Dual roles of Drosophila reward-encoding dopamine neurons in regulating innate and learned behaviors

Dopaminergic neurons (DANs) play a key role in learning the value of cues that predict reward. The fruit fly Drosophila has provided a powerful model to dissect the mechanisms by which reward-encoding DANs mediate reward learning. However, the role of these DANs in regulating innate behaviors is less clear. Here, we show that activating the entire population of reward-encoding DANs in Drosophila drives acute aversion in multiple behavioral assays, including feeding, locomotion, and spatial preference, even as these neurons confer a positive value onto associated cues to promote future learned attraction. Activating subsets of DANs reveals that the effects on innate and learned behaviors are dissociable. Based on the known circuitry, it is likely that immediate aversion and learned attraction mediated by DANs arise from distinct effects - direct activation versus synaptic plasticity - on the same target neurons. These results reveal distinct roles for reward-encoding DANs in guiding immediate and future behavior.