Neurons in the Ventral Striatum Exhibit Cell-Type-Specific Representations of Outcome during Learning

The ventromedial striatum (VMS) is a node in circuits underpinning both affect and reinforcement learning. The cellular bases of these functions and especially their potential linkages have been unclear. VMS cholinergic interneurons, however, have been singled out as being related both to affect and to reinforcement-based conditioning, raising the possibility that unique aspects of their signaling could account for these functions. Here we show that VMS tonically active neurons (TANs), including putative cholinergic interneurons, generate unique bidirectional outcome responses during reward-based learning, reporting both positive (reward) and negative (reward omission) outcomes when behavioral change is prompted by switches in reinforcement contingencies. VMS output neurons (SPNs), by contrast, are nearly insensitive to switches in reinforcement contingencies, gradually losing outcome signaling while maintaining responses at trial initiation and goal approach. Thus, TANs and SPNs in the VMS provide distinct signals optimized for different aspects of the learning process. •Plasticity in ventromedial striatum during reward learning is cell-type specific•Cholinergic interneurons signal outcome and track reinforcement contingencies•Spiny projection neurons (SPNs) lose outcome responses during learning•SPNs maintain responses at trial initiation and goal approach during learning Atallah et al. demonstrate that in the ventromedial striatum, a region related to emotion, special sets of neurons signal the success or failure of behaviors as animals learn. After learning, this signal subsides, suggesting that it is a true learning signal.