Cargando…

A spinal synergy of excitatory and inhibitory neurons coordinates ipsilateral body movements

Innate and goal-directed movements require a high-degree of trunk and appendicular muscle coordination to preserve body stability while ensuring the correct execution of the motor action. The spinal neural circuits underlying motor execution and postural stability are finely modulated by propriospin...

Descripción completa

Detalles Bibliográficos
Autores principales: Hayashi, Marito, Gullo, Miriam, Senturk, Gokhan, Di Costanzo, Stefania, Nagasaki, Shinji C., Kageyama, Ryoichiro, Imayoshi, Itaru, Goulding, Martyn, Pfaff, Samuel L., Gatto, Graziana
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10055247/
https://www.ncbi.nlm.nih.gov/pubmed/36993220
http://dx.doi.org/10.1101/2023.03.21.533603
_version_ 1785015844782211072
author Hayashi, Marito
Gullo, Miriam
Senturk, Gokhan
Di Costanzo, Stefania
Nagasaki, Shinji C.
Kageyama, Ryoichiro
Imayoshi, Itaru
Goulding, Martyn
Pfaff, Samuel L.
Gatto, Graziana
author_facet Hayashi, Marito
Gullo, Miriam
Senturk, Gokhan
Di Costanzo, Stefania
Nagasaki, Shinji C.
Kageyama, Ryoichiro
Imayoshi, Itaru
Goulding, Martyn
Pfaff, Samuel L.
Gatto, Graziana
author_sort Hayashi, Marito
collection PubMed
description Innate and goal-directed movements require a high-degree of trunk and appendicular muscle coordination to preserve body stability while ensuring the correct execution of the motor action. The spinal neural circuits underlying motor execution and postural stability are finely modulated by propriospinal, sensory and descending feedback, yet how distinct spinal neuron populations cooperate to control body stability and limb coordination remains unclear. Here, we identified a spinal microcircuit composed of V2 lineage-derived excitatory (V2a) and inhibitory (V2b) neurons that together coordinate ipsilateral body movements during locomotion. Inactivation of the entire V2 neuron lineage does not impair intralimb coordination but destabilizes body balance and ipsilateral limb coupling, causing mice to adopt a compensatory festinating gait and be unable to execute skilled locomotor tasks. Taken together our data suggest that during locomotion the excitatory V2a and inhibitory V2b neurons act antagonistically to control intralimb coordination, and synergistically to coordinate forelimb and hindlimb movements. Thus, we suggest a new circuit architecture, by which neurons with distinct neurotransmitter identities employ a dual-mode of operation, exerting either synergistic or opposing functions to control different facets of the same motor behavior.
format Online
Article
Text
id pubmed-10055247
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Cold Spring Harbor Laboratory
record_format MEDLINE/PubMed
spelling pubmed-100552472023-03-30 A spinal synergy of excitatory and inhibitory neurons coordinates ipsilateral body movements Hayashi, Marito Gullo, Miriam Senturk, Gokhan Di Costanzo, Stefania Nagasaki, Shinji C. Kageyama, Ryoichiro Imayoshi, Itaru Goulding, Martyn Pfaff, Samuel L. Gatto, Graziana bioRxiv Article Innate and goal-directed movements require a high-degree of trunk and appendicular muscle coordination to preserve body stability while ensuring the correct execution of the motor action. The spinal neural circuits underlying motor execution and postural stability are finely modulated by propriospinal, sensory and descending feedback, yet how distinct spinal neuron populations cooperate to control body stability and limb coordination remains unclear. Here, we identified a spinal microcircuit composed of V2 lineage-derived excitatory (V2a) and inhibitory (V2b) neurons that together coordinate ipsilateral body movements during locomotion. Inactivation of the entire V2 neuron lineage does not impair intralimb coordination but destabilizes body balance and ipsilateral limb coupling, causing mice to adopt a compensatory festinating gait and be unable to execute skilled locomotor tasks. Taken together our data suggest that during locomotion the excitatory V2a and inhibitory V2b neurons act antagonistically to control intralimb coordination, and synergistically to coordinate forelimb and hindlimb movements. Thus, we suggest a new circuit architecture, by which neurons with distinct neurotransmitter identities employ a dual-mode of operation, exerting either synergistic or opposing functions to control different facets of the same motor behavior. Cold Spring Harbor Laboratory 2023-03-21 /pmc/articles/PMC10055247/ /pubmed/36993220 http://dx.doi.org/10.1101/2023.03.21.533603 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Hayashi, Marito
Gullo, Miriam
Senturk, Gokhan
Di Costanzo, Stefania
Nagasaki, Shinji C.
Kageyama, Ryoichiro
Imayoshi, Itaru
Goulding, Martyn
Pfaff, Samuel L.
Gatto, Graziana
A spinal synergy of excitatory and inhibitory neurons coordinates ipsilateral body movements
title A spinal synergy of excitatory and inhibitory neurons coordinates ipsilateral body movements
title_full A spinal synergy of excitatory and inhibitory neurons coordinates ipsilateral body movements
title_fullStr A spinal synergy of excitatory and inhibitory neurons coordinates ipsilateral body movements
title_full_unstemmed A spinal synergy of excitatory and inhibitory neurons coordinates ipsilateral body movements
title_short A spinal synergy of excitatory and inhibitory neurons coordinates ipsilateral body movements
title_sort spinal synergy of excitatory and inhibitory neurons coordinates ipsilateral body movements
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10055247/
https://www.ncbi.nlm.nih.gov/pubmed/36993220
http://dx.doi.org/10.1101/2023.03.21.533603
work_keys_str_mv AT hayashimarito aspinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT gullomiriam aspinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT senturkgokhan aspinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT dicostanzostefania aspinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT nagasakishinjic aspinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT kageyamaryoichiro aspinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT imayoshiitaru aspinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT gouldingmartyn aspinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT pfaffsamuell aspinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT gattograziana aspinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT hayashimarito spinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT gullomiriam spinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT senturkgokhan spinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT dicostanzostefania spinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT nagasakishinjic spinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT kageyamaryoichiro spinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT imayoshiitaru spinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT gouldingmartyn spinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT pfaffsamuell spinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements
AT gattograziana spinalsynergyofexcitatoryandinhibitoryneuronscoordinatesipsilateralbodymovements