Common and distinct neural features of social and non-social reward processing in autism and social anxiety disorder

Abstract

Autism spectrum disorders (ASDs) and social anxiety disorder (SAD) are both characterized by social dysfunction, but no study to date has compared neural responses to social rewards in ASDs and SAD. Neural responses during social and non-social reward anticipation and outcomes were examined in individuals with ASD (n = 16), SAD (n = 15) and a control group (n = 19) via functional magnetic resonance imaging. Analyses modeling all three groups revealed increased nucleus accumbens (NAc) activation in SAD relative to ASD during monetary reward anticipation, whereas both the SAD and ASD group demonstrated decreased bilateral NAc activation relative to the control group during social reward anticipation. During reward outcomes, the SAD group did not differ significantly from the other two groups in ventromedial prefrontal cortex activation to either reward type. Analyses comparing only the ASD and SAD groups revealed greater bilateral amygdala activation to social rewards in SAD relative to ASD during both anticipation and outcome phases, and the magnitude of left amygdala hyperactivation in the SAD group during social reward anticipation was significantly correlated with the severity of trait anxiety symptoms. Results suggest reward network dysfunction to both monetary and social rewards in SAD and ASD during reward anticipation and outcomes, but that NAc hypoactivation during monetary reward anticipation differentiates ASD from SAD.

Keywords: autism; social anxiety disorder; functional magnetic resonance imaging; nucleus accumbens; reward; ventromedial prefrontal cortex.

Figures

Fig. 1

Incentive delay task. Participants alternated ‘money’ and ‘face’ reward runs, denoted by an instructional screen at the start of each run. Each trial consisted of a cue (i.e. a triangle indicated an incentive trial, a circle indicated a non-incentive trial), an anticipatory delay, a target and outcome feedback.

Fig. 2

Left: Average valence and arousal ratings of faces. Valence = 0 (extremely unpleasant) to + 8 (extremely pleasant); Arousal = 0 (not at all aroused) to + 8 (extremely aroused). Right: Average reaction times during face and money conditions for both potential reward (‘Rew’) and non potential reward (‘Non’) trials. Error bars represent standard errors of the mean.

Fig. 3

Brain areas showing significant Group (ASD, SAD, Control) × Reward Type (Money, Faces) interactions during the anticipatory phase of the task. The bar graphs depict parameter estimates by group and trial type in the significant NAc clusters.

Fig. 4

Brain areas showing significant Group (ASD, SAD, Control) × Reward Type (Money, Faces) interactions during the outcome phase of the task. The bar graph depicts parameter estimates by group and trial type in the significant vmPFC cluster.

Fig. 5

Brain areas showing significant Group (ASD, SAD) × Reward Type (Money, Faces) interactions during anticipatory (upper panel) and outcome (lower panel) phases of the task. The bar graphs depict parameter estimates by group and trial type in the significant amygdala clusters. The scatterplot illustrates the significant correlation (r = 0.65, P