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

Hongfei Ji,Bowen Yao,Zihao Li,Christopher Fang-Yen,Pilar Alvarez-Illera,Shelly Teng,Anthony D Fouad,Alice Liu

doi:10.7554/elife.69905

Abstract

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.

Highlights

Animal display locomotor behaviors such as crawling, walking, swimming, or flying via rhythmic patterns of muscle contractions and relaxations
We found that two important experimental findings, the nonsinusoidal free-moving dynamics and the sawtooth-shaped phase response curve (PRC) can be achieved in our original model, the van der
Our model can be compared to those previously described for C. elegans locomotion

Summary

Introduction

Animal display locomotor behaviors such as crawling, walking, swimming, or flying via rhythmic patterns of muscle contractions and relaxations. Isolated CPGs can produce outputs in the absence of sensory input, in the intact animal sensory feedback plays a critical role in coordinating motor rhythms across the body and modulating their characteristics (Friesen, 2009; Grillner and Wallen, 2002; Mullins et al, 2011; Pearson, 2004; Wen et al, 2012). In leeches (Cang et al, 2001; Cang and Friesen, 2000) and Drosophila (Akitake et al, 2015; Mendes et al, 2013), specialized proprioceptive neurons and sensory receptors in body muscles detect sensory inputs to regulate and coordinate the centrally generated motor patterns. Sensory inputs induced by electric stimulation of receptor cells (Yu and Friesen, 2004) or by mechanical perturbation of body segments (Grillner et al, 1981) can entrain an animal’s motor behavior to imposed patterns, demonstrating the flexibility of motor systems in responding to feedback. 2

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