Centralized brain networks underlie body part coordination during grooming

Abstract

Animals must coordinate multiple body parts to perform important tasks such as grooming, or locomotion. How this movement synchronization is achieved by the nervous system remains largely unknown. Here, we uncover the neural basis of body part coordination during goal-directed antennal grooming in the fly, Drosophila melanogaster. We find that unilateral or bilateral grooming of one or both antenna, respectively, arises from synchronized movements of the head, antennae, and forelegs. Simulated replay of these body part kinematics in a biomechanical model shows that this coordination makes grooming more efficient by permitting unobstructed, forceful collisions between the foreleg tibiae and antennae. Movements of one body part do not require proprioceptive sensory feedback from the others: neither amputation of the forelegs or antennae, nor immobilization of the head prevented movements of the other unperturbed body parts. By constructing a comprehensive antennal grooming network from the fly brain connectome, we find that centralized interneurons and shared premotor neurons interconnect and thus likely synchronize neck, antennal, and foreleg motor networks. A simulated activation screen of neurons in this network reveals cell classes required for the coordination of antennal movements during unilateral grooming. These cells form two coupled circuit motifs that enable robust body part synchronization: a recurrent excitatory subnetwork that promotes contralateral antennal pitch and broadcast inhibition that suppresses ipsilateral antennal pitch. Similarly centralized controllers may enable the flexible co-recruitment of multiple body parts to subserve a variety of behaviors.