Abstract

Coordinated rhythmic movements are ubiquitous in animal behavior. In many organisms, chains of neural oscillators underlie the generation of these rhythms. In C. elegans, locomotor wave generation has been poorly understood; in particular, it is unclear where in the circuit rhythms are generated, and whether there exists more than one such generator. We used optogenetic and ablation experiments to probe the nature of rhythm generation in the locomotor circuit. We found that multiple sections of forward locomotor circuitry are capable of independently generating rhythms. By perturbing different components of the motor circuit, we localize the source of secondary rhythms to cholinergic motor neurons in the midbody. Using rhythmic optogenetic perturbation, we demonstrate bidirectional entrainment of oscillations between different body regions. These results show that, as in many other vertebrates and invertebrates, the C. elegans motor circuit contains multiple oscillators that coordinate activity to generate behavior.

Highlights

  • Oscillatory neural activity underlies rhythmic animal behaviors such as feeding and locomotion

  • Rhythm generating units are sometimes functional in isolated spinal cord and invertebrate nerve cord preparations, producing fictive rhythmic motor outputs that resemble in vivo patterns (Marder and Calabrese, 1996; Marder et al, 2005; Kiehn, 2006; Mullins et al, 2011; Grillner and El Manira, 2015)

  • We found a fundamental architecture in the C. elegans motor circuit similar to that previously described in other vertebrate and invertebrate models

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Summary

Introduction

Oscillatory neural activity underlies rhythmic animal behaviors such as feeding and locomotion. Rhythm generating units are sometimes functional in isolated spinal cord and invertebrate nerve cord preparations, producing fictive rhythmic motor outputs that resemble in vivo patterns (Marder and Calabrese, 1996; Marder et al, 2005; Kiehn, 2006; Mullins et al, 2011; Grillner and El Manira, 2015). Network oscillators, and sensory feedback interact to enable rhythmic motor generation and coordination? Many components of the mammalian locomotor rhythm generator remain unidentified (Kiehn, 2006; Mullins et al, 2011; Kiehn, 2016). Work on vertebrate and invertebrate models, such as swimming leeches and lampreys, has allowed the basic principles and components of neural oscillators to be identified (Goulding, 2009; Mullins et al, 2011)

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