Flying Drosophila stabilize their vision-based velocity controller by sensing wind with their antennae
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.
© 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.
Published - PNAS-2014-Fuller-E1182-91.pdf
Supplemental Material - pnas.201323529SI.pdf