Neural evidence for an association between social proficiency and sensitivity to social reward

Abstract

Data from developmental psychology suggests a link between the growth of socio-emotional competences and the infant's sensitivity to the salience of social stimuli. The aim of the present study was to find evidence for this relationship in healthy adults. Thirty-five participants were recruited based on their score above the 85th or below the 15th percentile of the empathy quotient questionnaire (EQ, Baron-Cohen and Wheelwright, 2004). Functional magnetic resonance imaging (fMRI) was used to compare neural responses to cues of social and non-social (monetary) reward. When compared to the high-EQ group, the low-EQ group showed reduced activity of the brain s reward system, specifically the right nucleus accumbens, in response to cues predictive of social reward (videos showing gestures of approval)-but increased activation in this area for monetary incentives. Our data provide evidence for a link between self-reported deficits in social proficiency and reduced sensitivity to the motivational salience of positive social stimuli.

Keywords: NAcc; autism; empathy; social interest; social reward.

Fig. 1

Experimental design. Cues (circle, triangle) determined the possible outcome of trials in the two outcome conditions: social reward (SR) or monetary reward (MR). If in a reward trial (circle), the response to the target (square) was fast enough (hit), the participant was presented with a video of a woman showing signs of social approval (SR condition) or of money falling into a wallet (MR condition). Misses in reward trials resulted in neutral outcome videos (SR: neutral face/ MR: empty wallet). In control trials (triangle), both hits and misses resulted in seeing a control video (SR: woman with eyes closed and listening to music/MR: confetti falling into a wallet).

Fig. 2

Reaction times. Responses in hit trials were faster in the monetary than the social condition, and in response to reward cues relative to control cues (**P < 0.01). An interaction of ‘condition × cue type’ indicated that reaction time differences of reward and control cued trials were more pronounced for the SR than the MR condition.

Fig. 3

Mean rating (+ SEM) of subjectively perceived reward value of the outcome options ‘hit’, ‘miss’ and ‘control’ for both conditions for each group (high EQ = gray, low EQ = black). The interaction effect of ‘group × outcome’ [F(2, 66) = 3.54, P = 0.035 < 0.05] originates from a significantly different rating score between groups only for the miss videos [*P (two-sided) < 0.05].

Fig. 4

Interaction of ‘group × condition × cue type’ shows right NAcc reactivity for anticipated social reward vs. anticipated monetary reward between groups. (A) NAcc activation in ‘high-EQ vs. low-EQ, (social reward – social control) vs. (monetary reward – monetary control)’ axial, coronal and sagittal views [ROI-corrected, P (FWE) < 0.05]. (B) Parameter estimates derived from NAcc peak activation show significant differences between anticipation of social and monetary reward within and between groups (*P < 0.05).

Fig. 5

Contrasts of reward anticipation (vs. control) for the high-EQ (top) and the low-EQ (bottom) group on whole-brain level (P < 0.001, uncorrected).