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 αβ neurons, revealing a value-specific role for the ∼160 αβ core (αβ(c)) neurons. Blocking neurotransmission from αβ surface (αβ(s)) neurons revealed a requirement during retrieval of aversive and appetitive memory, whereas blocking αβ(c) only impaired appetitive memory. The αβ(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 αβ(c) and αβ(s) in the MB lobes. We propose that conditioned approach requires pooling synaptic outputs from across the αβ ensemble but only from the αβ(s) for conditioned aversion.