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Diversity of neurovascular coupling dynamics along vascular arbors in layer II/III somatosensory cortex

The spatial-temporal sequence of cerebral blood flow (CBF), cerebral blood volume (CBV) and blood velocity changes triggered by neuronal activation is critical for understanding functional brain imaging. This sequence follows a stereotypic pattern of changes across different zones of the vasculature...

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Autores principales: Rungta, Ravi L., Zuend, Marc, Aydin, Ali-Kemal, Martineau, Éric, Boido, Davide, Weber, Bruno, Charpak, Serge
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8270975/
https://www.ncbi.nlm.nih.gov/pubmed/34244604
http://dx.doi.org/10.1038/s42003-021-02382-w
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author Rungta, Ravi L.
Zuend, Marc
Aydin, Ali-Kemal
Martineau, Éric
Boido, Davide
Weber, Bruno
Charpak, Serge
author_facet Rungta, Ravi L.
Zuend, Marc
Aydin, Ali-Kemal
Martineau, Éric
Boido, Davide
Weber, Bruno
Charpak, Serge
author_sort Rungta, Ravi L.
collection PubMed
description The spatial-temporal sequence of cerebral blood flow (CBF), cerebral blood volume (CBV) and blood velocity changes triggered by neuronal activation is critical for understanding functional brain imaging. This sequence follows a stereotypic pattern of changes across different zones of the vasculature in the olfactory bulb, the first relay of olfaction. However, in the cerebral cortex, where most human brain mapping studies are performed, the timing of activity evoked vascular events remains controversial. Here we utilized a single whisker stimulation model to map out functional hyperemia along vascular arbours from layer II/III to the surface of primary somatosensory cortex, in anesthetized and awake Thy1-GCaMP6 mice. We demonstrate that sensory stimulation triggers an increase in blood velocity within the mid-capillary bed and a dilation of upstream large capillaries, and the penetrating and pial arterioles. We report that under physiological stimulation, response onset times are highly variable across compartments of different vascular arbours. Furthermore, generating transfer functions (TFs) between neuronal Ca(2+) and vascular dynamics across different brain states demonstrates that anesthesia decelerates neurovascular coupling (NVC). This spatial-temporal pattern of vascular events demonstrates functional diversity not only between different brain regions but also at the level of different vascular arbours within supragranular layers of the cerebral cortex.
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spelling pubmed-82709752021-07-23 Diversity of neurovascular coupling dynamics along vascular arbors in layer II/III somatosensory cortex Rungta, Ravi L. Zuend, Marc Aydin, Ali-Kemal Martineau, Éric Boido, Davide Weber, Bruno Charpak, Serge Commun Biol Article The spatial-temporal sequence of cerebral blood flow (CBF), cerebral blood volume (CBV) and blood velocity changes triggered by neuronal activation is critical for understanding functional brain imaging. This sequence follows a stereotypic pattern of changes across different zones of the vasculature in the olfactory bulb, the first relay of olfaction. However, in the cerebral cortex, where most human brain mapping studies are performed, the timing of activity evoked vascular events remains controversial. Here we utilized a single whisker stimulation model to map out functional hyperemia along vascular arbours from layer II/III to the surface of primary somatosensory cortex, in anesthetized and awake Thy1-GCaMP6 mice. We demonstrate that sensory stimulation triggers an increase in blood velocity within the mid-capillary bed and a dilation of upstream large capillaries, and the penetrating and pial arterioles. We report that under physiological stimulation, response onset times are highly variable across compartments of different vascular arbours. Furthermore, generating transfer functions (TFs) between neuronal Ca(2+) and vascular dynamics across different brain states demonstrates that anesthesia decelerates neurovascular coupling (NVC). This spatial-temporal pattern of vascular events demonstrates functional diversity not only between different brain regions but also at the level of different vascular arbours within supragranular layers of the cerebral cortex. Nature Publishing Group UK 2021-07-09 /pmc/articles/PMC8270975/ /pubmed/34244604 http://dx.doi.org/10.1038/s42003-021-02382-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Rungta, Ravi L.
Zuend, Marc
Aydin, Ali-Kemal
Martineau, Éric
Boido, Davide
Weber, Bruno
Charpak, Serge
Diversity of neurovascular coupling dynamics along vascular arbors in layer II/III somatosensory cortex
title Diversity of neurovascular coupling dynamics along vascular arbors in layer II/III somatosensory cortex
title_full Diversity of neurovascular coupling dynamics along vascular arbors in layer II/III somatosensory cortex
title_fullStr Diversity of neurovascular coupling dynamics along vascular arbors in layer II/III somatosensory cortex
title_full_unstemmed Diversity of neurovascular coupling dynamics along vascular arbors in layer II/III somatosensory cortex
title_short Diversity of neurovascular coupling dynamics along vascular arbors in layer II/III somatosensory cortex
title_sort diversity of neurovascular coupling dynamics along vascular arbors in layer ii/iii somatosensory cortex
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8270975/
https://www.ncbi.nlm.nih.gov/pubmed/34244604
http://dx.doi.org/10.1038/s42003-021-02382-w
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