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Published November 1, 2010 | Supplemental Material + Published
Journal Article Open

Olfactory modulation of flight in Drosophila is sensitive, selective and rapid

Abstract

Freely flying Drosophila melanogaster respond to odors by increasing their flight speed and turning upwind. Both these flight behaviors can be recapitulated in a tethered fly, which permits the odor stimulus to be precisely controlled. In this study, we investigated the relationship between these behaviors and odor-evoked activity in primary sensory neurons. First, we verified that these behaviors are abolished by mutations that silence olfactory receptor neurons (ORNs). We also found that antennal mechanosensors in Johnston's organ are required to guide upwind turns. Flight responses to an odor depend on the identity of the ORNs that are active, meaning that these behaviors involve odor discrimination and not just odor detection. Flight modulation can begin rapidly (within about 85 ms) after the onset of olfactory transduction. Moreover, just a handful of spikes in a single ORN type is sufficient to trigger these behaviors. Finally, we found that the upwind turn is triggered independently from the increase in wingbeat frequency, implying that ORN signals diverge to activate two independent and parallel motor commands. Together, our results show that odor-evoked flight modulations are rapid and sensitive responses to specific patterns of sensory neuron activity. This makes these behaviors a useful paradigm for studying the relationship between sensory neuron activity and behavioral decision-making in a simple and genetically tractable organism.

Additional Information

© 2010 Published by The Company of Biologists Ltd. Accepted 14 July 2010. First published online October 15, 2010. We thank K. I. Nagel for help in data acquisition, assistance in writing the image analysis software, and helpful conversations. We are grateful to members of the Wilson lab for feedback on the manuscript. This work was funded by a grant from the NIH (R01DC008174), a McKnight Scholar Award, a Sloan Foundation Research Fellowship, and a Beckman Young Investigator Award (to R.I.W.), together with a grant from the NSF (FIBR 0623527, to M.H.D.). V.B. was partially supported by Charles A. King Trust Postdoctoral Fellowship. G.M. was supported by a Caltech Della Martin Fellowship. R.I.W. is an HHMI Early Career Scientist. V.B. and R.I.W. designed the experiments. V.B. collected the data. Pilot experiments were performed by V.B. with assistance from G.M. in the laboratory of M.H.D. Both G.M. and M.H.D. provided technical support and intellectual contributions. V.B. and R.I.W. wrote the manuscript. Deposited in PMC for releaseafter 12 months.

Attached Files

Published - Bhandawat2010p11766J_Exp_Biol.pdf

Supplemental Material - Fig_S1.pdf

Supplemental Material - Fig_S2.pdf

Supplemental Material - Fig_S3.pdf

Supplemental Material - Fig_S4.pdf

Supplemental Material - Fig_S5.pdf

Supplemental Material - Fig_S6.pdf

Supplemental Material - Fig_S7.pdf

Supplemental Material - Fig_S8.pdf

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Additional details

Created:
August 22, 2023
Modified:
October 20, 2023