V3 Spinal Neurons Establish a Robust and Balanced Locomotor Rhythm during Walking

Ying Zhang; Sujatha Narayan; Eric Geiman; Guillermo M. Lanuza; Tomoko Velasquez; Bayle Shanks; Turgay Akay; Jason Dyck; Keir Pearson; Simon Gosgnach; Chen Ming Fan; Martyn Goulding

doi:10.1016/j.neuron.2008.09.027

V3 Spinal Neurons Establish a Robust and Balanced Locomotor Rhythm during Walking

Ying Zhang, Sujatha Narayan, Eric Geiman, Guillermo M. Lanuza, Tomoko Velasquez, Bayle Shanks, Turgay Akay, Jason Dyck, Keir Pearson, Simon Gosgnach, Chen Ming Fan, Martyn Goulding

Research output: Contribution to journal › Article › peer-review

263 Citations (Scopus)

Abstract

A robust and well-organized rhythm is a key feature of many neuronal networks, including those that regulate essential behaviors such as circadian rhythmogenesis, breathing, and locomotion. Here we show that excitatory V3-derived neurons are necessary for a robust and organized locomotor rhythm during walking. When V3-mediated neurotransmission is selectively blocked by the expression of the tetanus toxin light chain subunit (TeNT), the regularity and robustness of the locomotor rhythm is severely perturbed. A similar degeneration in the locomotor rhythm occurs when the excitability of V3-derived neurons is reduced acutely by ligand-induced activation of the allatostatin receptor. The V3-derived neurons additionally function to balance the locomotor output between both halves of the spinal cord, thereby ensuring a symmetrical pattern of locomotor activity during walking. We propose that the V3 neurons establish a regular and balanced motor rhythm by distributing excitatory drive between both halves of the spinal cord.

Original language	English
Pages (from-to)	84-96
Number of pages	13
Journal	Neuron
Volume	60
Issue number	1
DOIs	https://doi.org/10.1016/j.neuron.2008.09.027
Publication status	Published - Oct 9 2008
Externally published	Yes

Bibliographical note

Funding Information:
We thank Jean Rivier for the allatostatin peptide, Phil Soriano for Rosa26 lacZ mice, and Matsuya Yamamoto for the GFP-TeNT expression construct. PRV152 virus stocks were a gift from Lynn Enquist (Princeton). We would like to thank Drs. G. Lemke, C. Stevens, C. Kintner, J. Thomas, O. Britz, and F. Stam for their comments. This research was supported by grants from the National Institutes of Health (NS37075 and NS31249 to M.G. and HD35596 to C.-M. Fan) and the Human Frontiers Science Program (HFSP, M.G. and K.G.P.). G.M.L. was supported by an HFSP postdoctoral fellowship. E.G. was supported by an NIH NRSA fellowship.

ASJC Scopus Subject Areas

General Neuroscience

PubMed: MeSH publication types

Comparative Study
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

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10.1016/j.neuron.2008.09.027

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title = "V3 Spinal Neurons Establish a Robust and Balanced Locomotor Rhythm during Walking",

abstract = "A robust and well-organized rhythm is a key feature of many neuronal networks, including those that regulate essential behaviors such as circadian rhythmogenesis, breathing, and locomotion. Here we show that excitatory V3-derived neurons are necessary for a robust and organized locomotor rhythm during walking. When V3-mediated neurotransmission is selectively blocked by the expression of the tetanus toxin light chain subunit (TeNT), the regularity and robustness of the locomotor rhythm is severely perturbed. A similar degeneration in the locomotor rhythm occurs when the excitability of V3-derived neurons is reduced acutely by ligand-induced activation of the allatostatin receptor. The V3-derived neurons additionally function to balance the locomotor output between both halves of the spinal cord, thereby ensuring a symmetrical pattern of locomotor activity during walking. We propose that the V3 neurons establish a regular and balanced motor rhythm by distributing excitatory drive between both halves of the spinal cord.",

author = "Ying Zhang and Sujatha Narayan and Eric Geiman and Lanuza, {Guillermo M.} and Tomoko Velasquez and Bayle Shanks and Turgay Akay and Jason Dyck and Keir Pearson and Simon Gosgnach and Fan, {Chen Ming} and Martyn Goulding",

note = "Funding Information: We thank Jean Rivier for the allatostatin peptide, Phil Soriano for Rosa26 lacZ mice, and Matsuya Yamamoto for the GFP-TeNT expression construct. PRV152 virus stocks were a gift from Lynn Enquist (Princeton). We would like to thank Drs. G. Lemke, C. Stevens, C. Kintner, J. Thomas, O. Britz, and F. Stam for their comments. This research was supported by grants from the National Institutes of Health (NS37075 and NS31249 to M.G. and HD35596 to C.-M. Fan) and the Human Frontiers Science Program (HFSP, M.G. and K.G.P.). G.M.L. was supported by an HFSP postdoctoral fellowship. E.G. was supported by an NIH NRSA fellowship. ",

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AU - Geiman, Eric

AU - Lanuza, Guillermo M.

AU - Velasquez, Tomoko

AU - Shanks, Bayle

AU - Akay, Turgay

AU - Dyck, Jason

AU - Pearson, Keir

AU - Gosgnach, Simon

AU - Fan, Chen Ming

AU - Goulding, Martyn

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N2 - A robust and well-organized rhythm is a key feature of many neuronal networks, including those that regulate essential behaviors such as circadian rhythmogenesis, breathing, and locomotion. Here we show that excitatory V3-derived neurons are necessary for a robust and organized locomotor rhythm during walking. When V3-mediated neurotransmission is selectively blocked by the expression of the tetanus toxin light chain subunit (TeNT), the regularity and robustness of the locomotor rhythm is severely perturbed. A similar degeneration in the locomotor rhythm occurs when the excitability of V3-derived neurons is reduced acutely by ligand-induced activation of the allatostatin receptor. The V3-derived neurons additionally function to balance the locomotor output between both halves of the spinal cord, thereby ensuring a symmetrical pattern of locomotor activity during walking. We propose that the V3 neurons establish a regular and balanced motor rhythm by distributing excitatory drive between both halves of the spinal cord.

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V3 Spinal Neurons Establish a Robust and Balanced Locomotor Rhythm during Walking

Abstract

Bibliographical note

ASJC Scopus Subject Areas

PubMed: MeSH publication types

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