A premotor connectome reveals circuits for rapid, flexible, and precise wing control in Drosophila

Abstract

The nerve cord processes information from sensory systems and controls muscles. Thesecomputations are implemented by neural circuits: networks of neurons with synapses between them. This project seeks to gain insight into features of neural circuit organization that allow an animal to rapidly respond to a changing environment. Even a fly, which has a fraction of the number of neurons as a human, has neural circuits that give rise to highly precise control of muscles informed by complex sensory inputs. This precision is especially important when a fly is in flight, as the animal actively controls its path by making small adjustments in muscles that controls the wings. To gain insight into the anatomical circuits that coordinate flight, we reconstructed neurons in sensorimotor circuits that control the wing. We identified muscle targets of all the wing motor neurons, analyzed the synaptic weights between premotor neurons and motor neurons, and mapped sensory axons to the structures on the wing that they innervate. By analyzing wing circuitry alongside leg circuitry in the same animal, we found evidence that premotor circuit organization is dictated by the biomechanical properties of the joint it controls. This project demonstrates that the synaptic structure of sensorimotor circuits can vary even within the same animal. We propose that the specific circuit architectures we observe correspond to the biomechanical constraints of different types of joints. By analyzing circuits at the level of single neurons and synapses, this work seeks to expand our understanding of the many ways sensorimotor circuits can be organized.