Effects of oxytocin and prosocial behavior on brain responses to direct and vicariously experienced pain

Abstract

In this study, we tested the validity of 2 popular assumptions about empathy: (a) empathy can be enhanced by oxytocin, a neuropeptide known to be crucial in affiliative behavior, and (b) individual differences in prosocial behavior are positively associated with empathic brain responses. To do so, we measured brain activity in a double-blind placebo-controlled study of 20 male participants either receiving painful stimulation to their own hand (self condition) or observing their female partner receiving painful stimulation to her hand (other condition). Prosocial behavior was measured using a monetary economic interaction game with which participants classified as prosocial (N = 12) or selfish (N = 6), depending on whether they cooperated with another player. Empathy-relevant brain activation (anterior insula) was neither enhanced by oxytocin nor positively associated with prosocial behavior. However, oxytocin reduced amygdala activation when participants received painful stimulation themselves (in the nonsocial condition). Surprisingly, this effect was driven by "selfish" participants. The results suggest that selfish individuals may not be as rational and unemotional as usually suggested, their actions being determined by their feeling anxious rather than by reason.

Figure 1. Subjective unpleasantness ratings: Average unpleasantness ratings for the conditions self (green) and other (red), placebo (filled), and oxytocin (shaded) with error bars (SEM), * p < .01.

Figure 2. Empathic brain responses: Activation in the right anterior insula (AI) revealed by conjunction analyses depicting shared activation in painful versus nonpainful trials in the self and other placebo condition. Threshold is set at p < .001, uncorrected.

Figure 3. Individual differences in empathic brain responses: (A) Correlation of parameter estimates in the anterior insula/operculum for (pain vs. no pain) in the placebo other condition and subjective unpleasantness ratings. (B) Activation revealed in anterior insula/operculum for the contrast (pain vs. no pain) in the placebo other condition (red) and for the regression analysis of unpleasantness ratings on the contrast (pain vs. no pain) in the placebo other condition (yellow). Threshold is set at p < .001, uncorrected.

Figure 4. Effects of oxytocin and types on amygdala: The bar diagram illustrates parameter estimates derived from the right amygdala (21, −3, 18) revealed in the three-way interaction (pain, drug, prosociality) in self. Contrast estimates on the contrast (pain vs. no pain) are shown for the self (green) and the other (red) in the placebo (filled), and oxytocin (shaded) conditions, separately for prosocial and selfish participants. Threshold is set at p < .001, uncorrected.