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Flies Regulate Wing Motion via Active Control of a Dual-Function Gyroscope

Dickerson, Bradley H. and de Souza, Alysha M. and Huda, Ainul and Dickinson, Michael H. (2019) Flies Regulate Wing Motion via Active Control of a Dual-Function Gyroscope. Current Biology, 29 (20). pp. 3517-3524. ISSN 0960-9822. PMCID PMC7307274. https://resolver.caltech.edu/CaltechAUTHORS:20191010-123834351

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Abstract

Flies execute their remarkable aerial maneuvers using a set of wing steering muscles, which are activated at specific phases of the stroke cycle [1, 2, 3]. The activation phase of these muscles—which determines their biomechanical output [4, 5, 6]—arises via feedback from mechanoreceptors at the base of the wings and structures unique to flies called halteres [7, 8, 9]. Evolved from the hindwings, the tiny halteres oscillate at the same frequency as the wings, although they serve no aerodynamic function [10] and are thought to act as gyroscopes [10, 11, 12, 13, 14, 15]. Like the wings, halteres possess minute control muscles whose activity is modified by descending visual input [16], raising the possibility that flies control wing motion by adjusting the motor output of their halteres, although this hypothesis has never been directly tested. Here, using genetic techniques possible in Drosophila melanogaster, we tested the hypothesis that visual input during flight modulates haltere muscle activity and that this, in turn, alters the mechanosensory feedback that regulates the wing steering muscles. Our results suggest that rather than acting solely as a gyroscope to detect body rotation, halteres also function as an adjustable clock to set the spike timing of wing motor neurons, a specialized capability that evolved from the generic flight circuitry of their four-winged ancestors. In addition to demonstrating how the efferent control loop of a sensory structure regulates wing motion, our results provide insight into the selective scenario that gave rise to the evolution of halteres.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.cub.2019.08.065DOIArticle
https://doi.org/10.17632/kp9hbmxn47.1DOIData
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc7307274/PubMed CentralArticle
ORCID:
AuthorORCID
Huda, Ainul0000-0003-2073-6659
Dickinson, Michael H.0000-0002-8587-9936
Additional Information:© 2019 Elsevier Ltd. Received 24 June 2019, Revised 22 August 2019, Accepted 23 August 2019, Available online 10 October 2019. We thank Gwyneth Card, Erica Ehrhardt, and Wyatt Korff for sharing SS36076, SS41075, and SS43980. We also thank Anne von Philipsborn for providing us with UAS-Chrimson; VT22025-p65.ADZ VT29310-GAL4.DBD for the tp1-SG experiments. We are grateful to Thad Lindsay and Ivo Ros for help with setting up imaging experiments. This work was supported by grants from the NSF (DBI-1523434 to B.H.D.) and the NINDS-NIH (U01NS090514 and U19NS104655 to M.H.D.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Author Contributions: Conceptualization, B.H.D. and M.H.D.; Methodology, B.H.D., A.M.d.S., A.H., and M.H.D.; Investigation, B.H.D., A.M.d.S., and A.H.; Writing – Original Draft, B.H.D. and M.H.D.; Writing – Review & Editing, B.H.D. and M.H.D.; Funding Acquisition, B.H.D. and M.H.D.; Resources, M.H.D.; Supervision, M.H.D. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
NSFDBI-1523434
NIHU01NS090514
NIHU19NS104655
Subject Keywords:haltere; flight control; muscles; Drosophila
Issue or Number:20
PubMed Central ID:PMC7307274
Record Number:CaltechAUTHORS:20191010-123834351
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20191010-123834351
Official Citation:Bradley H. Dickerson, Alysha M. de Souza, Ainul Huda, Michael H. Dickinson, Flies Regulate Wing Motion via Active Control of a Dual-Function Gyroscope, Current Biology, Volume 29, Issue 20, 2019, Pages 3517-3524.e3, ISSN 0960-9822, https://doi.org/10.1016/j.cub.2019.08.065. (http://www.sciencedirect.com/science/article/pii/S0960982219311157)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:99214
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:10 Oct 2019 20:06
Last Modified:30 Jun 2020 22:27

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