Neural responsivity to social rewards in autistic female youth

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.

Fig. 1. fMRI task.

Schematic of an individual social trial within the experimental paradigm.

Fig. 2. Significant group differences in region of interest (ROI)-based nucleus accumbens (NAcc) activity to social rewards.

When averaging across all voxels in the bilateral NAcc region of interest (left), autistic females displayed significantly greater mean activity to social rewards than autistic males (right); error bars are +/− 1 standard error of the mean.

Fig. 3. Significant group differences in whole-brain activity to social rewards and relationship with behavior.

a Areas in which autistic girls exhibited significantly greater activity to socially rewarding stimuli than autistic boys in the whole-brain analyses (left). In the group of autistic boys, increased activity to social rewards in the right NAcc cluster was related to improved accuracy over the course of the task (i.e., greater implicit learning) (right); plotted values reflect mean parameter estimates extracted from the significant whole-brain cluster located in the right NAcc. b Regions in which autistic girls displayed significant hyperactivity to social rewards compared with TD girls in the whole-brain analyses. NAcc: nucleus accumbens; TD: typically developing; L: Left.