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

Taste is crucial for many innate and learned behaviors. In the fruit fly, Drosophila melanogaster, taste impacts processes including feeding, oviposition, locomotion, mating, and memory formation. 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 majority of taste-responsive cells in the subesophageal zone (SEZ), including local interneurons (SEZ-LNs) and projection neurons (SEZ-PNs) targeting the superior protocerebrum, are predicted to encode a single taste modality. This prediction is borne out by calcium imaging of cholinergic and GABAergic cells in the SEZ, as well as five representative SEZ-PNs. Although the connectome reveals some SEZ-PNs receiving direct inputs from sensory neurons, many receive primarily indirect taste inputs via cholinergic SEZ-LNs. These cholinergic SEZ-LNs appear to function as nodes to convey feedforward information to dedicated sets of morphologically similar SEZ-PNs. Together, these studies suggest a previously unappreciated logic and structure to fly taste circuits.