Distributed rhythm generators underlie Caenorhabditis elegans forward locomotion

Anthony D. Fouad, Shelly Teng, Julian R. Mark, Alice Liu, Pilar Alvarez-Illera, Hongfei Ji, Angelica Du, Priya D. Bhirgoo, Eli Cornblath, Sihui Asuka Guan, Christopher Fang-Yen

Research output: Contribution to journalArticlepeer-review

46 Citations (Scopus)

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.

Original languageEnglish
Article numbere29913
JournaleLife
Volume7
DOIs
Publication statusPublished - 2018 Jan 23

Bibliographical note

Funding Information:
We thank Mei Zhen, Quan Wen, Min Wu, Michelle Po, Yishi Jin, Andres Villu Mariq, and Alexander Gottschalk for providing strains. Some strains were provided by the by the CGC, which is funded by NIH Office of Research Infrastructure Programs (P40 OD010440). CF-Y was supported by the National Institutes of Health, Ellison Medical Foundation, and Sloan Research Foundation. ADF was supported by the National Institutes of Health. ST was supported by an Abraham Noordergraaf Research Fellowship and a Littlejohn Fellowship. JRM was supported by a Holtz Undergraduate Research Fellowship. We thank Mei Zhen, Michael Nusbaum, David Raizen, Vijay Balasubramanian, Robert Kalb, Gal Haspel, Brian Chow, and Edward Fouad for helpful suggestions and discussions, Matthew Churgin for technical assistance, and Wassana Techadilok for assistance with figure preparation.

Publisher Copyright:
© Fouad et al.

ASJC Scopus subject areas

  • General Neuroscience
  • General Biochemistry,Genetics and Molecular Biology
  • General Immunology and Microbiology

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