Miniature treadmills reveal proprioceptive mechanisms in walking Drosophila

Abstract

As animals navigate in an unpredictable and ever-changing world, their movement is bombarded by unanticipated perturbations. Proprioception, the sense of how the body is articulated and moving in space, enables animals to rapidly overcome these perturbations to avoid predators and to find mates, shelter, and food. However, it has been challenging to study the role of proprioception in adaptive movement because of the lack of tools to precisely perturb animal locomotion and the diminishment of spontaneous locomotion after manipulating proprioceptive neural circuits. To overcome these limitations, I engineered miniature treadmill systems for the genetic model organism, Drosophila melanogaster, that enable robust locomotion in flies lacking proprioceptive feedback, calibrated perturbations to walking, and quantifications of 3D walking kinematics. Using these systems, I found that proprioceptive feedback controls step kinematics across walking speeds, the middle legs of flies correct for asymmetric perturbations, and a class of proprioceptive neurons, called hair plates, facilitate the swing-to-stance transition, as predicted by the connectome. Overall, my dissertation work makes technical advances to reveal fundamental principles of how proprioception supports adaptive locomotion.