Multiple Dopamine Systems: Weal and Woe of Dopamine

The ability to predict future outcomes increases the fitness of the animal. Decades of research have shown that dopamine neurons broadcast reward prediction error (RPE) signals-the discrepancy between actual and predicted reward-to drive learning to predict future outcomes. Recent studies have begun to show, however, that dopamine neurons are more diverse than previously thought. In this review, we will summarize a series of our studies that have shown unique properties of dopamine neurons projecting to the posterior "tail" of the striatum (TS) in terms of anatomy, activity, and function. Specifically, TS-projecting dopamine neurons are activated by a subset of negative events including threats from a novel object, send prediction errors for external threats, and reinforce avoidance behaviors. These results indicate that there are at least two axes of dopamine-mediated reinforcement learning in the brain-one learning from canonical RPEs and another learning from threat prediction errors. We argue that the existence of multiple learning systems is an adaptive strategy that makes possible each system optimized for its own needs. The compartmental organization in the mammalian striatum resembles that of a dopamine-recipient area in insects (mushroom body), pointing to a principle of dopamine function conserved across phyla.