Nucleus accumbens core single cell ensembles bidirectionally respond to experienced versus observed aversive events

Abstract

SummaryEmpathy is the ability to adopt others’ sensory and emotional states and is an evolutionarily conserved trait among mammals. In rodents, empathy manifests itself as social modulation of aversive stimuli such as acknowledging and acting on conspecifics’ distress. The neuronal network underlying social transmission of information is known to overlap with the brain regions that mediate behavioral responses to aversive and rewarding stimuli. In this study, we recorded single cell activity patterns of nucleus accumbens (NAc) core neurons using in vivo optical imaging of calcium transients via miniature scopes. This cutting-edge imaging methodology not only allows us to record activity patterns of individual neurons but also lets us longitudinally follow these individual neurons across time and different behavioral states. Using this approach, we identified NAc core single cell ensembles that respond to experienced and/or observed aversive stimuli. Our results showed that experienced and observed aversive stimuli evoke NAc core ensemble activity that is largely positive, with a smaller subset of negative responses. The size of the NAc single cell ensemble response was greater for experienced aversive stimuli compared to observed aversive events. Our results also revealed a subpopulation within the NAc core single cell ensembles that show a bidirectional response to experienced aversive stimuli versus observed aversive stimuli (i.e., negative response to experienced and positive response to observed). These results suggest that the NAc plays a role in differentiating somatosensory experience from social observation of aversion at a single cell level. This has important implications for psychopathologies where social information processing is maladaptive, such as autism spectrum disorders.