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

Jenny Lu, Amir H. Behbahani, Lydia Hamburg, Elena A. Westeinde, Paul M. Dawson, Cheng Lyu, Gaby Maimon, Michael H. Dickinson, Shaul Druckmann and Rachel I. Wilson ()
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Jenny Lu: Harvard Medical School
Amir H. Behbahani: California Institute of Technology
Lydia Hamburg: Stanford University
Elena A. Westeinde: Harvard Medical School
Paul M. Dawson: Harvard Medical School
Cheng Lyu: The Rockefeller University
Gaby Maimon: The Rockefeller University
Michael H. Dickinson: California Institute of Technology
Shaul Druckmann: Stanford University
Rachel I. Wilson: Harvard Medical School

Nature, 2022, vol. 601, issue 7891, 98-104

Abstract: Abstract When an animal moves through the world, its brain receives a stream of information about the body’s translational velocity from motor commands and sensory feedback signals. These incoming signals are referenced to the body, but ultimately, they must be transformed into world-centric coordinates for navigation1,2. Here we show that this computation occurs in the fan-shaped body in the brain of Drosophila melanogaster. We identify two cell types, PFNd and PFNv3–5, that conjunctively encode translational velocity and heading as a fly walks. In these cells, velocity signals are acquired from locomotor brain regions6 and are multiplied with heading signals from the compass system. PFNd neurons prefer forward–ipsilateral movement, whereas PFNv neurons prefer backward–contralateral movement, and perturbing PFNd neurons disrupts idiothetic path integration in walking flies7. Downstream, PFNd and PFNv neurons converge onto hΔB neurons, with a connectivity pattern that pools together heading and translation direction combinations corresponding to the same movement in world-centric space. This network motif effectively performs a rotation of the brain’s representation of body-centric translational velocity according to the current heading direction. Consistent with our predictions, we observe that hΔB neurons form a representation of translational velocity in world-centric coordinates. By integrating this representation over time, it should be possible for the brain to form a working memory of the path travelled through the environment8–10.

Date: 2022
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DOI: 10.1038/s41586-021-04191-x

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