The roles of feedback loops in the Caenorhabditis elegans rhythmic forward locomotion.

Abstract

Rhythmic behaviors are essential in biological systems, particularly in animal locomotion. The central pattern generator and sensory feedback loop mechanism have been instrumental in explaining many rhythmic locomotion patterns, however, it is insufficient to account for the tunability and robustness of frequency and amplitude in certain oscillatory movements. This suggests the involvement of additional, less understood circuit mechanisms. This study employs calcium imaging and neuromechanical modelling to investigate the circuit mechanism responsible for sinusoidal forward locomotion in Caenorhabditis elegans. We demonstrate that the feedback loop circuit, consisting of motoneurons and muscles, could govern the generation of oscillations and regulate rhythmic forward movement. This circuit is composed of both negative and positive feedback loops, which together regulate the turnability and robustness of oscillations. The oscillatory behavior of C. elegans typically involves a rhythmic alternation of dorsoventral muscles. Our neuromechanical model of the functional oscillatory unit reveals that asymmetric inputs from interneurons to motoneurons, and asymmetric connections from motoneurons to muscles, are essential for this switching mechanism. Our findings suggest that, besides the established roles of existed oscillator mechanisms, circuits formed by both negative and positive feedback loops contribute to the generation and robust modulation of rhythmic behaviors.