Flies Require Bilateral Sensory Input to Track Odor Gradients in Flight

Fruit flies make their living "on the fly" in search of attractive food odors. Flies balance the strength of self-induced bilateral visual motion and bilateral wind cues, but it is unknown whether they also use bilateral olfactory cues to track odors in flight. Tracking an odor gradient requires comparisons across spatially separated chemosensory organs and has been observed in several walking insects, including Drosophila. The olfactory antennae are separated by a fraction of a millimeter, and most sensory neurons project bilaterally and also symmetrically activate the first-order olfactory relay; both properties would seem to constrain the capacity for gradient tracking. Nevertheless, using a modified flight simulator that enables maneuvers in the yaw axis, we found that flies readily steer directly toward a laterally positioned odor plume. This capability is abolished by occluding sensory input to one antenna. Mechanosensory input from the Johnston's organ and olfactory input from the third antennal segment cooperate to direct small-angle yaw turns up the plume gradient. We additionally show that sensory signals from the left antenna contribute disproportionately more to odor tracking than signals from the right, providing further evidence of sensory lateralization in invertebrates.