Sarah Baumeister, Carolin Moessnang, Nico Bast, Sarah Hohmann, Pascal Aggensteiner, Anna Kaiser, 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, Bethany Oakley, Marianne Oldehinkel, Antonio M. Persico, Antonia San José Cáceres, Thomas Wolfers, Eva Loth, Declan G. M. Murphy, Jan K. Buitelaar, Heike Tost, Andreas Meyer-Lindenberg, Tobias Banaschewski, Daniel Brandeis and the EU-AIMS LEAP Group
The British Journal of Psychiatry
Publication year: 2023

Abstract

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, post hoc comparisons showed that ASD effects were most pronounced in participants with ASD without co-occurring ADHD.

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.

Keywords: Autism spectrum disorder, autism traits, reward processing, fMRI, ADHD symptoms, multisite

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