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Published March 1, 2022 | Submitted + Supplemental Material
Report Open

Neuromuscular embodiment of feedback control elements in Drosophila flight

Abstract

While insects like Drosophila are flying, aerodynamic instabilities require that they make millisecond-timescale adjustments to their wing motion to stay aloft and on course. These stabilization reflexes can be modeled as a proportional-integral (PI) controller; however, it is unclear how such control might be instantiated in insects at the level of muscles and neurons. Here, we show that the b1 and b2 motor units—prominent components of the fly's steering muscles system—modulate specific elements of the PI controller: the angular displacement (integral, I) and angular velocity (proportional, P), respectively. Moreover, these effects are observed only during the stabilization of pitch. Our results provide evidence for an organizational principle in which each muscle contributes to a specific functional role in flight control, a finding that highlights the power of using top-down behavioral modeling to guide bottom-up cellular manipulation studies.

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 4.0 International license. Version 1: February 24, 2022; Version 2: March 7, 2022; Version 3: April 11, 2022. We thank Tsevi Beatus for advice on data analysis techniques; Anne von Phillipsborn, Yoshi Aso, Gwyneth Card, Wyatt Korff, and Erica Ehrhardt for providing reagents; Jesse Goldberg and Joe Fetcho for guidance and support; Meera Ramaswamy for general feedback; and the members of the Cohen Lab for myriad useful conversations. Further, we are grateful to the Biotechnology Resource Center (BRC) at Cornell for the use of their imaging tools, as well as the Cornell Statistical Consulting Unit (CSCU)—particularly Lynn Johnson—for assistance with statistical methods. This work was supported by: National Institute of Health (NINDS, 1R01NS116595); National Science Foundation (IOS, 1546710; IOS 1452510 (to M.H.D)); Janelia Research Campus Visitor Project Program; Department of Defense (NDSEG Fellowship); Army Research Office (61651-EG); Office of Naval Research (N00014-21-1-2431 (to NJC)). Author contributions statement: Conceptualization: SCW, IC, TS, DS; Methodology: SCW, IC, TS, DS, NY, TL, MD; Resources: SCW, IC, NY, TS, DS, MD; Investigation: SCW, TL, SL, MM; Formal Analysis: SCW, NC; Software: SCW; Visualization: SCW; Writing – original draft: SCW, IC; Writing – reviewing and editing: SCW, IC, TS, DS, MD, NC, MM, NY. The authors declare that they have no financial or other competing interests. Processed data and code will be available through Cornell University Library's institutional repository, eCommons. Raw high-speed video data is available upon request.

Attached Files

Submitted - 2022.02.22.481344v2.full.pdf

Submitted - 2022.02.22.481344v3.full.pdf

Supplemental Material - media-1.mp4

Supplemental Material - media-10.mp4

Supplemental Material - media-11.mp4

Supplemental Material - media-12.mp4

Supplemental Material - media-13.mp4

Supplemental Material - media-14.mp4

Supplemental Material - media-2.mp4

Supplemental Material - media-3.mp4

Supplemental Material - media-4.mp4

Supplemental Material - media-5.mp4

Supplemental Material - media-6.mp4

Supplemental Material - media-7.mp4

Supplemental Material - media-8.mp4

Supplemental Material - media-9.mp4

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Additional details

Created:
August 20, 2023
Modified:
December 22, 2023