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. 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. 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 five-second warning cue. We found that NAc Core and vmShell dopamine signals responded oppositely during shocks and warning cues. Both signals evolved substantially - but differently - with learning. NAc vmShell dopamine responses to cues and shocks were present during early learning but not sustained during expert performance. NAc Core dopamine responses strengthen with learning and are especially evident during expert performance. Our data support a model in which NAc vmShell dopamine guides initial cue-shock associations by signaling salience, while NAc Core dopamine encodes prediction errors that guide the consolidation of avoidance learning.