A descending pathway through electrical coupling facilitates undulatory wave propagation in C. elegans

Descending signals from the brain play critical roles in controlling and modulating locomotion kinematics. The anatomical wiring diagram of the C. elegans nervous system suggests that the premotor interneurons AVB, the hub for sensorimotor transformation, make exclusively electrical synapses with the B-type motor neurons that activate body wall muscles and drive forward locomotion. Here, we combined genetic analysis, optogenetic manipulation, and computational modeling to elucidate the functions of AVB-B electrical couplings. First, we found that the B-type motor neurons could intrinsically generate rhythmic activity, constituting distributed center pattern generators. Second, AVB-B electrical couplings provide a descending pathway to drive bifurcation of motor neuron dynamics, triggering their transition from being stationary to generating rhythmic activity. Third, directional proprioceptive couplings between neighboring B-type motor neurons entrain the undulation frequency, forcing coherent bending waves to propagate along the body. Together, we propose that AVB-B electrical couplings work synergistically with proprioceptive couplings to enhance sequential activation of motor activity, and to facilitate the propagation of body undulation from head to tail during C. elegans forward locomotion.