Excitatory motor neurons are local oscillators for backward locomotion

Shangbang Gao, Sihui Asuka Guan, Anthony D. Fouad, Jun Meng, Taizo Kawano, Yung Chi Huang, Yi Li, Salvador Alcaire, Wesley Hung, Yangning Lu, Yingchuan Billy Qi, Yishi Jin, Mark Alkema, Christopher Fang-Yen, Mei Zhen

Research output: Contribution to journalArticle

20 Citations (Scopus)

Abstract

Cell- or network-driven oscillators underlie motor rhythmicity. The identity of C. elegans oscillators remains unknown. Through cell ablation, electrophysiology, and calcium imaging, we show: (1) forward and backward locomotion is driven by different oscillators; (2) the cholinergic and excitatory A-class motor neurons exhibit intrinsic and oscillatory activity that is sufficient to drive backward locomotion in the absence of premotor interneurons; (3) the UNC-2 P/Q/N high-voltage-activated calcium current underlies A motor neuron’s oscillation; (4) descending premotor interneurons AVA, via an evolutionarily conserved, mixed gap junction and chemical synapse configuration, exert state-dependent inhibition and potentiation of A motor neuron’s intrinsic activity to regulate backward locomotion. Thus, motor neurons themselves derive rhythms, which are dually regulated by the descending interneurons to control the reversal motor state. These and previous findings exemplify compression: essential circuit properties are conserved but executed by fewer numbers and layers of neurons in a small locomotor network.

Original languageEnglish
Article numbere29915
JournaleLife
Volume7
DOIs
Publication statusPublished - 2018 Jan 23
Externally publishedYes

Fingerprint

Motor Neurons
Locomotion
Neurons
Interneurons
Calcium
Electrophysiology
Gap Junctions
Periodicity
Synapses
Cholinergic Agents
Ablation
Imaging techniques
Networks (circuits)
Electric potential

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)

Cite this

Gao, S., Guan, S. A., Fouad, A. D., Meng, J., Kawano, T., Huang, Y. C., ... Zhen, M. (2018). Excitatory motor neurons are local oscillators for backward locomotion. eLife, 7, [e29915]. https://doi.org/10.7554/eLife.29915

Excitatory motor neurons are local oscillators for backward locomotion. / Gao, Shangbang; Guan, Sihui Asuka; Fouad, Anthony D.; Meng, Jun; Kawano, Taizo; Huang, Yung Chi; Li, Yi; Alcaire, Salvador; Hung, Wesley; Lu, Yangning; Qi, Yingchuan Billy; Jin, Yishi; Alkema, Mark; Fang-Yen, Christopher; Zhen, Mei.

In: eLife, Vol. 7, e29915, 23.01.2018.

Research output: Contribution to journalArticle

Gao, S, Guan, SA, Fouad, AD, Meng, J, Kawano, T, Huang, YC, Li, Y, Alcaire, S, Hung, W, Lu, Y, Qi, YB, Jin, Y, Alkema, M, Fang-Yen, C & Zhen, M 2018, 'Excitatory motor neurons are local oscillators for backward locomotion', eLife, vol. 7, e29915. https://doi.org/10.7554/eLife.29915
Gao S, Guan SA, Fouad AD, Meng J, Kawano T, Huang YC et al. Excitatory motor neurons are local oscillators for backward locomotion. eLife. 2018 Jan 23;7. e29915. https://doi.org/10.7554/eLife.29915
Gao, Shangbang ; Guan, Sihui Asuka ; Fouad, Anthony D. ; Meng, Jun ; Kawano, Taizo ; Huang, Yung Chi ; Li, Yi ; Alcaire, Salvador ; Hung, Wesley ; Lu, Yangning ; Qi, Yingchuan Billy ; Jin, Yishi ; Alkema, Mark ; Fang-Yen, Christopher ; Zhen, Mei. / Excitatory motor neurons are local oscillators for backward locomotion. In: eLife. 2018 ; Vol. 7.
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