Reward-related neural responses are dependent on the beneficiary

Abstract

Prior studies have suggested that positive social interactions are experienced as rewarding. Yet, it is not well understood how social relationships influence neural responses to other persons' gains. In this study, we investigated neural responses during a gambling task in which healthy participants (N = 31; 18 females) could win or lose money for themselves, their best friend or a disliked other (antagonist). At the moment of receiving outcome, person-related activity was observed in the dorsal medial prefrontal cortex (dmPFC), precuneus and temporal parietal junction (TPJ), showing higher activity for friends and antagonists than for self, and this activity was independent of outcome. The only region showing an interaction between the person-participants played for and outcome was the ventral striatum. Specifically, the striatum was more active following gains than losses for self and friends, whereas for the antagonist this pattern was reversed. Together, these results show that, in a context with social and reward information, social aspects are processed in brain regions associated with social cognition (mPFC, TPJ), and reward aspects are processed in primary reward areas (striatum). Furthermore, there is an interaction of social and reward information in the striatum, such that reward-related activity was dependent on social relationship.

Keywords: fMRI; reward processing; social relationships; striatum.

Fig. 1

Example of a trial. On trial onset, participants were presented with a screen for 4000 ms indicating for whom they were playing (Self, Friend or Antagonist) and how many coins could be won or lost. During this time, participants chose to play heads or tails by pressing the corresponding button. After a 1000 ms delay, trial outcome was presented for 1500 ms. Participants won when the computer randomly selected the same side of the coin as chosen by the participant.

Fig. 2

An ANOVA for Person, with levels Self, Friend and Antagonist, modeled at stimulus onset resulted in activation in (A) the right ventral striatum (peak voxel MNI 9, 15, 0) and (B) mPFC (peak voxel MNI −12, 42, −6) (P < 0.001, uncorrected for multiple comparisons, >10 contiguous voxels). Post hoc comparisons revealed that the striatum was more active when playing for Self and Friend, whereas the mPFC was selectively active when playing for Friend.

Fig. 3

(A) Brain regions showing a main effect of Person in the Person × Outcome ANOVA modeled at the onset of feedback presentation (P < 0.001, uncorrected for multiple comparisons, > 10 contiguous voxels). These regions included the left TPJ (MNI −48, −63, 39), precuneus (MNI −3, −60, 33) and the dorsal mPFC (MNI −9, 51, 36). Post hoc comparisons revealed more activation in these regions when receiving outcomes for Friend and Antagonist compared with receiving outcomes for Self, independent of the valence of the outcome. (B) Figure showing an interaction effect of Person × Outcome modeled at the onset of feedback presentation in the bilateral ventral striatum (MNI 15, 24, 0 and −12, 21, 0). Post hoc comparisons on ROIs derived from this contrast revealed that the ventral striatum was more active when receiving gain compared with loss for Self and for Friend, whereas for the Antagonist, this pattern was reversed, such that losses for the Antagonist resulted in more striatum activation compared with receiving gain.

Fig. 4

Correlation between neural responses to gains for Friend and losses for Antagonist in the right ventral striatum region (MNI 15, 24, 0) (Figure 3).