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Flying Drosophila stabilize their vision-based velocity controller by sensing wind with their antennae

Fuller, Sawyer Buckminster and Straw, Andrew D. and Peek, Martin Y. and Murray, Richard M. and Dickinson, Michael H. (2014) Flying Drosophila stabilize their vision-based velocity controller by sensing wind with their antennae. Proceedings of the National Academy of Sciences of the United States of America, 111 (13). E1182-E1191. ISSN 0027-8424. PMCID PMC3977237. https://resolver.caltech.edu/CaltechAUTHORS:20140502-103349067

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Abstract

Flies and other insects use vision to regulate their groundspeed in flight, enabling them to fly in varying wind conditions. Compared with mechanosensory modalities, however, vision requires a long processing delay (~100 ms) that might introduce instability if operated at high gain. Flies also sense air motion with their antennae, but how this is used in flight control is unknown. We manipulated the antennal function of fruit flies by ablating their aristae, forcing them to rely on vision alone to regulate groundspeed. Arista-ablated flies in flight exhibited significantly greater groundspeed variability than intact flies. We then subjected them to a series of controlled impulsive wind gusts delivered by an air piston and experimentally manipulated antennae and visual feedback. The results show that an antenna-mediated response alters wing motion to cause flies to accelerate in the same direction as the gust. This response opposes flying into a headwind, but flies regularly fly upwind. To resolve this discrepancy, we obtained a dynamic model of the fly’s velocity regulator by fitting parameters of candidate models to our experimental data. The model suggests that the groundspeed variability of arista-ablated flies is the result of unstable feedback oscillations caused by the delay and high gain of visual feedback. The antenna response drives active damping with a shorter delay (~20 ms) to stabilize this regulator, in exchange for increasing the effect of rapid wind disturbances. This provides insight into flies’ multimodal sensory feedback architecture and constitutes a previously unknown role for the antennae.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1323529111 DOIArticle
http://www.pnas.org/content/111/13/E1182PublisherArticle
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1323529111/-/DCSupplementalPublisherSupplemental material
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3977237/PubMed CentralArticle
ORCID:
AuthorORCID
Straw, Andrew D.0000-0001-8381-0858
Murray, Richard M.0000-0002-5785-7481
Dickinson, Michael H.0000-0002-8587-9936
Additional Information:© 2014 National Academy of Sciences. Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved February 20, 2014 (received for review December 18, 2013). Published online before print March 17, 2014. The authors thank Matthias Wittlinger for help constructing the apparatus and Michael Elzinga, Robert Engle, K. Rhett Nichols, and Katharina Reinecke for helpful comments regarding the manuscript. Also, thanks to Patrice Engle, in memoriam, for the laughter. This work was supported by the Institute for Collaborative Biotechnologies through Grant DAAD19-03-D-0004 from the US Army Research Office and by a National Science Foundation Graduate Fellowship (to S.B.F.). Author contributions: S.B.F., A.D.S., R.M.M., and M.H.D. designed research; S.B.F. and M.Y.P. performed research; S.B.F. and A.D.S. contributed new reagents/analytic tools; S.B.F. analyzed data; and S.B.F. and M.H.D. wrote the paper. The authors declare no conflict of interest.
Funders:
Funding AgencyGrant Number
Army Research Office (ARO)DAAD19-03-D-0004
NSF Graduate Research FellowshipUNSPECIFIED
Subject Keywords:stability; sensory fusion; feedback delay; system identification; turbulence
Issue or Number:13
PubMed Central ID:PMC3977237
Record Number:CaltechAUTHORS:20140502-103349067
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20140502-103349067
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:45467
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:02 May 2014 18:38
Last Modified:03 Oct 2019 06:31

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