A spinal circuit for collective coordination

Abstract

The coordinated movement of animal groups is one of the most widespread social behaviors, which are generally attributed to high-order cognitive processing in the brain. Yet, collective coordination can seemingly emerge from rapid, local interactions between individuals, suggesting the existence of decentralized mechanisms of online coordination that remain to be identified. Here, we show that a low-order spinal sensorimotor circuit is required for real-time social coordination during schooling in zebrafish. Central to this circuit are intraspinal proprioceptive neurons that detect local body bending and deliver direct, curvature-based inhibition to precisely time the locomotor network. Combining electrophysiology, calcium imaging, optogenetics, and behavioral analysis, we show that this circuit encodes both self-generated (egocentric) and neighbor-induced (allocentric) body bending signals, enabling fish to match the phase of their swimming to the wakes of their neighbors (vortex phase matching). In a neuromechanical model and physical robot, this single feedback loop is sufficient to generate vortex phase matching and to lower the energetic cost of swimming. Disrupting this circuit uncouples neighboring fish and abolishes schooling behavior. These results show that a spinal circuit dynamically synchronizes individuals through simple, local interactions, revealing how low-order mechanisms can drive the emergence of coordinated group behavior.