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Neuromuscular embodiment of feedback control elements in Drosophila flight

Whitehead, Samuel C. and Leone, Sofia and Lindsay, Theodore and Meiselman, Matthew R. and Cowan, Noah and Dickinson, Michael and Yapici, Nilay and Stern, David L. and Shirangi, Troy and Cohen, Itai (2022) Neuromuscular embodiment of feedback control elements in Drosophila flight. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20220228-619449000

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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.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2022.02.22.481344DOIDiscussion Paper
ORCID:
AuthorORCID
Whitehead, Samuel C.0000-0002-8170-1401
Lindsay, Theodore0000-0001-8550-5865
Meiselman, Matthew R.0000-0001-8655-743X
Cowan, Noah0000-0003-2502-3770
Dickinson, Michael0000-0002-8587-9936
Yapici, Nilay0000-0002-1130-5083
Stern, David L.0000-0002-1847-6483
Cohen, Itai0000-0001-9218-043X
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.
Funders:
Funding AgencyGrant Number
NIH1R01NS116595
NSFIOS-1546710
NSFIOS-1452510
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
National Defense Science and Engineering Graduate (NDSEG) FellowshipUNSPECIFIED
Army Research Office (ARO)61651-EG
Office of Naval Research (ONR)N00014-21-1-2431
DOI:10.1101/2022.02.22.481344
Record Number:CaltechAUTHORS:20220228-619449000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220228-619449000
Official Citation:Neuromuscular embodiment of feedback control elements in Drosophila flight. Samuel C. Whitehead, Sofia Leone, Theodore Lindsay, Matthew R. Meiselman, Noah Cowan, Michael Dickinson, Nilay Yapici, David L. Stern, Troy Shirangi, Itai Cohen. bioRxiv 2022.02.22.481344; doi: https://doi.org/10.1101/2022.02.22.481344
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:113624
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:01 Mar 2022 19:42
Last Modified:13 Apr 2022 16:21

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