The Structure of Motor Control Circuits in Adult Drosophila

Abstract

Animals’ nervous systems are able to coordinate contractions of dozens of muscles to smoothly navigate complex environments. Engineering animal-level mobility into robots is a major goal of current robotics research, but this has not yet been accomplished. A deeper understanding of how nervous systems control movement could facilitate reverse engineering of animals’ motor control algorithms. Here, we studied motor control in the adult fruit fly Drosophila melanogaster, a species that can perform fast, accurate, and flexible limb movements using a relatively compact nervous system. By developing high-throughput methods for performing X-ray microscopy and serial section electron microscopy on biological tissue, we imaged the fly’s legs and motor control circuits in 3D at synaptic resolution. To study the interactions between the nervous system and the limbs, we reconstructed the leg’s sensory organs, muscle fibers, tendons, and joints. We then reconstructed sensory neurons and motor neurons to comprehensively map the cell types that connect the nervous system to the legs. These reconstructions revealed that each of the fly’s six legs is controlled by 60 to 70 motor neurons. The majority of motor neurons have a unique dendritic branching pattern that is individually identifiable across left and right sides of the body and across animals. We identified a new class of large, bilaterally projecting sensory neurons and found that they synapse directly onto the motor neurons with the largest diameter axons, perhaps underlying a novel monosynaptic leg reflex. These structural datasets and reconstructions are made publicly available to serve as a resource for future studies of the fly’s motor control systems.