Active antennal movements in Drosophila can tune wind encoding.

Insects use their antennae to smell odors,1,2 detect auditory cues,3,4 and sense mechanosensory stimuli such as wind5 and objects,6,7,8 frequently by combining sensory processing with active movements. Genetic access to antennal motor systems would therefore provide a powerful tool for dissecting the circuit mechanisms underlying active sensing, but little is known about how the most genetically tractable insect, Drosophila melanogaster, moves its antennae. Here, we use deep learning to measure how tethered Drosophila move their antennae in the presence of sensory stimuli and identify genetic reagents for controlling antennal movement. We find that flies perform both slow adaptive movements and fast flicking movements in response to wind-induced deflections, but not the attractive odor apple cider vinegar. Next, we describe four muscles in the first antennal segment that control antennal movements and identify genetic driver lines that provide access to two groups of antennal motor neurons and an antennal muscle. Through optogenetic inactivation, we provide evidence that antennal motor neurons contribute to active movements with different time courses. Finally, we show that activation of antennal motor neurons and muscles can adjust the gain and acuity of wind direction encoding by antennal displacement. Together, our experiments provide insight into the neural control of antennal movement and suggest that active antennal positioning in Drosophila may tune the precision of wind encoding.

A neural circuit for wind-guided olfactory navigation.

To navigate towards a food source, animals frequently combine odor cues about source identity with wind direction cues about source location. Where and how these two cues are integrated to support navigation is unclear. Here we describe a pathway to the Drosophila fan-shaped body that encodes attractive odor and promotes upwind navigation. We show that neurons throughout this pathway encode odor, but not wind direction. Using connectomics, we identify fan-shaped body local neurons called h∆C that receive input from this odor pathway and a previously described wind pathway. We show that h∆C neurons exhibit odor-gated, wind direction-tuned activity, that sparse activation of h∆C neurons promotes navigation in a reproducible direction, and that h∆C activity is required for persistent upwind orientation during odor. Based on connectome data, we develop a computational model showing how h∆C activity can promote navigation towards a goal such as an upwind odor source. Our results suggest that odor and wind cues are processed by separate pathways and integrated within the fan-shaped body to support goal-directed navigation.