Flies Require Bilateral Sensory Input to Track Odor Gradients in Flight

Abstract

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].

Behavior Reveals Selective Summation and Max Pooling among Olfactory Processing Channels

“…One strategy is to turn upwind upon encountering an odor, because odors disperse downwind from the source. Previous studies have shown that Drosophila tend to fly or walk upwind in response to odor (Bhandawat et al, 2010; Budick and Dickinson, 2006; Duistermars et al, 2009; Steck et al, 2012; Thoma et al, 2014; van Breugel and Dickinson, 2014). Whereas flying insects must use visual cues to estimate wind direction from their own self-motion, walking insects can use mechanosensory cues to estimate wind direction (Bell and Kramer, 1979).…”

Whole-Brain Calcium Imaging Reveals an Intrinsic Functional Network in Drosophila

“…The FB also responds to a wide range of visual stimuli during flight, suggesting that it plays a role in flight motor control[23]. As olfactory cues can also direct flight, in addition to visual feedback[24, 25], the observed strong functional connections with the MB may reflect the FB’s role in integrating multimodal signals to control flight. Conversely, the AVLP, which has been shown to be involved in auditory processing[26], shows very low correlations with other auditory regions, such as the AMMC, and instead is highly correlated with its homolog, suggesting additional roles for these regions.…”

Use of bilateral information to determine the walking direction during orientation to a pheromone source in the silkmoth Bombyx mori

“…Two antennae are required to facilitate odor localization in insects (Bell and Tobin 1981;Borst and Heisenberg 1982;Louis et al 2008;Duistermars et al 2009;Steck et al 2010). Furthermore, bilateral information is also employed in robot odor localization (Webster et al 2001).…”