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The role of a population of descending neurons in the optomotor response in flying Drosophila

Palmer, Emily H. and Omoto, Jaison J. and Dickinson, Michael H. (2022) The role of a population of descending neurons in the optomotor response in flying Drosophila. . (Unpublished)

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To maintain stable flight, animals continuously perform trimming adjustments to compensate for internal and external perturbations. Whereas animals use many different sensory modalities to detect such perturbations, insects rely extensively on optic flow to modify their motor output and remain on course. We studied this behavior in the fruit fly,Drosophila melanogaster, by exploiting the optomotor response, a robust reflex in which an animal steers so as to minimize the magnitude of rotatory optic flow it perceives. Whereas the behavioral and algorithmic structure of the optomotor response has been studied in great detail, its neural implementation is not well-understood. In this paper, we present findings implicating a group of nearly homomorphic descending neurons, the DNg02s, as a core component for the optomotor response in flyingDrosophila. Prior work on these cells suggested that they regulate the mechanical power to the flight system, presumably via connections to asynchronous flight motor neurons in the ventral nerve cord. When we chronically inactivated these cells, we observed that the magnitude of the optomotor response was diminished in proportion to the number of cells silenced, suggesting that the cells also regulate bilaterally asymmetric steering responses via population coding. During an optomotor response, flies coordinate changes in wing motion with movements of their head, abdomen, and hind legs, which are also diminished when the DNg02 cells are silenced. Using two-photon functional imaging, we show that the DNg02 cells respond most strongly to patterns of horizontal motion and that neuronal activity is closely correlated to motor output. However, unilateral optogenetic activation of DNg02 neurons does not elicit the asymmetric changes in wing motion characteristic of the optomotor response to a visual stimulus, but rather generates bilaterally symmetric increases in wingbeat amplitude. We interpret our experiments to suggest that flight maneuvers in flies require a more nuanced coordination of power muscles and steering muscles than previously appreciated, and that the physical flight apparatus of a fly might permit mechanical power to be distributed differentially between the two wings. Thus, whereas our experiments identify the DNg02 cells as a critical component of the optomotor reflex, our results suggest that other classes of descending cells targeting the steering muscle motor neurons are also required for the behavior.

Item Type:Report or Paper (Discussion Paper)
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URLURL TypeDescription Paper
Omoto, Jaison J.0000-0003-2032-6350
Dickinson, Michael H.0000-0002-8587-9936
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. We would like to thank all members of our lab for helpful discussions. In particular, we thank Will Dickson for building the laser cutter used for the functional imaging experiments. We also thank the Parker laboratory for confocal microscope access. Research reported in this publication was supported by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under Award U19NS104655. AUTHOR CONTRIBUTIONS. (Following CRediT taxonomy): conceptualization—E.H.P., J.J.O., and M.H.D.; investigation— E.H.P. and J.J.O.; resources—J.J.O.; visualization—E.H.P. and J.J.O.; methodology—E.H.P., J.J.O.; software—E.H.P., formal analysis—E.H.P.; validation—E.H.P., writing original draft—E.H.P., M.H.D.; writing review and editing—E.H.P., J.J.O., and M.H.D.; J.J.O.; data curation—E.H.P.; funding acquisition—M.H.D.; supervision—M.H.D.; project administration—M.H.D. The authors have declared no competing interest.
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Record Number:CaltechAUTHORS:20230316-182776000.59
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:120169
Deposited By: George Porter
Deposited On:17 Mar 2023 23:09
Last Modified:17 Mar 2023 23:09

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