Sticking the landing: leg mechanosensory feedback coordinates the transition from flight to landing

Abstract

Landing is an especially demanding stage of flight. Flying animals must rapidly transform multimodal sensory information into the coordinated movement of multiple limbs in order to transition from flight to a stable standing posture, often on surfaces that vary in stability, texture, and orientation. Failure to do so can be costly, leading to injury or death. Here, we examine the role of mechanosensory feedback in guiding landing in the fruit fly, Drosophila melanogaster. We describe a novel behavioral assay in which we deliver localized mechanical contact to individual legs of tethered, flying flies while simultaneously quantifying their three-dimensional behavioral kinematics. We find that mechanical contact of the distal legs reliably induces flight cessation, and initial leg contact triggers distinct patterns of inter-leg coordination. Recruitment of subsequent leg contacts predicts landing likelihood, suggesting that coordinated feedback from multiple legs reinforces the landing transition. Next, we combine synapse-resolution connectomes with optogenetic manipulations to identify the mechanosensory pathways underlying these behaviors. Finally, we describe a population of inhibitory ascending neurons that integrates mechanosensory input from the legs and facilitates the transition from visually-mediated landing initiation to touch-mediated flight cessation. Overall, our results reveal an important set of neural circuits that convert local tactile feedback into a coordinated, rapid behavioral state transition.