Abstract

Autism is hypothesized to be in part driven by a reduced sensitivity to the inherently rewarding nature of social stimuli. Previous neuroimaging studies have indicated that autistic males do indeed display reduced neural activity to social rewards, but it is unknown whether this finding extends to autistic females, particularly as behavioral evidence suggests that affected females may not exhibit the same reduction in social motivation as their male peers. We therefore used functional magnetic resonance imaging to examine social reward processing during an instrumental implicit learning task in 154 children and adolescents (ages 8–17): 39 autistic girls, 43 autistic boys, 33 typically developing girls, and 39 typically developing boys. We found that autistic girls displayed increased activity to socially rewarding stimuli, including greater activity in the nucleus accumbens relative to autistic boys, as well as greater activity in lateral frontal cortices and the anterior insula compared with typically developing girls. These results demonstrate for the first time that autistic girls do not exhibit the same reduction in activity within social reward systems as autistic boys. Instead, autistic girls display increased neural activation to such stimuli in areas related to reward processing and salience detection. Our findings indicate that a reduced sensitivity to social rewards, as assessed with a rewarded instrumental implicit learning task, does not generalize to affected female youth and highlight the importance of studying potential sex differences in autism to improve our understanding of the condition and its heterogeneity.

Highlights

  • Autism is a neurodevelopmental condition characterized by difficulties with social communication, as well as the presence of repetitive behaviors and circumscribed interests[1]

  • region of interest (ROI) analyses Descriptive within-group analyses averaging across our bilateral nucleus accumbens (NAcc) ROI revealed that autistic girls exhibited significant increases in neural activity to socially rewarding stimuli (p = 0.0007), whereas autistic boys did not (p = 0.4)

  • We examined whether autistic girls and boys differed from their same-sex typically developing (TD) counterparts and found no significant differences when averaging within the NAcc ROI

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Summary

Introduction

Autism is a neurodevelopmental condition characterized by difficulties with social communication, as well as the presence of repetitive behaviors and circumscribed interests[1]. Recent functional magnetic resonance imaging (fMRI) studies in primarily male samples have directly tested this hypothesis by examining neural activity in autism when social stimuli are presented as feedback during tasks (e.g., a picture of a smiling face appearing as feedback when participants make a correct choice)[9,10,11,12,13,14,15,16,17] This body of work has provided evidence in support of the notion that autistic individuals display reduced neural activation compared with their neurotypical peers in reward-related frontostriatal circuitry and corticolimbic regions during the anticipation and/or receipt of positive social feedback[9,12].

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