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The Drosophila fan-shaped body stores a vector in an allocentric coordinate system

Abstract

The nervous systems of animals perform computations that support adaptive behavior. In the case of insect navigation, a region of the insect brain, called the central complex, performs vector computations that facilitate the representation of space in a world-centered (allocentric) reference frame. While there is an in depth understanding of the anatomy of the central complex in the fruit fly, Drosophila melanogaster, the function of most of its cell types remains a mystery. I leveraged the theoretical framework of vector computation in combination with electron microscopy anatomy data to hypothesize a function for a previously uncharacterized cell type called PFL1. Specifically, I propose that it transforms a vector stored in the fly’s memory from an allocentric reference frame to an egocentric (fly-centered) reference frame. Through 2-photon functional imaging experiments, I show that PFL1’s input output relationship is consistent with this hypothesis. This finding leads me to investigate how the circuitry upstream of PFL1 encodes the stored vector. Via 2-color calcium imaging experiments where I simultaneously record from three cell types at once, I rule out a simple mechanism where the vector is encoded by the calcium activity of the presynaptic neurons, suggesting a more complex mechanism is at play. Through further imaging experiments, I find that a cell type called FC1 drives local second messenger signaling in the axons of another cell type called FB2B. These results build on our understanding of the fly’s navigational system and provide fundamental insights into the nature of neural computation.