Processing of social and monetary rewards in autism spectrum disorders

Author:

Baumeister SarahORCID,Moessnang Carolin,Bast Nico,Hohmann Sarah,Aggensteiner PascalORCID,Kaiser Anna,Tillmann Julian,Goyard David,Charman TonyORCID,Ambrosino Sara,Baron-Cohen Simon,Beckmann Christian,Bölte Sven,Bourgeron Thomas,Rausch Annika,Crawley Daisy,Dell'Acqua Flavio,Dumas Guillaume,Durston Sarah,Ecker Christine,Floris Dorothea L.,Frouin Vincent,Hayward Hannah,Holt Rosemary,Johnson Mark H.,Jones Emily J. H.,Lai Meng-Chuan,Lombardo Michael V.,Mason Luke,Oakley Bethany,Oldehinkel Marianne,Persico Antonio M.,San José Cáceres Antonia,Wolfers Thomas,Loth Eva,Murphy Declan G. M.,Buitelaar Jan K.,Tost Heike,Meyer-Lindenberg Andreas,Banaschewski TobiasORCID,Brandeis Daniel,

Abstract

BackgroundReward 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.AimsUtilising a large sample, we aimed to assess reward processing in response to reward type (social, monetary) and reward phase (anticipation, delivery) in ASD.MethodFunctional 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).ResultsAcross 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 hoccomparisons showed that ASD effects were most pronounced in participants with ASD without co-occurring ADHD.ConclusionsOur 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.

Funder

Autism Speaks

Autistica

Simons Foundation Autism Research Initiative

Innovative Medicines Initiative

European Federation of Pharmaceutical Industries and Associations

Publisher

Royal College of Psychiatrists

Subject

Psychiatry and Mental health

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