Functional imaging and connectome analyses reveal organizing principles of taste circuits in Drosophila

Taste is crucial for many innate and learned behaviors. In the fly, taste impacts feeding, oviposition, locomotion, mating, and memory formation, to name a few. These diverse roles may necessitate the apparent distributed nature of taste responses across different circuits in the fly brain, leading to complexity that has hindered attempts to deduce unifying principles of taste processing and coding. Here, we combine information from the whole brain connectome with functional calcium imaging to examine the neural representation of taste at early steps of processing. We find that the representation of taste quality remains largely segregated in cholinergic and GABAergic local interneurons (LNs) that are directly postsynaptic to taste sensory neurons of the labellum. Although some taste projection neurons (TPNs) projecting to superior protocerebrum receive direct inputs from sensory neurons, many receive primarily indirect taste inputs via cholinergic LNs. Moreover, we found that cholinergic interneurons appear to function as nodes to convey feedforward information to dedicated sets of morphologically similar TPNs. Examining a small number of representative TPNs suggests that taste information remains mostly segregated at this level as well. Together, these studies suggest a previously unappreciated logic in the organization of fly taste circuits.