A Dopamine-Gated Nucleus Accumbens Circuit for Cognitive Map Reification

Abstract

Animals navigate environment based on cognitive map built upon spatial cues and desired outcomes. However, how the goal representation stems from spatial information and outcomes, and its causal role in action control, remain elusive. Here we show that ‘where-to-escape’ relies on the cognitive map formulated by shelter experience. Dopamine (DA) neurons in the ventral tegmental area (VTA) exhibit valence encodings and the phasic burst stimulations of VTADA neurons sufficiently generate latent goal memory. Converging DA and excitatory inputs from VTA and hippocampus (HPC), respectively, onto the nucleus accumbens (NAc) is required for goal memory formation, integrating spatial value with the place. Tracking cellular dynamics of NAc neurons reveals emerging ensembles representing shelter positions. Targeting functionally-selective neuronal ensemble guides movements towards the goal location, regardless of the animal’s position. Thus, our findings reveal a neural basis of goal memory-to-action instantiation, demonstrating the feasibility of cognitive action tracing in space and time.