Gender-specific modulation of neural mechanisms underlying social reward processing by Autism Quotient

Abstract

Autism spectrum disorder refers to a neurodevelopmental condition primarily characterized by deficits in social cognition and behavior. Subclinically, autistic features are supposed to be present in healthy humans and can be quantified using the Autism Quotient (AQ). Here, we investigated a potential relationship between AQ and neural correlates of social and monetary reward processing, using functional magnetic resonance imaging in young, healthy participants. In an incentive delay task with either monetary or social reward, reward anticipation elicited increased ventral striatal activation, which was more pronounced during monetary reward anticipation. Anticipation of social reward elicited activation in the default mode network (DMN), a network previously implicated in social processing. Social reward feedback was associated with bilateral amygdala and fusiform face area activation. The relationship between AQ and neural correlates of social reward processing varied in a gender-dependent manner. In women and, to a lesser extent in men, higher AQ was associated with increased posterior DMN activation during social reward anticipation. During feedback, we observed a negative correlation of AQ and right amygdala activation in men only. Our results suggest that social reward processing might constitute an endophenotype for autism-related traits in healthy humans that manifests in a gender-specific way.

Keywords: amygdala; autism quotient; default mode network; fusiform face area; gender differences; precuneus; social reward.

Fig. 1.

Schematic illustration of the experimental paradigm. Two different reward conditions were employed: in the monetary condition the participant could win money (1€), in the social condition a picture of a smiling face was presented upon successful response in a RT task. In a neutral control condition, white noise was always presented as feedback. Different cue categories signaled both reward trials and the no-outcome trials. See Methods and Supplementary Online Information for further details.

Fig. 2.

Positive effect of reward. The anticipation of reward led to a striatal activation (reward > neutral baseline). This positive effect of reward was significant at P < 0.001, FWE-corrected for ROI volume. Activations are superimposed on the MNI template brain provided by MRIcron. Coordinates are in MNI space. Bar plots depict contrasts of parameter estimates at the peak coordinate separated by gender and reward condition. Error bars depict standard errors of the mean. No R: neutral baseline. Mon R: condition with monetary reward. Soc R: condition with social reward.

Fig. 3.

Reward-dependent modulation of striatal activation. The anticipation of monetary reward elicited more pronounced striatal activation as compared with anticipation of social reward (monetary reward > social reward). This effect was significant at P < 0.05, FWE-corrected for ROI volume. Activations are superimposed on the MNI template brain provided by MRIcron. Coordinates are in MNI space. Bar plots depict contrasts of parameter estimates at the peak coordinate separated by gender and reward condition. Error bars depict standard errors of the mean. Mon R: condition with monetary reward. Soc R: condition with social reward.

Fig. 4.

Anticipation of social vs monetary reward. (A) The anticipation of social but not monetary reward (social reward > monetary reward) was associated with a relative activation difference in posterior DMN structures (PCC/precuneus and TPJ). This effect was significant at P < 0.05, FWE-corrected for ROI volume. Activations are superimposed on the MNI template brain provided by MRIcron. Coordinates are in MNI space. Bar plots depict contrasts of parameter estimates at the peak coordinate separated by gender and reward condition. Error bars depict standard errors of the mean. Mon R: condition with monetary reward. Soc R: condition with social reward. (B) Relationship between Autism Quotient (AQ) and blood oxygen level-dependent signal in PCC/precuneus to anticipation of social vs monetary reward. Robust Shepherd’s pi correlations are shown. AQ was correlated positively with PCC/precuneus blood oxygen level-dependent signal to anticipation of social vs monetary reward in women, and a trend was observed in men.

Fig. 5.

Social vs monetary reward feedback. (A) Bilateral activation of the FFA and the amygdala was observed during social feedback, when compared with monetary feedback (social feedback > monetary feedback). This effect was significant at P < 0.001, FWE-corrected for ROI volume. Activations are superimposed on the MNI template brain provided by MRIcron. Coordinates are in MNI space. Bar plots depict contrasts of parameter estimates at the peak coordinate separated by gender and reward condition. Error bars depict standard errors of the mean. Mon R: condition with monetary reward. Soc R: condition with social reward. (B) Relationship between the Autism Quotient (AQ) and the blood oxygen level-dependent signal in the right amygdala, separated by gender. Robust Shepherd’s pi correlations are shown. AQ was correlated negatively with right amygdala blood oxygen BOLD response to social vs monetary reward feedback in men but not in women.