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...
Autores principales: | , , , , , , , , , |
---|---|
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 |