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Published March 14, 2022 | public
Journal Article Open

A population of descending neurons that regulates the flight motor of Drosophila


Similar to many insect species, Drosophila melanogaster is capable of maintaining a stable flight trajectory for periods lasting up to several hours. Because aerodynamic torque is roughly proportional to the fifth power of wing length, even small asymmetries in wing size require the maintenance of subtle bilateral differences in flapping motion to maintain a stable path. Flies can even fly straight after losing half of a wing, a feat they accomplish via very large, sustained kinematic changes to both the damaged and intact wings. Thus, the neural network responsible for stable flight must be capable of sustaining fine-scaled control over wing motion across a large dynamic range. In this study, we describe an unusual type of descending neuron (DNg02) that projects directly from visual output regions of the brain to the dorsal flight neuropil of the ventral nerve cord. Unlike many descending neurons, which exist as single bilateral pairs with unique morphology, there is a population of at least 15 DNg02 cell pairs with nearly identical shape. By optogenetically activating different numbers of DNg02 cells, we demonstrate that these neurons regulate wingbeat amplitude over a wide dynamic range via a population code. Using two-photon functional imaging, we show that DNg02 cells are responsive to visual motion during flight in a manner that would make them well suited to continuously regulate bilateral changes in wing kinematics. Collectively, we have identified a critical set of descending neurons that provides the sensitivity and dynamic range required for flight control.

Additional Information

© 2022 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). Received 5 August 2021, Revised 6 December 2021, Accepted 5 January 2022, Available online 31 January 2022. A portion of this work was conducted as part of the Descending Interneuron Project Team at Janelia Research Campus. We would like to thank the Janelia Visiting Science Program for hosting M.H.D., Gudrun Ihrke and the Project Technical Resources group for assistance in coordinating the screening, the Janelia FlyCore for assistance with animal preparations, and the Janelia FlyLight Project Team for providing additional anatomical images. Research reported in this publication was supported by the Howard Hughes Medical Institute (S.N., W.J.R., G.M.C., and W.K.) and the National Institute of Neurological Disorders and Stroke of the National Institutes of Health (I.G.R. and M.H.D.) under award U19NS104655. This article is subject to HHMI's Open Access to Publications policy. HHMI scientists have previously granted a nonexclusive CC BY 4.0 license to the public and a sublicensable license to HHMI in their research articles. Pursuant to those licenses, the author-accepted manuscript of this article can be made freely available under a CC BY 4.0 license immediately upon publication. Author contributions: (Following CRediT taxonomy): conceptualization—S.N., G.M.C., W.K., and M.H.D.; methodology—S.N., G.M.C., W.K., and M.H.D.; software—I.G.R. and W.J.R.; validation—W.J.R., C.M., W.K., G.M.C., I.G.R., and M.H.D.; formal analysis—S.N., I.G.R., C.M., W.J.R., W.K., and M.H.D.; investigation—S.N., I.G.R., and W.J.R.; resources—G.M.C., W.K., and M.H.D.; data curation—C.M., W.J.R., and I.G.R.; writing original draft—S.N. and M.H.D.; writing review and editing—W.K., G.M.C., I.G.R., and M.H.D.; visualization—S.N., I.G.R., C.M., W.K., and M.H.D.; funding acquisition—G.M.C., W.K., and M.H.D.; supervision—G.M.C., W.K., and M.H.D.; and project administration—G.M.C., W.K., and M.H.D. The authors declare no competing interests. Data and code availability: All data have been deposited on Mendeley at https://doi.org/10.17632/7g984jm2zc.1 and are publicly available as of the date of publication. The DOI is listed in the key resources table. All original code for data analysis has been deposited on Mendeley at https://doi.org/10.17632/7g984jm2zc.1 and is publicly available as of the date of publication. All original code used for the kinefly wing tracking software is publicly available on Github at https://github.com/ssafarik/Kinefly. The DOIs are listed in the key resources table. Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.

Attached Files

Published - 1-s2.0-S0960982222000197-main.pdf

Supplemental Material - 1-s2.0-S0960982222000197-mmc1.pdf

Submitted - 2021.08.05.455281v1.full.pdf


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August 22, 2023
September 11, 2023