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Investigation of hindbrain activity during active locomotion reveals inhibitory neurons involved in sensorimotor processing

Locomotion in vertebrates relies on motor circuits in the spinal cord receiving inputs from the hindbrain to execute motor commands while dynamically integrating proprioceptive sensory feedback. The spatial organization of the neuronal networks driving locomotion in the hindbrain and role of inhibit...

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Autores principales: Severi, Kristen E., Böhm, Urs L., Wyart, Claire
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6134141/
https://www.ncbi.nlm.nih.gov/pubmed/30206288
http://dx.doi.org/10.1038/s41598-018-31968-4
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author Severi, Kristen E.
Böhm, Urs L.
Wyart, Claire
author_facet Severi, Kristen E.
Böhm, Urs L.
Wyart, Claire
author_sort Severi, Kristen E.
collection PubMed
description Locomotion in vertebrates relies on motor circuits in the spinal cord receiving inputs from the hindbrain to execute motor commands while dynamically integrating proprioceptive sensory feedback. The spatial organization of the neuronal networks driving locomotion in the hindbrain and role of inhibition has not been extensively investigated. Here, we mapped neuronal activity with single-cell resolution in the hindbrain of restrained transgenic Tg(HuC:GCaMP5G) zebrafish larvae swimming in response to whole-field visual motion. We combined large-scale population calcium imaging in the hindbrain with simultaneous high-speed recording of the moving tail in animals where specific markers label glycinergic inhibitory neurons. We identified cells whose activity preferentially correlates with the visual stimulus or motor activity and used brain registration to compare data across individual larvae. We then morphed calcium imaging data onto the zebrafish brain atlas to compare with known transgenic markers. We report cells localized in the cerebellum whose activity is shut off by the onset of the visual stimulus, suggesting these cells may be constitutively active and silenced during sensorimotor processing. Finally, we discover that the activity of a medial stripe of glycinergic neurons in the domain of expression of the transcription factor engrailed1b is highly correlated with the onset of locomotion. Our efforts provide a high-resolution, open-access dataset for the community by comparing our functional map of the hindbrain to existing open-access atlases and enabling further investigation of this population’s role in locomotion.
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spelling pubmed-61341412018-09-15 Investigation of hindbrain activity during active locomotion reveals inhibitory neurons involved in sensorimotor processing Severi, Kristen E. Böhm, Urs L. Wyart, Claire Sci Rep Article Locomotion in vertebrates relies on motor circuits in the spinal cord receiving inputs from the hindbrain to execute motor commands while dynamically integrating proprioceptive sensory feedback. The spatial organization of the neuronal networks driving locomotion in the hindbrain and role of inhibition has not been extensively investigated. Here, we mapped neuronal activity with single-cell resolution in the hindbrain of restrained transgenic Tg(HuC:GCaMP5G) zebrafish larvae swimming in response to whole-field visual motion. We combined large-scale population calcium imaging in the hindbrain with simultaneous high-speed recording of the moving tail in animals where specific markers label glycinergic inhibitory neurons. We identified cells whose activity preferentially correlates with the visual stimulus or motor activity and used brain registration to compare data across individual larvae. We then morphed calcium imaging data onto the zebrafish brain atlas to compare with known transgenic markers. We report cells localized in the cerebellum whose activity is shut off by the onset of the visual stimulus, suggesting these cells may be constitutively active and silenced during sensorimotor processing. Finally, we discover that the activity of a medial stripe of glycinergic neurons in the domain of expression of the transcription factor engrailed1b is highly correlated with the onset of locomotion. Our efforts provide a high-resolution, open-access dataset for the community by comparing our functional map of the hindbrain to existing open-access atlases and enabling further investigation of this population’s role in locomotion. Nature Publishing Group UK 2018-09-11 /pmc/articles/PMC6134141/ /pubmed/30206288 http://dx.doi.org/10.1038/s41598-018-31968-4 Text en © The Author(s) 2018 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
Severi, Kristen E.
Böhm, Urs L.
Wyart, Claire
Investigation of hindbrain activity during active locomotion reveals inhibitory neurons involved in sensorimotor processing
title Investigation of hindbrain activity during active locomotion reveals inhibitory neurons involved in sensorimotor processing
title_full Investigation of hindbrain activity during active locomotion reveals inhibitory neurons involved in sensorimotor processing
title_fullStr Investigation of hindbrain activity during active locomotion reveals inhibitory neurons involved in sensorimotor processing
title_full_unstemmed Investigation of hindbrain activity during active locomotion reveals inhibitory neurons involved in sensorimotor processing
title_short Investigation of hindbrain activity during active locomotion reveals inhibitory neurons involved in sensorimotor processing
title_sort investigation of hindbrain activity during active locomotion reveals inhibitory neurons involved in sensorimotor processing
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6134141/
https://www.ncbi.nlm.nih.gov/pubmed/30206288
http://dx.doi.org/10.1038/s41598-018-31968-4
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