Threat and Bidirectional Valence Signaling in the Nucleus Accumbens Core

Abstract

Appropriate responding to threat and reward is essential to survival. The nucleus accumbens core (NAcc) is known to support and organize reward behavior. The NAcc is also necessary to fully discriminate threat and safety cues. To directly reveal NAcc threat firing, we recorded single-unit activity from seven female rats undergoing pavlovian fear discrimination. Rats fully discriminated danger, uncertainty, and safety cues, and most NAcc neurons showed the greatest firing change to danger and uncertainty. Heterogeneity in cue and reward firing led us to identify distinct functional populations. One NAcc population signaled threat, specifically decreasing firing to danger and uncertainty cues. A separate population signaled Bidirectional Valence, decreasing firing to the danger cue (negative valence), but increasing firing to reward (positive valence). The results reveal the NAcc to be a source of threat information and a more general valence hub.SIGNIFICANCE STATEMENT The nucleus accumbens core (NAcc) is synonymous with reward. Yet, anatomy, neurotoxic lesions, and optogenetic manipulation implicate the NAcc in threat. Here, we directly revealed NAcc threat firing by recording single-unit activity during multicue fear discrimination. Most cue-responsive NAcc neurons markedly altered firing to threat cues. Finer analyses revealed a NAcc population signaling threat, specifically decreasing firing to danger and uncertainty cues; and a NAcc population signaling Bidirectional Valence, increasing firing to reward but decreasing firing to the danger cue. The results reveal the NAcc to be a source of threat information and a valence hub.

Keywords: associative learning; fear; single unit; ventral striatum.