Observation of Reward Delivery to a Conspecific Modulates Dopamine Release in Ventral Striatum

Abstract

Dopamine (DA) neurons increase and decrease firing for rewards that are better and worse than expected, respectively. These correlates have been observed at the level of single-unit firing and in measurements of phasic DA release in ventral striatum (VS). Here, we ask whether DA release is modulated by delivery of reward, not to oneself, but to a conspecific. It is unknown what, if anything, DA release encodes during social situations in which one animal witnesses another animal receive reward. It might be predicted that DA release will increase, suggesting that watching a conspecific receive reward is a favorable outcome. Conversely, DA release may be entirely dependent on personal experience, or perhaps observation of receipt of reward might be experienced as a negative outcome because another individual, rather than oneself, receives the reward. Our data show that animals display a mixture of affective states during observation of conspecific reward, first exhibiting increases in appetitive calls (50 kHz), then exhibiting increases in aversive calls (22 kHz). Like ultrasonic vocalizations (USVs), DA signals were modulated by delivery of reward to the conspecific. We show stronger DA release during observation of the conspecific receiving reward relative to observation of reward delivered to an empty box, but only on the first trial. During the following trials, this relationship reversed: DA release was reduced during observation of the conspecific receiving reward. These findings suggest that positive and negative states associated with conspecific reward delivery modulate DA signals related to learning in social situations.