Extrasynaptic signaling enables an asymmetric juvenile motor circuit to produce symmetric undulation

• DOI: 10.1016/j.cub.2022.09.002
• Publication Date: 2022-09-30T17:46:10Z
• Authors: Yangning Lu; Tosif Ahamed; Ben Mulcahy; Jun Meng; Daniel Witvliet; Sihui Asuka Guan; Douglas Holmyard; Wesley Hung; Quan Wen; Andrew D. Chisholm; Aravinthan D.T. S...; Mei Zhen
• Keywords: Life Sciences & Biomedicine - Other Topics; Motor Neurons; 0301 basic medicine; Biochemistry & Molecular Biology; Science & Technology; COMPLEX; C.-ELEGANS; COMPONENTS; Cell Biology; NEMATODE; RECEPTORS; GABA; 03 medical and health sciences; Interneurons; Larva; NEURAL CIRCUIT; Animals; VOLUME TRANSMISSION; CAENORHABDITIS-ELEGANS; Caenorhabditis elegans; Life Sciences & Biomedicine; Biology; Locomotion

SummaryIn many animals, there is a direct correspondence between the motor patterns that drive locomotion and the motor neuron innervation onto the muscle groups. For example, the adult C. elegans moves with symmetric and alternating dorsal-ventral bending waves arising from symmetric motor neuron input onto the dorsal and ventral muscles. In contrast to the adult, the C. elegans motor circuit at the juvenile larval stage has asymmetric wiring between motor neurons and muscles, but still generates adult-like bending waves with dorsal-ventral symmetry. We show that in the juvenile circuit, wiring between excitatory and inhibitory motor neurons coordinates the contraction of dorsal muscles with relaxation of ventral muscles, producing dorsal bends. However, ventral bending is not driven by analogous wiring. Instead, ventral muscles are excited uniformly by premotor interneurons through extrasynaptic signaling. Ventral bends occur in anti-phasic entrainment to activity of the same motor neurons that drive dorsal bends. During maturation, the juvenile motor circuit is replaced by two motor subcircuits that separately drive dorsal and ventral bending. Modeling reveals that the juvenile’s immature motor circuit is an adequate solution to generate adult-like dorsal-ventral bending before the animal matures. Developmental rewiring between functionally degenerate circuit solutions, that both generate symmetric bending patterns, minimizes behavioral disruption across maturation.HighlightsC. elegans larvae generate symmetric motor pattern with an asymmetrically wired motor circuit.Synaptic wiring between excitatory and inhibitory motor neurons drives dorsal bending.Extrasynaptic excitation by premotor interneurons entrains ventral muscles for anti-phasic ventral bending.A developmental strategy to enable mature motor pattern before the circuit structurally matures.