Different Kenyon Cell Populations Drive Learned Approach and Avoidance in Drosophila

In Drosophila, anatomically discrete dopamine neurons that innervate distinct zones of the mushroom body (MB) assign opposing valence to odors during olfactory learning. Subsets of MB neurons have temporally unique roles in memory processing, but valence-related organization has not been demonstrated. We functionally subdivided the alpha beta neurons, revealing a value-specific role for the similar to 160 alpha beta core (alpha beta(c)) neurons. Blocking neurotransmission from alpha beta surface (alpha beta(s)) neurons revealed a requirement during retrieval of aversive and appetitive memory, whereas blocking alpha beta(c) only impaired appetitive memory. The alpha beta(c) were also required to express memory in a differential aversive paradigm demonstrating a role in relative valuation and approach behavior. Strikingly, both reinforcing dopamine neurons and efferent pathways differentially innervate alpha beta(c) and alpha beta(s) in the MB lobes. We propose that conditioned approach requires pooling synaptic outputs from across the alpha beta ensemble but only from the alpha beta(s) for conditioned aversion.