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Attenuated Anticipation of Social and Monetary Rewards in Autism Spectrum Disorders

Sarah Baumeister, Carolin Moessnang, Nico Bast, Sarah Hohmann, Julian Tillmann, David Goyard, Tony Charman, Sara Ambrosino, Simon Baron-Cohen, Christian Beckmann, Sven Bölte, Thomas Bourgeron, Annika Rausch, Daisy Crawley, Flavio Dell’Acqua, Guillaume Dumas, Sarah Durston, Christine Ecker, Dorothea L. Floris, Vincent Frouin, Hannah Hayward, Rosemary Holt, Mark H. Johnson, Emily J.H. Jones, Meng-Chuan Lai, Michael V. Lombardo, Luke Mason, Marianne Oldehinkel, Tony Persico, Antonia San José Cáceres, Thomas Wolfers, Will Spooren, Eva Loth, Declan G. M. Murphy, Jan K. Buitelaar, Heike Tost, Andreas Meyer-Lindenberg, Tobias Banaschewski, Daniel Brandeis, the AIMS-2-TRIALS group
doi: https://doi.org/10.1101/2020.07.06.186650
Sarah Baumeister
1Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany
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  • For correspondence: sarah.baumeister@zi-mannheim.de
Carolin Moessnang
2Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, University of Heidelberg, Mannheim, Germany
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Nico Bast
1Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany
3Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital Frankfurt am Main, Goethe University, Frankfurt, Germany
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Sarah Hohmann
1Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany
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Julian Tillmann
4Department of Psychology, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom
5Department of Applied Psychology: Health, Development, Enhancement, and Intervention, University of Vienna, Vienna, Austria
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David Goyard
6Neurospin Centre CEA, Saclay, Gif sur Yvette, France
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Tony Charman
4Department of Psychology, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom
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Sara Ambrosino
7Department of Psychiatry, University Medical Center Utrecht Brain Center, Utrecht University, Utrecht, The Netherlands
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Simon Baron-Cohen
8Autism Research Centre, Department of Psychiatry, University of Cambridge, United Kingdom
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Christian Beckmann
9Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
10Department of Cognitive Neuroscience, Radboud University Medical Centre, Nijmegen, The Netherlands
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Sven Bölte
11Center 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
12Curtin Autism Research Group, School of Occupational Therapy, Social Work and Speech Pathology, Curtin University, Perth, Western Australia
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Thomas Bourgeron
13Institut Pasteur, Human Genetics and Cognitive Functions Unit, Paris, France
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Annika Rausch
9Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
10Department of Cognitive Neuroscience, Radboud University Medical Centre, Nijmegen, The Netherlands
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Daisy Crawley
14Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom
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Flavio Dell’Acqua
14Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom
15Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom
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Guillaume Dumas
13Institut Pasteur, Human Genetics and Cognitive Functions Unit, Paris, France
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Sarah Durston
7Department of Psychiatry, University Medical Center Utrecht Brain Center, Utrecht University, Utrecht, The Netherlands
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Christine Ecker
3Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital Frankfurt am Main, Goethe University, Frankfurt, Germany
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Dorothea L. Floris
9Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
10Department of Cognitive Neuroscience, Radboud University Medical Centre, Nijmegen, The Netherlands
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Vincent Frouin
6Neurospin Centre CEA, Saclay, Gif sur Yvette, France
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Hannah Hayward
14Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom
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Rosemary Holt
8Autism Research Centre, Department of Psychiatry, University of Cambridge, United Kingdom
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Mark H. Johnson
7Department of Psychiatry, University Medical Center Utrecht Brain Center, Utrecht University, Utrecht, The Netherlands
16Centre for Brain and Cognitive Development, Birkbeck, University of London
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Emily J.H. Jones
16Centre for Brain and Cognitive Development, Birkbeck, University of London
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Meng-Chuan Lai
8Autism Research Centre, Department of Psychiatry, University of Cambridge, United Kingdom
17Centre for Addiction and Mental Health and The Hospital for Sick Children, Department of Psychiatry, University of Toronto, Toronto, Canada
18Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei, Taiwan
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Michael V. Lombardo
8Autism Research Centre, Department of Psychiatry, University of Cambridge, United Kingdom
19Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, Italy
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Luke Mason
16Centre for Brain and Cognitive Development, Birkbeck, University of London
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Marianne Oldehinkel
9Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
10Department of Cognitive Neuroscience, Radboud University Medical Centre, Nijmegen, The Netherlands
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Tony Persico
20Child and Adolescent Neuropsychiatry Unit, “Gaetano Martino” University Hospital, University of Messina, Messina, Italy
21Mafalda Luce Center for Pervasive Developmental Disorders, University Campus Bio-Medico, Milan, Italy
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Antonia San José Cáceres
14Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom
22Instituto de Investigación Sanitaria Gregorio Marañón, Hospital General Universitario Gregorio Marañón, Madrid, Spain
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Thomas Wolfers
9Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
10Department of Cognitive Neuroscience, Radboud University Medical Centre, Nijmegen, The Netherlands
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Will Spooren
23Roche Pharmaceutical Research and Early Development, NORD Discovery and Translational Area, Roche Innovation Center Basel, Basel, Switzerland
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Eva Loth
14Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom
15Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom
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Declan G. M. Murphy
14Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom
15Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom
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Jan K. Buitelaar
9Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
10Department of Cognitive Neuroscience, Radboud University Medical Centre, Nijmegen, The Netherlands
24Karakter Child and Adolescent Psychiatry University Centre, Nijmegen, The Netherlands
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Heike Tost
2Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, University of Heidelberg, Mannheim, Germany
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Andreas Meyer-Lindenberg
2Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, University of Heidelberg, Mannheim, Germany
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Tobias Banaschewski
1Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany
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Daniel Brandeis
1Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany
25Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric Hospital, University of Zurich, Zurich Switzerland
26Neuroscience Center Zurich, University of Zurich and ETH Zurich, Zurich, Switzerland
27Center for Integrative Human Physiology Zurich, University of Zurich, Zurich, Switzerland
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Abstract

Background Reward processing has been proposed to underpin atypical social behavior, a core feature of autism spectrum disorder (ASD). However, previous neuroimaging studies have yielded inconsistent results regarding the specificity of atypicalities for social rewards in ASD. Utilizing a large sample, we aimed to assess altered reward processing in response to reward type (social, monetary) and reward phase (anticipation, delivery) in ASD.

Methods Functional magnetic resonance imaging during social and monetary reward anticipation and delivery was performed in 212 individuals with ASD (7.6-30.5 years) and 181 typically developing (TD) participants (7.6-30.8 years).

Results Across social and monetary reward anticipation, whole-brain analyses (p<0.05, family-wise error-corrected) showed hypoactivation of the right ventral striatum (VS) in ASD. Further, region of interest (ROI) analysis across both reward types yielded hypoactivation in ASD in both the left and right VS. Across delivery of social and monetary reward, hyperactivation of the VS in individuals with ASD did not survive correction for multiple comparisons. Reward type by diagnostic group interactions, and a dimensional analysis of autism trait scores were not significant during anticipation or delivery. Levels of attention-deficit/hyperactivity disorder (ADHD) symptoms did not affect reward processing in ASD.

Conclusions Our results do not support current theories linking atypical social interaction in ASD to specific alterations in processing of social rewards. Instead, they point towards a generalized hypoactivity of VS in ASD during anticipation of both social and monetary rewards. We suggest that this indicates attenuated subjective reward value in ASD independent of social content and ADHD symptoms.

Competing Interest Statement

A.M.-L. has received consultant fees from American Association for the Advancement of Science, Atheneum Partners, Blueprint Partnership, Boehringer Ingelheim, Daimler und Benz Stiftung, Elsevier, F. Hoffmann-La Roche, ICARE Schizophrenia, K. G. Jebsen Foundation, L.E.K Consulting, Lundbeck International Foundation (LINF), R. Adamczak, Roche Pharma, Science Foundation, Sumitomo Dainippon Pharma, Synapsis Foundation Alzheimer Research Switzerland, System Analytics, and has received lectures fees including travel fees from Boehringer Ingelheim, Fama Public Relations, Institut d investigacions Biomediques August Pi i Sunyer (IDIBAPS), Janssen-Cilag, Klinikum Christophsbad, Goeppingen, Lilly Deutschland, Luzerner Psychiatrie, LVR Klinikum Duesseldorf, LWL Psychiatrie Verbund Westfalen-Lippe, Otsuka Pharmaceuticals, Reunions i Ciencia S. L., Spanish Society of Psychiatry, Suedwestrundfunk Fernsehen, Stern TV, and Vitos Klinikum Kurhessen. DM has served on advisory boards for Roche and Servier, and has received research grants from Roche and J&J. W.M. has received lecture or travel fees from Pfizer, Gruenenthal, University of Zurich, International Association for the Study on Pain (IASP) and European Federation of IASP Chapters (EFIC). S.B. discloses that he has in the last 5 years acted as an author, consultant or lecturer for Medice and Roche. He receives royalties for text-books and diagnostic tools from Huber/Hogrefe (German/Swedish versions of ADI-R, ADOS-2, SRS, SCQ), Kohlhammer and UTB. T. B. has served in an advisory or consultancy role for Actelion, Hexal Pharma, Lilly, Medice, Novartis, Oxford outcomes, Otsuka, PCM Scientific, Shire and Viforpharma. He received conference support or speakers fee by Medice, Novartis and Shire. He is/has been involved in clinical trials conducted by Shire and Viforpharma. He received royalties from Hogrefe, Kohlhammer, CIP Medien, and Oxford University Press. D. B. serves as an unpaid scientific consultant for an EU-funded neurofeedback trial. ASJC receives consultant fees from Roche and Servier. JKB has been in the past 3 years a consultant to / member of advisory board of / and/or speaker for Takeda/Shire, Roche, Medice, Angelini, Janssen, and Servier. He is not an employee of any of these companies, and not a stock shareholder of any of these companies. He has no other financial or material support, including expert testimony, patents, royalties. All other authors report no potential conflict of interest. The present work is unrelated to the above grants and relationships.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Attenuated Anticipation of Social and Monetary Rewards in Autism Spectrum Disorders
Sarah Baumeister, Carolin Moessnang, Nico Bast, Sarah Hohmann, Julian Tillmann, David Goyard, Tony Charman, Sara Ambrosino, Simon Baron-Cohen, Christian Beckmann, Sven Bölte, Thomas Bourgeron, Annika Rausch, Daisy Crawley, Flavio Dell’Acqua, Guillaume Dumas, Sarah Durston, Christine Ecker, Dorothea L. Floris, Vincent Frouin, Hannah Hayward, Rosemary Holt, Mark H. Johnson, Emily J.H. Jones, Meng-Chuan Lai, Michael V. Lombardo, Luke Mason, Marianne Oldehinkel, Tony Persico, Antonia San José Cáceres, Thomas Wolfers, Will Spooren, Eva Loth, Declan G. M. Murphy, Jan K. Buitelaar, Heike Tost, Andreas Meyer-Lindenberg, Tobias Banaschewski, Daniel Brandeis, the AIMS-2-TRIALS group
bioRxiv 2020.07.06.186650; doi: https://doi.org/10.1101/2020.07.06.186650
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Attenuated Anticipation of Social and Monetary Rewards in Autism Spectrum Disorders
Sarah Baumeister, Carolin Moessnang, Nico Bast, Sarah Hohmann, Julian Tillmann, David Goyard, Tony Charman, Sara Ambrosino, Simon Baron-Cohen, Christian Beckmann, Sven Bölte, Thomas Bourgeron, Annika Rausch, Daisy Crawley, Flavio Dell’Acqua, Guillaume Dumas, Sarah Durston, Christine Ecker, Dorothea L. Floris, Vincent Frouin, Hannah Hayward, Rosemary Holt, Mark H. Johnson, Emily J.H. Jones, Meng-Chuan Lai, Michael V. Lombardo, Luke Mason, Marianne Oldehinkel, Tony Persico, Antonia San José Cáceres, Thomas Wolfers, Will Spooren, Eva Loth, Declan G. M. Murphy, Jan K. Buitelaar, Heike Tost, Andreas Meyer-Lindenberg, Tobias Banaschewski, Daniel Brandeis, the AIMS-2-TRIALS group
bioRxiv 2020.07.06.186650; doi: https://doi.org/10.1101/2020.07.06.186650

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