Descending pathway facilitates undulatory wave propagation in <i>Caenorhabditis elegans</i> through gap junctions

Abstract

Descending signals from the brain play critical roles in controlling and modulating locomotion kinematics. In the <i>Caenorhabditis elegans</i> nervous system, descending AVB premotor interneurons exclusively form gap junctions with the B-type motor neurons that execute forward locomotion. We combined genetic analysis, optogenetic manipulation, calcium imaging, and computational modeling to elucidate the function of AVB-B gap junctions during forward locomotion. First, we found that some B-type motor neurons generate rhythmic activity, constituting distributed oscillators. Second, AVB premotor interneurons use their electric inputs to drive bifurcation of B-type motor neuron dynamics, triggering their transition from stationary to oscillatory activity. Third, proprioceptive couplings between neighboring B-type motor neurons entrain the frequency of body oscillators, forcing coherent bending wave propagation. Despite substantial anatomical differences between the motor circuits of <i>C. elegans</i> and higher model organisms, converging principles govern coordinated locomotion.