Excitatory motor neurons are local oscillators for backward locomotion
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...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2018-01-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/29915 |
| _version_ | 1811252937321611264 |
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| author | 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 |
| author_facet | 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 |
| author_sort | Shangbang Gao |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-12T16:43:16Z |
| format | Article |
| id | doaj.art-62ecbf53feb54087bf1af93b53b2e2c4 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T16:43:16Z |
| publishDate | 2018-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-62ecbf53feb54087bf1af93b53b2e2c42022-12-22T03:24:42ZengeLife Sciences Publications LtdeLife2050-084X2018-01-01710.7554/eLife.29915Excitatory motor neurons are local oscillators for backward locomotionShangbang Gao0https://orcid.org/0000-0001-5431-4628Sihui Asuka Guan1Anthony D Fouad2Jun Meng3Taizo Kawano4Yung-Chi Huang5Yi Li6Salvador Alcaire7Wesley Hung8Yangning Lu9Yingchuan Billy Qi10https://orcid.org/0000-0002-4267-4770Yishi Jin11https://orcid.org/0000-0002-9371-9860Mark Alkema12Christopher Fang-Yen13https://orcid.org/0000-0002-4568-3218Mei Zhen14https://orcid.org/0000-0003-0086-9622Key Laboratory of Molecular Biophysics of the Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaLunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada; Department of Molecular Genetics, University of Toronto, Toronto, Canada; Department of Physiology, University of Toronto, Toronto, CanadaDepartment of Bioengineering, School of Engineering and Applied Science, University of Pennsylvania, Philadelphia, United StatesLunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada; Department of Molecular Genetics, University of Toronto, Toronto, Canada; Department of Physiology, University of Toronto, Toronto, CanadaLunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, CanadaDepartment of Neurobiology, University of Massachusetts Medical School, Worcester, United StatesKey Laboratory of Molecular Biophysics of the Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaLunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada; Department of Molecular Genetics, University of Toronto, Toronto, Canada; Department of Physiology, University of Toronto, Toronto, CanadaLunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, CanadaLunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada; Department of Molecular Genetics, University of Toronto, Toronto, Canada; Department of Physiology, University of Toronto, Toronto, CanadaNeurobiology Section, Division of Biological Sciences, University of California, San Diego, United StatesNeurobiology Section, Division of Biological Sciences, University of California, San Diego, United StatesDepartment of Neurobiology, University of Massachusetts Medical School, Worcester, United StatesDepartment of Bioengineering, School of Engineering and Applied Science, University of Pennsylvania, Philadelphia, United States; Department of Neuroscience, University of Pennsylvania, Philadelphia, United StatesLunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada; Department of Molecular Genetics, University of Toronto, Toronto, Canada; Department of Physiology, University of Toronto, Toronto, CanadaCell- 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.https://elifesciences.org/articles/29915motor neuronrhythmCentral Pattern Generator (CPG)locomotionC. elegansoscillation |
| spellingShingle | 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 Excitatory motor neurons are local oscillators for backward locomotion eLife motor neuron rhythm Central Pattern Generator (CPG) locomotion C. elegans oscillation |
| title | Excitatory motor neurons are local oscillators for backward locomotion |
| title_full | Excitatory motor neurons are local oscillators for backward locomotion |
| title_fullStr | Excitatory motor neurons are local oscillators for backward locomotion |
| title_full_unstemmed | Excitatory motor neurons are local oscillators for backward locomotion |
| title_short | Excitatory motor neurons are local oscillators for backward locomotion |
| title_sort | excitatory motor neurons are local oscillators for backward locomotion |
| topic | motor neuron rhythm Central Pattern Generator (CPG) locomotion C. elegans oscillation |
| url | https://elifesciences.org/articles/29915 |
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