Dopamine projections to the basolateral amygdala drive the encoding of identity-specific reward memories

Summary: Dopamine has long been known to critically contribute to learning. The canonical view is that midbrain dopamine neurons broadcast errors in reward prediction. These learning signals are thought to cache the general value of an outcome to its predictor and to reinforce response policies that rely on past success, rather than forethought of specific outcomes. But, to ensure flexible behavior, we do not just learn the general value of predictive events. We also encode the relationships between these cues and the identifying features of their associated outcomes. Such stimulus-outcome memories are fundamental components of the internal model of environmental relationships we use to generate the predictions and inferences needed for flexible, advantageous decision making. New data have challenged the value-centric dogma of dopamine function, indicating it plays a much broader role in learning than originally thought, including potentially supporting stimulus-outcome learning. Here we reveal a role for dopamine in forming detailed identity-specific stimulus-outcome memories and evaluate the pathway through which this occurs. Using fiber photometry, cell-type and pathway-specific bidirectional optogenetic manipulations, Pavlovian cue-reward conditioning, and a decision-making test in male and female rats, we show that ventral tegmental area dopamine (VTADA) neurons drive the encoding of stimulus-outcome memories through projections to the basolateral amygdala (BLA). Dopamine is released in the BLA during stimulus-outcome pairing and VTADA-->BLA activity is both necessary and sufficient to link the identifying features of a reward to a predictive cue, but does not mediate general value assignment or reinforcement. These data reveal a critical pathway through which dopamine mediates the encoding of identity-specific reward memories and, more broadly, suggest dopamine may support different forms of learning through its projections to diverse targets.