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Summary Fruit flies make their living on the fly in search of attractive food odors. To maintain forward flight, flies balance the strength of self-induced bilateral visual motion [1] and bilateral wind cues [2], but it is unknown whether they use bilateral olfactory cues to track odors in flight. Tracking an odor gradient requires comparisons across two spatially separated chemosensory organs and has been observed in several walking insects [3–5], including Drosophila [6]. The olfactory antennae are separated by a fraction of a millimeter, and most sensory neurons project bilaterally and symmetrically activate the first-order olfactory relay [7, 8], both of which would seem to constrain the capacity for bilateral sensory comparisons. Are fruit flies nonetheless able to track an odor gradient during flight? Using a modified flight simulator that enables maneuvers in the yaw axis [9], 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 the right, providing further evidence of sensory lateralization in invertebrates [10–13].

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Flies generate robust and high-performance olfactory and visual behaviors. Adult fruit flies can distinguish small differences in odor concentration across antennae separated by less than 1 mm [1], and a single olfactory sensory neuron is sufficient for near-normal gradient tracking in larvae [2]. During flight a male housefly chasing a female executes a corrective turn within 40 ms after a course deviation by its target [3]. The challenges imposed by flying apparently benefit from the tight integration of unimodal sensory cues. Crossmodal interactions reduce the discrimination threshold for unimodal memory retrieval by enhancing stimulus salience [4], and dynamic crossmodal processing is required for odor search during free flight because animals fail to locate an odor source in the absence of rich visual feedback [5]. The visual requirements for odor localization are unknown. We tethered a hungry fly in a magnetic field, allowing it to yaw freely, presented odor plumes, and examined how visual cues influence odor tracking. We show that flies are unable to use a small-field object or landmark to assist plume tracking, whereas odor activates wide-field optomotor course control to enable accurate orientation toward an attractive food odor.