Processing of social and monetary rewards in autism spectrum disorders

TY - JOUR

T1 - Processing of social and monetary rewards in autism spectrum disorders

AU - Baumeister, Sarah

AU - Moessnang, Carolin

AU - Bast, Nico

AU - Hohmann, Sarah

AU - Aggensteiner, Pascal

AU - Kaiser, Anna

AU - Tillmann, Julian

AU - Goyard, David

AU - Charman, Tony

AU - Ambrosino, Sara

AU - Baron-Cohen, Simon

AU - Beckmann, Christian

AU - Bölte, Sven

AU - Bourgeron, Thomas

AU - Rausch, Annika

AU - Crawley, Daisy

AU - Dell'Acqua, Flavio

AU - Dumas, Guillaume

AU - Durston, Sarah

AU - Ecker, Christine

AU - Floris, Dorothea L

AU - Frouin, Vincent

AU - Hayward, Hannah

AU - Holt, Rosemary

AU - Johnson, Mark H

AU - Jones, Emily J H

AU - Lai, Meng-Chuan

AU - Lombardo, Michael V

AU - Mason, Luke

AU - Oakley, Bethany

AU - Oldehinkel, Marianne

AU - Persico, Antonio M

AU - San José Cáceres, Antonia

AU - Wolfers, Thomas

AU - Loth, Eva

AU - Murphy, Declan G M

AU - Buitelaar, Jan K

AU - Tost, Heike

AU - Meyer-Lindenberg, Andreas

AU - Banaschewski, Tobias

AU - Brandeis, Daniel

AU - EU-AIMS LEAP group

PY - 2023/3

Y1 - 2023/3

N2 - 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.

AB - 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.

KW - Humans

KW - Autism Spectrum Disorder/diagnostic imaging

KW - Brain/diagnostic imaging

KW - Autistic Disorder

KW - Brain Mapping

KW - Reward

KW - Magnetic Resonance Imaging/methods

KW - Attention Deficit Disorder with Hyperactivity

U2 - 10.1192/bjp.2022.157

DO - 10.1192/bjp.2022.157

M3 - SCORING: Journal article

C2 - 36700346

VL - 222

SP - 100

EP - 111

JO - BRIT J PSYCHIAT

JF - BRIT J PSYCHIAT

SN - 0007-1250

IS - 3

ER -