Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control

The spinal cord contains a diverse array of interneurons that govern motor output. Traditionally, models of spinal circuits have emphasized the role of inhibition in enforcing reciprocal alternation between left and right sides or flexors and extensors. However, recent work has shown that inhibition...

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Main Authors: Rebecca A Callahan, Richard Roberts, Mohini Sengupta, Yukiko Kimura, Shin-ichi Higashijima, Martha W Bagnall
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/47837
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author Rebecca A Callahan
Richard Roberts
Mohini Sengupta
Yukiko Kimura
Shin-ichi Higashijima
Martha W Bagnall
author_facet Rebecca A Callahan
Richard Roberts
Mohini Sengupta
Yukiko Kimura
Shin-ichi Higashijima
Martha W Bagnall
author_sort Rebecca A Callahan
collection DOAJ
description The spinal cord contains a diverse array of interneurons that govern motor output. Traditionally, models of spinal circuits have emphasized the role of inhibition in enforcing reciprocal alternation between left and right sides or flexors and extensors. However, recent work has shown that inhibition also increases coincident with excitation during contraction. Here, using larval zebrafish, we investigate the V2b (Gata3+) class of neurons, which contribute to flexor-extensor alternation but are otherwise poorly understood. Using newly generated transgenic lines we define two stable subclasses with distinct neurotransmitter and morphological properties. These V2b subclasses synapse directly onto motor neurons with differential targeting to speed-specific circuits. In vivo, optogenetic manipulation of V2b activity modulates locomotor frequency: suppressing V2b neurons elicits faster locomotion, whereas activating V2b neurons slows locomotion. We conclude that V2b neurons serve as a brake on axial motor circuits. Together, these results indicate a role for ipsilateral inhibition in speed control.
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spelling doaj.art-814e76c7bafb4d759b95f9b800a142262022-12-22T03:33:28ZengeLife Sciences Publications LtdeLife2050-084X2019-07-01810.7554/eLife.47837Spinal V2b neurons reveal a role for ipsilateral inhibition in speed controlRebecca A Callahan0Richard Roberts1Mohini Sengupta2https://orcid.org/0000-0002-5234-8258Yukiko Kimura3https://orcid.org/0000-0001-8381-8622Shin-ichi Higashijima4https://orcid.org/0000-0001-6350-4992Martha W Bagnall5https://orcid.org/0000-0003-2102-6165Department of Neuroscience, Washington University School of Medicine, St Louis, United StatesDepartment of Neuroscience, Washington University School of Medicine, St Louis, United StatesDepartment of Neuroscience, Washington University School of Medicine, St Louis, United StatesNational Institute for Basic Biology, Okazaki, JapanNational Institute for Basic Biology, Okazaki, JapanDepartment of Neuroscience, Washington University School of Medicine, St Louis, United StatesThe spinal cord contains a diverse array of interneurons that govern motor output. Traditionally, models of spinal circuits have emphasized the role of inhibition in enforcing reciprocal alternation between left and right sides or flexors and extensors. However, recent work has shown that inhibition also increases coincident with excitation during contraction. Here, using larval zebrafish, we investigate the V2b (Gata3+) class of neurons, which contribute to flexor-extensor alternation but are otherwise poorly understood. Using newly generated transgenic lines we define two stable subclasses with distinct neurotransmitter and morphological properties. These V2b subclasses synapse directly onto motor neurons with differential targeting to speed-specific circuits. In vivo, optogenetic manipulation of V2b activity modulates locomotor frequency: suppressing V2b neurons elicits faster locomotion, whereas activating V2b neurons slows locomotion. We conclude that V2b neurons serve as a brake on axial motor circuits. Together, these results indicate a role for ipsilateral inhibition in speed control.https://elifesciences.org/articles/47837spinal cordlocomotioncircuitryinhibition
spellingShingle Rebecca A Callahan
Richard Roberts
Mohini Sengupta
Yukiko Kimura
Shin-ichi Higashijima
Martha W Bagnall
Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control
eLife
spinal cord
locomotion
circuitry
inhibition
title Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control
title_full Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control
title_fullStr Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control
title_full_unstemmed Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control
title_short Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control
title_sort spinal v2b neurons reveal a role for ipsilateral inhibition in speed control
topic spinal cord
locomotion
circuitry
inhibition
url https://elifesciences.org/articles/47837
work_keys_str_mv AT rebeccaacallahan spinalv2bneuronsrevealaroleforipsilateralinhibitioninspeedcontrol
AT richardroberts spinalv2bneuronsrevealaroleforipsilateralinhibitioninspeedcontrol
AT mohinisengupta spinalv2bneuronsrevealaroleforipsilateralinhibitioninspeedcontrol
AT yukikokimura spinalv2bneuronsrevealaroleforipsilateralinhibitioninspeedcontrol
AT shinichihigashijima spinalv2bneuronsrevealaroleforipsilateralinhibitioninspeedcontrol
AT marthawbagnall spinalv2bneuronsrevealaroleforipsilateralinhibitioninspeedcontrol