Projection-defined functional characterization of dopamine activity
Animal behavior is controlled through the coordinated action of multiple learning systems in the brain. One of these systems, the basal ganglia, instantiates a reinforcement learning (RL) algorithm in which dopamine (DA) neurons transmit reward prediction error (RPE) signals—the difference between actual and expected rewards—to enable value learning via cortico-striatal plasticity. Recent studies have highlighted two novel aspects: first, that RPE signals from midbrain DA neurons can encode entire reward distributions through a distributional RL algorithm that mirrors cutting-edge machine learning approaches, and second, that dopamine axons projecting to different regions of the striatum exhibit functional heterogeneity, indicating that not all DA neurons encode RPE. To examine how distributional RL RPE signals are transmitted to the striatum and how these are anatomically organized in conjunction with non-RPE signals, we performed projection-identified electrophysiological recordings from midbrain DA neurons and conducted multi-fiber photometry recordings of dopamine axonal activity across the entire striatum. Our results suggest that RPE-encoding DA neurons project to the lateral nucleus accumbens shell (lAcbSh), and broadly across the striatum. Moreover, lAcbSh- and broadly-projecting DA neurons show structured RPE heterogeneity consistent with distributional RL predictions for a quantile-like population code. On the other hand non-RPE signals, such as threat and punishment, show heterogeneous activity across striatal regions.