. Further, region of interest analysis across both reward types yielded ASD-related hypoactivation in both the left and right ventral striatum. Across delivery of social and monetary reward, hyperactivation of the ventral striatum in individuals with ASD did not survive correction for multiple comparisons. Dimensional analyses of autism and attention-deficit hyperactivity disorder (ADHD) scores were not significant. In categorical analyses,
CONCLUSIONS
Our results do not support current theories linking atypical social interaction in ASD to specific alterations in social reward processing. Instead, they point towards a generalised hypoactivity of ventral striatum in ASD during anticipation of both social and monetary rewards. We suggest this indicates attenuated reward seeking in ASD independent of social content and that elevated ADHD symptoms may attenuate altered reward seeking in ASD.

Identifiants

pubmed: 36700346
doi: 10.1192/bjp.2022.157
pii: S000712502200157X
pmc: PMC9929925
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

100-111

Subventions

Organisme : Autistica
Organisme : Simons Foundation Autism Research Initiative
Organisme : Innovative Medicines Initiative
ID : 115300
Organisme : Innovative Medicines Initiative
ID : 777394
Organisme : European Federation of Pharmaceutical Industries and Associations
Organisme : Autism Speaks
Pays : United States

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Auteurs

Sarah Baumeister (S)

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

Carolin Moessnang (C)

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

Nico Bast (N)

Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany and Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital Frankfurt am Main, Goethe University, Frankfurt, Germany.

Sarah Hohmann (S)

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

Pascal Aggensteiner (P)

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

Anna Kaiser (A)

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, United Kingdom and Department of Applied Psychology: Health, Development, Enhancement, and Intervention, University of Vienna, Vienna, Austria.

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, University Medical Center Utrecht Brain Center, Utrecht University, Utrecht, the Netherlands.

Simon Baron-Cohen (S)

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

Christian Beckmann (C)

Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, the Netherlands and Department of Cognitive Neuroscience, Radboud University Medical Centre, 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, Region Stockholm, Stockholm, Sweden and School of Allied Health, University of Western Australia, Perth, Western Australia.

Thomas Bourgeron (T)

Institut Pasteur, Human Genetics and Cognitive Functions Unit, Paris, France.

Annika Rausch (A)

Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, the Netherlands and Department of Cognitive Neuroscience, Radboud University Medical Centre, 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 and Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.

Guillaume Dumas (G)

Institut Pasteur, Human Genetics and Cognitive Functions Unit, Paris, France.

Sarah Durston (S)

Department of Psychiatry, University Medical Center Utrecht Brain Center, Utrecht University, Utrecht, the Netherlands.

Christine Ecker (C)

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

Dorothea L Floris (DL)

Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, the Netherlands; Department of Cognitive Neuroscience, Radboud University Medical Centre, Nijmegen, the Netherlands and Methods of Plasticity Research, Department of Psychology, University of Zurich, Zurich, Switzerland.

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, UK.

Rosemary Holt (R)

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

Mark H Johnson (MH)

Autism Research Centre, Department of Psychiatry, University of Cambridge, UK and Centre for Brain and Cognitive Development, Birkbeck, University of London, UK.

Emily J H Jones (EJH)

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

Michael V Lombardo (MV)

Autism Research Centre, Department of Psychiatry, University of Cambridge, UK and Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Italy.

Luke Mason (L)

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

Bethany Oakley (B)

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

Marianne Oldehinkel (M)

Donders Institute for Brain, Cognition and Behaviour, Radboud University, the Netherlands and Department of Cognitive Neuroscience, Radboud University Medical Centre, the Netherlands.

Antonio M Persico (AM)

Child and Adolescent Neuropsychiatry Program at Modena University Hospital, & Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Italy.

Antonia San José Cáceres (A)

Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King's College London, UK and Instituto de Investigación Sanitaria Gregorio Marañón, Hospital General Universitario Gregorio Marañón and CIBERSAM, Spain.

Thomas Wolfers (T)

Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, the Netherlands and Department of Cognitive Neuroscience, Radboud University Medical Centre, Nijmegen, the Netherlands.

Eva Loth (E)

Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK and 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 and 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 Behaviour, Radboud University, Nijmegen, the Netherlands; Department of Cognitive Neuroscience, Radboud University Medical Centre, Nijmegen, the Netherlands and Karakter Child and Adolescent Psychiatry University Centre, Nijmegen, the Netherlands.

Heike Tost (H)

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

Andreas Meyer-Lindenberg (A)

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

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; Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric University Hospital, University of Zurich, Zurich, Switzerland and Neuroscience Center Zurich, University of Zurich and ETH Zurich, Zurich, Switzerland.

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