Inhibitory control of locomotor statistics in walking Drosophila

Abstract

In order to forage for food, many animals regulate not only specific limb movements but the statistics of locomotor behavior over time, switching between long-range dispersal and localized search depending on resource availability. How pre-motor circuits regulate such locomotor statistics is not clear. Here we analyze and model locomotor statistics in walking Drosophila, and their modulation by attractive food odor. Odor evokes three motor regimes in flies: baseline walking, upwind running during odor, and search behavior following odor loss. During search behavior, we find that flies adopt higher angular velocities and slower ground speeds, and tend to turn for longer periods of time in one direction. We further find that flies spontaneously adopt periods of different mean ground speed, and that these changes in state influence the length of odor-evoked runs. We next developed a simple model of neural locomotor control that suggests that contralateral inhibition plays a key role in regulating the statistical features of locomotion. As the fly connectome predicts decussating inhibitory neurons in the lateral accessory lobe (LAL), a pre-motor structure, we gained genetic access to a subset of these neurons and tested their effects on behavior. We identified one population of neurons whose activation induces all three signature of search and that bi-directionally regulates angular velocity at odor offset. We identified a second group of neurons, including a single LAL neuron pair, that bi-directionally regulate ground speed. Together, our work develops a biologically plausible computational architecture that captures the statistical features of fly locomotion across behavioral states and identifies potential neural substrates of these computations.