Motor neurons generate pose-targeted movements via proprioceptive sculpting

Benjamin Gorko, Igor Siwanowicz, Kari Close, Christina Christoforou, Karen L. Hibbard, Mayank Kabra, Allen Lee, Jin-Yong Park, Si Ying Li, Alex B. Chen, Shigehiro Namiki, Chenghao Chen, John C. Tuthill, Davi D. Bock, Hervé Rouault, Kristin Branson, Gudrun Ihrke and Stephen J. Huston ()
Additional contact information
Benjamin Gorko: Howard Hughes Medical Institute
Igor Siwanowicz: Howard Hughes Medical Institute
Kari Close: Howard Hughes Medical Institute
Christina Christoforou: Howard Hughes Medical Institute
Karen L. Hibbard: Howard Hughes Medical Institute
Mayank Kabra: Howard Hughes Medical Institute
Allen Lee: Howard Hughes Medical Institute
Jin-Yong Park: Howard Hughes Medical Institute
Si Ying Li: Howard Hughes Medical Institute
Alex B. Chen: Howard Hughes Medical Institute
Shigehiro Namiki: Howard Hughes Medical Institute
Chenghao Chen: Howard Hughes Medical Institute
John C. Tuthill: University of Washington
Davi D. Bock: Howard Hughes Medical Institute
Hervé Rouault: Howard Hughes Medical Institute
Kristin Branson: Howard Hughes Medical Institute
Gudrun Ihrke: Howard Hughes Medical Institute
Stephen J. Huston: Howard Hughes Medical Institute

Nature, 2024, vol. 628, issue 8008, 596-603

Abstract: Abstract Motor neurons are the final common pathway1 through which the brain controls movement of the body, forming the basic elements from which all movement is composed. Yet how a single motor neuron contributes to control during natural movement remains unclear. Here we anatomically and functionally characterize the individual roles of the motor neurons that control head movement in the fly, Drosophila melanogaster. Counterintuitively, we find that activity in a single motor neuron rotates the head in different directions, depending on the starting posture of the head, such that the head converges towards a pose determined by the identity of the stimulated motor neuron. A feedback model predicts that this convergent behaviour results from motor neuron drive interacting with proprioceptive feedback. We identify and genetically2 suppress a single class of proprioceptive neuron3 that changes the motor neuron-induced convergence as predicted by the feedback model. These data suggest a framework for how the brain controls movements: instead of directly generating movement in a given direction by activating a fixed set of motor neurons, the brain controls movements by adding bias to a continuing proprioceptive–motor loop.

Date: 2024
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DOI: 10.1038/s41586-024-07222-5

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