Dissociation between the processing of humorous and monetary rewards in the ‘motivation’ and ‘hedonic’ brains

Humor elicits feelings of amusement and can be thought of as a social reward. We identified distinct mesolimbic reward system (MRS) processing patterns for monetary and humorous rewards. During both the reward anticipation and outcome phases, the nucleus accumbens (NAc) and anterior cingulate cortex (ACC) were active in response to monetary cues and monetary gains, while the amygdala and midbrain showed a differential response to humorous rewards, apparently driven by the hedonic enjoyment and appreciation of humor consumption. Psychophysiological interaction analysis (PPI) further demonstrated the functional coupling of the amygdala-midbrain circuit in response to humorous gains during the reward outcome phase, while neural signaling was observed in the NAc-ACC circuit during both the reward anticipation and outcome phases in response to monetary rewards. This is consistent with a view in which the NAc plays a key role in the ‘motivation brain’, and the amygdala in the ‘hedonic brain’. The findings further suggest that the neural mechanisms underlying reward consumption are more modality-specific than those underlying reward anticipation. Our study contributes to a growing understanding of neural responses to social rewards and represent an important first step toward understanding the neural processing of humor as one significant type of social reward.