Region-specific nucleus accumbens dopamine signals encode distinct aspects of avoidance learning

Abstract

Avoidance learning-learning to avoid bad outcomes-is an essential survival behavior. Dopamine signals are widely observed in response to aversive stimuli, indicating they could play a role in learning about how to avoid these stimuli.^1,2,3,4,5 However, it is unclear what computations dopamine signals perform to support avoidance learning. Furthermore, substantial heterogeneity in dopamine responses to aversive stimuli has been observed across nucleus accumbens (NAc) subregions.^3,6,7,8 To understand how heterogeneous dopamine responses to aversive stimuli contribute to avoidance learning, we recorded NAc core (Core) and NAc ventromedial shell (vmShell) dopamine during a task in which mice could avoid a footshock punishment by moving to the opposite side of a 2-chamber apparatus during a 5-s warning cue. Both signals evolved substantially-but differently-with learning. We found that Core and vmShell dopamine signals responded oppositely to shocks at the beginning of training and oppositely to warning cues as cue-shock associations developed in mid-training. Core dopamine responses strengthen with learning and are especially evident during expert performance. vmShell dopamine responses to cues and shocks were present during early learning but were not sustained during expert performance. Our data support a model in which Core dopamine encodes prediction errors that guide the consolidation of avoidance learning, while vmShell dopamine guides initial cue-shock associations by signaling aversive salience.

Keywords: dopamine heterogeneity; instrumental learning; negative reinforcement; nucleus accumbens; striatum; ventral tegmental area.