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.
