Neural Responsivity to Social Rewards in Girls with Autism Spectrum Disorder

Background: The social motivation hypothesis of autism spectrum disorder (ASD) posits that ASD is driven by a diminished sensitivity to the inherently rewarding nature of social stimuli, which contributes to reduced opportunities for social learning and thereby leads to the social challenges observed in ASD. Previous functional magnetic resonance (fMRI) studies have indicated that males with ASD do indeed display reduced neural activity to social rewards, but it is unknown whether this finding extends to females with ASD, particularly as behavioral evidence suggests that affected girls may not exhibit the same reduction in social motivation as their male counterparts.

Objectives: We aimed to test whether neural evidence supports the social motivation hypothesis among girls with ASD by investigating how social reward processing may differ between girls and boys with ASD, as well as between girls with ASD and typically developing (TD) girls.

Methods: As part of an NIH-funded multi-site network, fMRI data was collected during an implicit-learning socially-rewarded task from a total of 154 youths with ASD and TD controls. An approximately equal number of girls and boys contributed data to each group, and participants were between the ages of 8 and 17 years old. Prior to starting the fMRI scan, participants were told that a number of abstract fractal-like images would be presented multiple times over the course of the task, and each time an image appeared they should guess via button press whether it belonged to “Team 1” or “Team 2”, after which they would receive feedback on their response. If the participant guessed correctly, feedback consisted of a smiling male or female face with the text “That’s right!”; if the subject’s response was incorrect, a sad male or female face was instead displayed along with the text “That’s wrong.”

Results: Our group-level analyses focused on the contrast Correct > Incorrect (i.e., happy face > sad face). We used both a whole-brain approach and a region of interest (ROI) approach where we focused on the nucleus accumbens due to its known importance in reward processing. Groups were matched on implicit learning rate. Girls with ASD displayed increased activity to socially rewarding stimuli, including greater activity in the nucleus accumbens relative to boys with ASD, as well as greater activity in the lateral orbitofrontal cortex, the ventrolateral prefrontal cortex and the anterior insula compared to typically developing girls.

Conclusions: These results demonstrate for the first time that girls with ASD do not exhibit the same reduction in social reward sensitivity as boys with ASD. Instead, girls with ASD display increased neural activation to such stimuli in areas related to reward processing and salience detection. This heightened neural sensitivity to social rewards may be a protective biological mechanism underlying the reduced prevalence of ASD among females and the sex differences in friendship patterns among youth with ASD. Importantly, our findings suggest that the social motivation hypothesis may not generalize to affected females and highlight the importance of studying potential sex differences in ASD.