Centralized brain networks controlling antennal grooming coordination

Animals must coordinate their body parts to perform essential behaviors like grooming and locomotion. Here, we investigate the neural basis of body part coordination during antennal grooming in the fly, Drosophila melanogaster. Unilateral and bilateral grooming, targeting one or both antennae, respectively, arise from synchronized movements of the head, antennae, and forelegs. Replay of these kinematics in a biomechanical model suggests that coordination allows for unobstructed, forceful collisions between the foreleg tibiae and antennae, potentially increasing grooming efficiency. 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. An antennal grooming network from the brain connectome shows that centralized interneurons and shared premotor neurons interconnect and thus likely synchronize body part movements. A simulated activation screen of this network reveals that cell classes critical for coordination form coupled circuit motifs of recurrent excitation and broadcast inhibition, the latter of which we experimentally validate through manipulations of 'asteroid' broadcast inhibitory neurons during antennal grooming. Similarly centralized controllers may represent a general motif for the flexible co-recruitment of multiple body parts for a variety of behaviors.