V1 and V2b interneurons secure the alternating flexor-extensor motor activity mice require for limbed locomotion

Jingming Zhang; Guillermo M. Lanuza; Olivier Britz; Zhi Wang; Valerie C. Siembab; Ying Zhang; Tomoko Velasquez; Francisco J. Alvarez; Eric Frank; Martyn Goulding

doi:10.1016/j.neuron.2014.02.013

V1 and V2b interneurons secure the alternating flexor-extensor motor activity mice require for limbed locomotion

Jingming Zhang, Guillermo M. Lanuza, Olivier Britz, Zhi Wang, Valerie C. Siembab, Ying Zhang, Tomoko Velasquez, Francisco J. Alvarez, Eric Frank, Martyn Goulding

Medicine

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

157 Citations (Scopus)

Abstract

Reciprocal activation of flexor and extensor muscles constitutes the fundamental mechanism that tetrapod vertebrates use for locomotion and limb-driven reflex behaviors. This aspect of motor coordination is controlled by inhibitory neurons in the spinal cord; however, the identity of the spinal interneurons that serve this function is not known. Here, we show that the production of an alternating flexor-extensor motor rhythm depends on the composite activities of two classes of ventrally located inhibitory neurons, V1 and V2b interneurons (INs). Abrogating V1 and V2b IN-derived neurotransmission in the isolated spinal cord results in a synchronous pattern of L2 flexor-related and L5 extensor-related locomotor activity. Mice lacking V1 and V2b inhibition are unable to articulate their limb joints and display marked deficits in limb-driven reflex movements. Taken together, these findings identify V1- and V2b-derived neurons as the core interneuronal components of the limb central pattern generator (CPG) that coordinate flexor-extensor motor activity.

Original language	English
Pages (from-to)	138-150
Number of pages	13
Journal	Neuron
Volume	82
Issue number	1
DOIs	https://doi.org/10.1016/j.neuron.2014.02.013
Publication status	Published - Apr 2 2014

Bibliographical note

Funding Information:
We would like to thank Simon Gosgnach for his early contribution to the analysis of the Pax6 mutant mice. We also thank Tom Jessell, Chris Kintner, Greg Lemke, John Thomas, Lidia Garcia-Campmany, and James Flynn for their thoughtful comments and criticisms. This research was supported by grants from the National Institutes of Health (R37-NS037075, P01-NS031249, R01-NS080586, and R01-NS047357), the Human Frontier Science Program, and the Christopher and Dana Reeve Foundation. G.M.L. was supported by an HFSP postdoctoral fellowship.

ASJC Scopus Subject Areas

General Neuroscience

PubMed: MeSH publication types

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

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10.1016/j.neuron.2014.02.013

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title = "V1 and V2b interneurons secure the alternating flexor-extensor motor activity mice require for limbed locomotion",

abstract = "Reciprocal activation of flexor and extensor muscles constitutes the fundamental mechanism that tetrapod vertebrates use for locomotion and limb-driven reflex behaviors. This aspect of motor coordination is controlled by inhibitory neurons in the spinal cord; however, the identity of the spinal interneurons that serve this function is not known. Here, we show that the production of an alternating flexor-extensor motor rhythm depends on the composite activities of two classes of ventrally located inhibitory neurons, V1 and V2b interneurons (INs). Abrogating V1 and V2b IN-derived neurotransmission in the isolated spinal cord results in a synchronous pattern of L2 flexor-related and L5 extensor-related locomotor activity. Mice lacking V1 and V2b inhibition are unable to articulate their limb joints and display marked deficits in limb-driven reflex movements. Taken together, these findings identify V1- and V2b-derived neurons as the core interneuronal components of the limb central pattern generator (CPG) that coordinate flexor-extensor motor activity.",

author = "Jingming Zhang and Lanuza, {Guillermo M.} and Olivier Britz and Zhi Wang and Siembab, {Valerie C.} and Ying Zhang and Tomoko Velasquez and Alvarez, {Francisco J.} and Eric Frank and Martyn Goulding",

note = "Funding Information: We would like to thank Simon Gosgnach for his early contribution to the analysis of the Pax6 mutant mice. We also thank Tom Jessell, Chris Kintner, Greg Lemke, John Thomas, Lidia Garcia-Campmany, and James Flynn for their thoughtful comments and criticisms. This research was supported by grants from the National Institutes of Health (R37-NS037075, P01-NS031249, R01-NS080586, and R01-NS047357), the Human Frontier Science Program, and the Christopher and Dana Reeve Foundation. G.M.L. was supported by an HFSP postdoctoral fellowship. ",

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AU - Wang, Zhi

AU - Siembab, Valerie C.

AU - Zhang, Ying

AU - Velasquez, Tomoko

AU - Alvarez, Francisco J.

AU - Frank, Eric

AU - Goulding, Martyn

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PY - 2014/4/2

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N2 - Reciprocal activation of flexor and extensor muscles constitutes the fundamental mechanism that tetrapod vertebrates use for locomotion and limb-driven reflex behaviors. This aspect of motor coordination is controlled by inhibitory neurons in the spinal cord; however, the identity of the spinal interneurons that serve this function is not known. Here, we show that the production of an alternating flexor-extensor motor rhythm depends on the composite activities of two classes of ventrally located inhibitory neurons, V1 and V2b interneurons (INs). Abrogating V1 and V2b IN-derived neurotransmission in the isolated spinal cord results in a synchronous pattern of L2 flexor-related and L5 extensor-related locomotor activity. Mice lacking V1 and V2b inhibition are unable to articulate their limb joints and display marked deficits in limb-driven reflex movements. Taken together, these findings identify V1- and V2b-derived neurons as the core interneuronal components of the limb central pattern generator (CPG) that coordinate flexor-extensor motor activity.

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V1 and V2b interneurons secure the alternating flexor-extensor motor activity mice require for limbed locomotion

Abstract

Bibliographical note

ASJC Scopus Subject Areas

PubMed: MeSH publication types

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