Miniature linear and split-belt treadmills reveal mechanisms of adaptive motor control in walking Drosophila

Abstract

To navigate complex environments, walking animals must detect and overcome unexpected perturbations. One technical challenge when investigating adaptive locomotion is measuring behavioral responses to precise perturbations during naturalistic walking; another is that manipulating neural activity in sensorimotor circuits often reduces spontaneous locomotion. To overcome these obstacles, we introduce miniature treadmill systems for coercing locomotion and tracking 3D kinematics of walking Drosophila. By systematically comparing walking in three experimental setups, we show that flies compelled to walk on the linear treadmill have similar stepping kinematics to freely walking flies, while kinematics of tethered walking flies are subtly different. Genetically silencing mechanosensory neurons alters step kinematics of flies walking on the linear treadmill across all speeds, while inter-leg coordination remains intact. We also found that flies can maintain a forward heading on a split-belt treadmill by adapting the step distance of their middle legs. Overall, these new insights demonstrate the utility of miniature treadmills for studying insect locomotion.