Phase response analyses support a relaxation oscillator model of locomotor rhythm generation in Caenorhabditis elegans

• DOI: 10.7554/elife.69905
• Publication Date: 2021-09-27T12:30:15Z
• Authors: Hongfei Ji; Anthony D Fouad; Shelly Teng; Alice Liu; Pilar Alvarez-Illera; Bowen Yao; Zihao Li; Christopher Fang-Yen
• Keywords: Periodicity; 0303 health sciences; QH301-705.5; Science; Q; motor circuit; R; modeling; Motor Activity; rhythm generation; locomotion; 03 medical and health sciences; Biological Clocks; Medicine; Animals; Biology (General); Caenorhabditis elegans; Locomotion; Computational and Systems Biology

Neural circuits coordinate with muscles and sensory feedback to generate motor behaviors appropriate to an animal’s environment. In C. elegans, the mechanisms by which the motor circuit generates undulations and modulates them based on the environment are largely unclear. We quantitatively analyzed C. elegans locomotion during free movement and during transient optogenetic muscle inhibition. Undulatory movements were highly asymmetrical with respect to the duration of bending and unbending during each cycle. Phase response curves induced by brief optogenetic inhibition of head muscles showed gradual increases and rapid decreases as a function of phase at which the perturbation was applied. A relaxation oscillator model based on proprioceptive thresholds that switch the active muscle moment was developed and is shown to quantitatively agree with data from free movement, phase responses, and previous results for gait adaptation to mechanical loadings. Our results suggest a neuromuscular mechanism underlying C. elegans motor pattern generation within a compact circuit.