Extrasynaptic signaling enables an asymmetric juvenile motor circuit to produce a symmetric mature gait.

Bilaterians generate motor patterns with symmetries that correspond to their body plans. This is thought to arise from wiring symmetries in their motor circuitries. We show that juvenile C. elegans larva has an asymmetrically wired motor circuit, but they still generate bending pattern with dorsal-ventral symmetry. In this juvenile circuit, wiring between excitatory and inhibitory motor neurons drives and coordinates contraction of dorsal muscles with relaxation of ventral muscles, producing dorsal bends. Ventral bending is not driven by its own circuitry. Instead, ventral muscles are excited uniformly by premotor interneurons through extrasynaptic signaling, and ventral bends occur in entrainment to the activity of motor neurons for dorsal bends. During maturation, the juvenile motor circuit is replaced by two homologous motor circuits that separately generate dorsal and ventral bending. Our modeling reveals that the juvenile circuit configuration provides an adequate solution for an immature motor circuit to drive functional gait long before the animal matures.