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A GABAergic and peptidergic sleep neuron as a locomotion stop neuron with compartmentalized Ca2+ dynamics

Animals must slow or halt locomotion to integrate sensory inputs or to change direction. In Caenorhabditis elegans, the GABAergic and peptidergic neuron RIS mediates developmentally timed quiescence. Here, we show RIS functions additionally as a locomotion stop neuron. RIS optogenetic stimulation ca...

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Autores principales: Steuer Costa, Wagner, Van der Auwera, Petrus, Glock, Caspar, Liewald, Jana F., Bach, Maximilian, Schüler, Christina, Wabnig, Sebastian, Oranth, Alexandra, Masurat, Florentin, Bringmann, Henrik, Schoofs, Liliane, Stelzer, Ernst H. K., Fischer, Sabine C., Gottschalk, Alexander
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6736843/
https://www.ncbi.nlm.nih.gov/pubmed/31506439
http://dx.doi.org/10.1038/s41467-019-12098-5
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author Steuer Costa, Wagner
Van der Auwera, Petrus
Glock, Caspar
Liewald, Jana F.
Bach, Maximilian
Schüler, Christina
Wabnig, Sebastian
Oranth, Alexandra
Masurat, Florentin
Bringmann, Henrik
Schoofs, Liliane
Stelzer, Ernst H. K.
Fischer, Sabine C.
Gottschalk, Alexander
author_facet Steuer Costa, Wagner
Van der Auwera, Petrus
Glock, Caspar
Liewald, Jana F.
Bach, Maximilian
Schüler, Christina
Wabnig, Sebastian
Oranth, Alexandra
Masurat, Florentin
Bringmann, Henrik
Schoofs, Liliane
Stelzer, Ernst H. K.
Fischer, Sabine C.
Gottschalk, Alexander
author_sort Steuer Costa, Wagner
collection PubMed
description Animals must slow or halt locomotion to integrate sensory inputs or to change direction. In Caenorhabditis elegans, the GABAergic and peptidergic neuron RIS mediates developmentally timed quiescence. Here, we show RIS functions additionally as a locomotion stop neuron. RIS optogenetic stimulation caused acute and persistent inhibition of locomotion and pharyngeal pumping, phenotypes requiring FLP-11 neuropeptides and GABA. RIS photoactivation allows the animal to maintain its body posture by sustaining muscle tone, yet inactivating motor neuron oscillatory activity. During locomotion, RIS axonal Ca2+ signals revealed functional compartmentalization: Activity in the nerve ring process correlated with locomotion stop, while activity in a branch correlated with induced reversals. GABA was required to induce, and FLP-11 neuropeptides were required to sustain locomotion stop. RIS attenuates neuronal activity and inhibits movement, possibly enabling sensory integration and decision making, and exemplifies dual use of one cell across development in a compact nervous system.
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spelling pubmed-67368432019-09-12 A GABAergic and peptidergic sleep neuron as a locomotion stop neuron with compartmentalized Ca2+ dynamics Steuer Costa, Wagner Van der Auwera, Petrus Glock, Caspar Liewald, Jana F. Bach, Maximilian Schüler, Christina Wabnig, Sebastian Oranth, Alexandra Masurat, Florentin Bringmann, Henrik Schoofs, Liliane Stelzer, Ernst H. K. Fischer, Sabine C. Gottschalk, Alexander Nat Commun Article Animals must slow or halt locomotion to integrate sensory inputs or to change direction. In Caenorhabditis elegans, the GABAergic and peptidergic neuron RIS mediates developmentally timed quiescence. Here, we show RIS functions additionally as a locomotion stop neuron. RIS optogenetic stimulation caused acute and persistent inhibition of locomotion and pharyngeal pumping, phenotypes requiring FLP-11 neuropeptides and GABA. RIS photoactivation allows the animal to maintain its body posture by sustaining muscle tone, yet inactivating motor neuron oscillatory activity. During locomotion, RIS axonal Ca2+ signals revealed functional compartmentalization: Activity in the nerve ring process correlated with locomotion stop, while activity in a branch correlated with induced reversals. GABA was required to induce, and FLP-11 neuropeptides were required to sustain locomotion stop. RIS attenuates neuronal activity and inhibits movement, possibly enabling sensory integration and decision making, and exemplifies dual use of one cell across development in a compact nervous system. Nature Publishing Group UK 2019-09-10 /pmc/articles/PMC6736843/ /pubmed/31506439 http://dx.doi.org/10.1038/s41467-019-12098-5 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Steuer Costa, Wagner
Van der Auwera, Petrus
Glock, Caspar
Liewald, Jana F.
Bach, Maximilian
Schüler, Christina
Wabnig, Sebastian
Oranth, Alexandra
Masurat, Florentin
Bringmann, Henrik
Schoofs, Liliane
Stelzer, Ernst H. K.
Fischer, Sabine C.
Gottschalk, Alexander
A GABAergic and peptidergic sleep neuron as a locomotion stop neuron with compartmentalized Ca2+ dynamics
title A GABAergic and peptidergic sleep neuron as a locomotion stop neuron with compartmentalized Ca2+ dynamics
title_full A GABAergic and peptidergic sleep neuron as a locomotion stop neuron with compartmentalized Ca2+ dynamics
title_fullStr A GABAergic and peptidergic sleep neuron as a locomotion stop neuron with compartmentalized Ca2+ dynamics
title_full_unstemmed A GABAergic and peptidergic sleep neuron as a locomotion stop neuron with compartmentalized Ca2+ dynamics
title_short A GABAergic and peptidergic sleep neuron as a locomotion stop neuron with compartmentalized Ca2+ dynamics
title_sort gabaergic and peptidergic sleep neuron as a locomotion stop neuron with compartmentalized ca2+ dynamics
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6736843/
https://www.ncbi.nlm.nih.gov/pubmed/31506439
http://dx.doi.org/10.1038/s41467-019-12098-5
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