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
© 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY). We thank T. Beatus for advice on data analysis techniques; A. von Phillipsborn, Y. Aso, G. Card, W. Korff, and E. Ehrhardt for providing reagents; J. Goldberg and J. Fetcho for guidance and support; M. Ramaswamy for general feedback; and the members of the Cohen Lab for myriad useful conversations. Furthermore, we are grateful to the Biotechnology Resource Center (BRC) at Cornell for the use of their imaging tools and the Cornell Statistical Consulting Unit (CSCU)—particularly L. Johnson—for assistance with statistical methods. Funding: This work was supported by the National Institute of Health (NINDS, 1R01NS116595), National Science Foundation [IOS 1546710 and IOS 1452510 (to M.H.D.) and IOS 1845673 (to T.S.)], Janelia Research Campus Visitor Project Program, Department of Defense (NDSEG Fellowship), Army Research Office (61651-EG), and Office of Naval Research [N00014-21-1-2431 (to N.J.C.)]. Author contributions: Conceptualization: S.C.W., I.C., T.S., and D.L.S. Methodology: S.C.W., I.C., T.S., D.L.S., N.Y., T.L., and M.H.D. Resources: S.C.W., I.C., N.Y., T.S., D.L.S., and M.H.D. Investigation: S.C.W., T.L., S.L., and M.R.M. Formal analysis: S.C.W. and N.J.C. Software: S.C.W. Visualization: S.C.W. Writing—original draft: S.C.W. and I.C. Writing—reviewing and editing: S.C.W., I.C., T.S., D.L.S., M.H.D., N.J.C., M.R.M., and N.Y. The authors declare that they have no competing interests.Attached Files
Published - sciadv.abo7461.pdf
Supplemental Material - sciadv.abo7461_movies_s1_to_s14.zip
Supplemental Material - sciadv.abo7461_sm.pdf
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Additional details
- PMCID
- PMC9750141
- Eprint ID
- 122528
- Resolver ID
- CaltechAUTHORS:20230725-706484000.38
- 1R01NS116595
- NIH
- IOS-1546710
- NSF
- IOS-1452510
- NSF
- IOS-1845673
- NSF
- Janelia Research Campus
- National Defense Science and Engineering Graduate (NDSEG) Fellowship
- 61651-EG
- Army Research Office (ARO)
- N00014-21-1-2431
- Office of Naval Research (ONR)
- Created
-
2023-08-11Created from EPrint's datestamp field
- Updated
-
2023-08-14Created from EPrint's last_modified field
- Caltech groups
- Division of Biology and Biological Engineering