Plume-Tracking Behavior of Flying Drosophila Emerges from a Set of Distinct Sensory-Motor Reflexes
Background: For a fruit fly, locating fermenting fruit where it can feed, find mates, and lay eggs is an essential and difficult task requiring the integration of olfactory and visual cues. Here, we develop an approach to correlate flies' free-flight behavior with their olfactory experience under different wind and visual conditions, yielding new insight into plume tracking based on over 70 hr of data. Results: To localize an odor source, flies exhibit three iterative, independent, reflex-driven behaviors, which remain constant through repeated encounters of the same stimulus: (1) 190 ± 75 ms after encountering a plume, flies increase their flight speed and turn upwind, using visual cues to determine wind direction. Due to this substantial response delay, flies pass through the plume shortly after entering it. (2) 450 ± 165 ms after losing the plume, flies initiate a series of vertical and horizontal casts, using visual cues to maintain a crosswind heading. (3) After sensing an attractive odor, flies exhibit an enhanced attraction to small visual features, which increases their probability of finding the plume's source. Conclusions: Due to plume structure and sensory-motor delays, a fly's olfactory experience during foraging flights consists of short bursts of odor stimulation. As a consequence, delays in the onset of crosswind casting and the increased attraction to visual features are necessary behavioral components for efficiently locating an odor source. Our results provide a quantitative behavioral background for elucidating the neural basis of plume tracking using genetic and physiological approaches.
© 2014 Elsevier Ltd. Received: October 28, 2013; Revised: November 25, 2013; Accepted: December 11, 2013; Published: January 16, 2014. The authors wish to thank Jeff Riffell for many helpful comments and advice on this work. Andrew Straw provided help with use of the fly-tracking system. This work was supported by grants from the National Science Foundation (0623527), the Air Force Office of Scientific Research (FA9550-10-1-0368), and the Paul G. Allen Family Foundation (to M.H.D.) and graduate training fellowships from The Hertz Foundation and The National Science Foundation (to F.v.B.).
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