Abstract

BackgroundSocial motivation theory suggests that deficits in social reward processing underlie social impairments in autism spectrum disorders (ASD). However, the extent to which abnormalities in reward processing generalize to other classes of stimuli remains unresolved. The aim of the current study was to examine if reward processing abnormalities in ASD are specific to social stimuli or can be generalized to other classes of reward. Additionally, we sought to examine the results in the light of behavioral impairments in ASD.MethodsParticipants performed adapted versions of the social and monetary incentive delay tasks. Data from 21 unmedicated right-handed male participants with ASD and 21 age- and IQ-matched controls were analyzed using a factorial design to examine the blood-oxygen-level-dependent (BOLD) response during the anticipation and receipt of both reward types.ResultsBehaviorally, the ASD group showed less of a reduction in reaction time (RT) for rewarded compared to unrewarded trials than the control group. In terms of the fMRI results, there were no significant group differences in reward circuitry during reward anticipation. During the receipt of rewards, there was a significant interaction between group and reward type in the left dorsal striatum (DS). The ASD group showed reduced activity in the DS compared to controls for social rewards but not monetary rewards and decreased activation for social rewards compared to monetary rewards. Controls showed no significant difference between the two reward types. Increased activation in the DS during social reward processing was associated with faster response times for rewarded trials, compared to unrewarded trials, in both groups. This is in line with behavioral results indicating that the ASD group showed less of a reduction in RT for rewarded compared to unrewarded trials. Additionally, de-activation to social rewards was associated with increased repetitive behavior in ASD.ConclusionsIn line with social motivation theory, the ASD group showed reduced activation, compared to controls, during the receipt of social rewards in the DS. Groups did not differ significantly during the processing of monetary rewards. BOLD activation in the DS, during social reward processing, was associated with behavioral impairments in ASD.

Highlights

  • Social motivation theory suggests that deficits in social reward processing underlie social impairments in autism spectrum disorders (ASD)

  • Groups did not differ in terms of age, Full Scale IQ (FSIQ), Verbal IQ (VIQ), or Performance IQ (PIQ)

  • Difference scores (RT ‘small reward’ - reaction time (RT) ‘no reward’; RT ‘large reward’ - RT ‘no reward’; RT ‘large reward’ - RT ‘small reward’) were calculated to examine the group by magnitude interaction. These indicated that the ASD group showed less of a difference in RT between ‘no reward’ and ‘small reward’ (t(40) = −2.337, P = 0.025)) and between ‘no reward’ and ‘large reward’ than the control group (t(40) = −2.434, P = 0.020) but not between ‘large reward’ and ‘small reward’ (t(40) = −0.809, P = 0.424)

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Summary

Introduction

Social motivation theory suggests that deficits in social reward processing underlie social impairments in autism spectrum disorders (ASD). The extent to which abnormalities in reward processing generalize to other classes of stimuli remains unresolved. The aim of the current study was to examine if reward processing abnormalities in ASD are specific to social stimuli or can be generalized to other classes of reward. Autism spectrum disorders (ASD) are characterized by deficits in social communication and restricted interests and repetitive behaviors [1]. Reward processing involves a well defined, interconnected, network of cortical and subcortical regions including the orbitofrontal (OFC) and ventromedial prefrontal cortex (vmPFC), anterior cingulate cortex (ACC), striatum, amygdala, and the dopaminergic midbrain [69]. The striatum is critical to this circuit; the ventral striatum (VS) for the motivational control of action and dorsal striatum (DS) for integrating rewards with executive functions and action control [9,12]

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