Transforming representations of movement from body- to world-centric space

Abstract

When an animal moves through the world, its brain receives a stream of information about the body’s translational movement. These incoming movement signals, relayed from sensory organs or as copies of motor commands, are referenced relative to the body. Ultimately, such body-centric movement signals must be transformed into world-centric coordinates for navigation1. Here we show that this computation occurs in the fan-shaped body in the Drosophila brain. We identify two cell types in the fan-shaped body, PFNd and PFNv2,3, that conjunctively encode translational velocity signals and heading signals in walking flies. Specifically, PFNd and PFNv neurons form a Cartesian representation of body-centric translational velocity – acquired from premotor brain regions4,5 – that is layered onto a world-centric heading representation inherited from upstream compass neurons6–8. Then, we demonstrate that the next network layer, comprising hΔB neurons, is wired so as to transform the representation of translational velocity from body-centric to world-centric coordinates. We show that this transformation is predicted by a computational model derived directly from electron microscopy connectomic data9. The model illustrates the key role of a specific network motif, whereby the PFN neurons that synapse onto the same hΔB neuron have heading-tuning differences that offset the differences in their preferred body-centric directions of movement. By integrating a world-centric representation of travel velocity over time, it should be possible for the brain to form a working memory of the path traveled through the environment10–12.