Abstract
Up to 40% of youth with autism spectrum disorder (ASD) also suffer from anxiety, and this comorbidity is linked with significant functional impairment. However, the mechanisms of this overlap are poorly understood. We investigated the interplay between ASD traits and anxiety during reward processing, known to be affected in ASD, in a community sample of 1472 adolescents (mean age=14.4 years) who performed a modified monetary incentive delay task as part of the Imagen project. Blood-oxygen-level dependent (BOLD) responses to reward anticipation and feedback were compared using a 2x2 analysis of variance test (ASD traits: low/high; anxiety symptoms: low/high), controlling for plausible covariates. In addition, we used a longitudinal design to assess whether neural responses during reward processing predicted anxiety at 2-year follow-up. High ASD traits were associated with reduced BOLD responses in dorsal prefrontal regions during reward anticipation and negative feedback. Participants with high anxiety symptoms showed increased lateral prefrontal responses during anticipation, but decreased responses following feedback. Interaction effects revealed that youth with combined ASD traits and anxiety, relative to other youth, showed high right insula activation when anticipating reward, and low right-sided caudate, putamen, medial and lateral prefrontal activations during negative feedback (all clusters PFWE<0.05). BOLD activation patterns in the right dorsal cingulate and right medial frontal gyrus predicted new-onset anxiety in participants with high but not low ASD traits. Our results reveal both quantitatively enhanced and qualitatively distinct neural correlates underlying the comorbidity between ASD traits and anxiety. Specific neural responses during reward processing may represent a risk factor for developing anxiety in ASD youth.
Highlights
Anxiety is common in youth with autism spectrum disorder (ASD)[1,2,3,4,5] and in young people with sub-diagnostic autistic traits.[6,7] Comorbid anxiety causes significant functional impairment in young people with ASD8,9 and impacts on the quality of life of their families.[10]
We found interaction effects whereby youth with combined ASD traits and anxiety showed distinctively high right MTG and insula activation when anticipating reward, and low prefrontal activation during negative feedback
ASD traits & Anxiety patterns during reward anticipation predicted new onset of anxiety 2 years later. During both reward anticipation and negative feedback, we observed attenuated Blood-oxygen-level dependent (BOLD) activation in prefrontal regions in participants with high compared to low ASD traits
Summary
Anxiety is common in youth with autism spectrum disorder (ASD)[1,2,3,4,5] and in young people with sub-diagnostic autistic traits.[6,7] Comorbid anxiety causes significant functional impairment in young people with ASD8,9 and impacts on the quality of life of their families.[10] the mechanisms of this association are poorly understood. While considerable research has examined the neural correlates of anxiety in adolescents, few studies have examined these correlates in children with symptoms of ASD. We investigate whether aberrations in reward processing underlie the co-occurrence of ASD traits and anxiety and whether they predict the new onset of anxiety in youth with ASD traits. Reward processing has been proposed to be central to ASD,[11,12] with aberrant processing of primary,[13] social[14,15] and monetary rewards[16] reported in children and young people with
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