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Identification of peripheral neural circuits that regulate heart rate using optogenetic and viral vector strategies

Heart rate is under the precise control of the autonomic nervous system. However, the wiring of peripheral neural circuits that regulate heart rate is poorly understood. Here, we develop a clearing-imaging-analysis pipeline to visualize innervation of intact hearts in 3D and employed a multi-techniq...

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Autores principales: Rajendran, Pradeep S., Challis, Rosemary C., Fowlkes, Charless C., Hanna, Peter, Tompkins, John D., Jordan, Maria C., Hiyari, Sarah, Gabris-Weber, Beth A., Greenbaum, Alon, Chan, Ken Y., Deverman, Benjamin E., Münzberg, Heike, Ardell, Jeffrey L., Salama, Guy, Gradinaru, Viviana, Shivkumar, Kalyanam
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6486614/
https://www.ncbi.nlm.nih.gov/pubmed/31028266
http://dx.doi.org/10.1038/s41467-019-09770-1
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author Rajendran, Pradeep S.
Challis, Rosemary C.
Fowlkes, Charless C.
Hanna, Peter
Tompkins, John D.
Jordan, Maria C.
Hiyari, Sarah
Gabris-Weber, Beth A.
Greenbaum, Alon
Chan, Ken Y.
Deverman, Benjamin E.
Münzberg, Heike
Ardell, Jeffrey L.
Salama, Guy
Gradinaru, Viviana
Shivkumar, Kalyanam
author_facet Rajendran, Pradeep S.
Challis, Rosemary C.
Fowlkes, Charless C.
Hanna, Peter
Tompkins, John D.
Jordan, Maria C.
Hiyari, Sarah
Gabris-Weber, Beth A.
Greenbaum, Alon
Chan, Ken Y.
Deverman, Benjamin E.
Münzberg, Heike
Ardell, Jeffrey L.
Salama, Guy
Gradinaru, Viviana
Shivkumar, Kalyanam
author_sort Rajendran, Pradeep S.
collection PubMed
description Heart rate is under the precise control of the autonomic nervous system. However, the wiring of peripheral neural circuits that regulate heart rate is poorly understood. Here, we develop a clearing-imaging-analysis pipeline to visualize innervation of intact hearts in 3D and employed a multi-technique approach to map parasympathetic and sympathetic neural circuits that control heart rate in mice. We identify cholinergic neurons and noradrenergic neurons in an intrinsic cardiac ganglion and the stellate ganglia, respectively, that project to the sinoatrial node. We also report that the heart rate response to optogenetic versus electrical stimulation of the vagus nerve displays different temporal characteristics and that vagal afferents enhance parasympathetic and reduce sympathetic tone to the heart via central mechanisms. Our findings provide new insights into neural regulation of heart rate, and our methodology to study cardiac circuits can be readily used to interrogate neural control of other visceral organs.
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spelling pubmed-64866142019-04-29 Identification of peripheral neural circuits that regulate heart rate using optogenetic and viral vector strategies Rajendran, Pradeep S. Challis, Rosemary C. Fowlkes, Charless C. Hanna, Peter Tompkins, John D. Jordan, Maria C. Hiyari, Sarah Gabris-Weber, Beth A. Greenbaum, Alon Chan, Ken Y. Deverman, Benjamin E. Münzberg, Heike Ardell, Jeffrey L. Salama, Guy Gradinaru, Viviana Shivkumar, Kalyanam Nat Commun Article Heart rate is under the precise control of the autonomic nervous system. However, the wiring of peripheral neural circuits that regulate heart rate is poorly understood. Here, we develop a clearing-imaging-analysis pipeline to visualize innervation of intact hearts in 3D and employed a multi-technique approach to map parasympathetic and sympathetic neural circuits that control heart rate in mice. We identify cholinergic neurons and noradrenergic neurons in an intrinsic cardiac ganglion and the stellate ganglia, respectively, that project to the sinoatrial node. We also report that the heart rate response to optogenetic versus electrical stimulation of the vagus nerve displays different temporal characteristics and that vagal afferents enhance parasympathetic and reduce sympathetic tone to the heart via central mechanisms. Our findings provide new insights into neural regulation of heart rate, and our methodology to study cardiac circuits can be readily used to interrogate neural control of other visceral organs. Nature Publishing Group UK 2019-04-26 /pmc/articles/PMC6486614/ /pubmed/31028266 http://dx.doi.org/10.1038/s41467-019-09770-1 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
Rajendran, Pradeep S.
Challis, Rosemary C.
Fowlkes, Charless C.
Hanna, Peter
Tompkins, John D.
Jordan, Maria C.
Hiyari, Sarah
Gabris-Weber, Beth A.
Greenbaum, Alon
Chan, Ken Y.
Deverman, Benjamin E.
Münzberg, Heike
Ardell, Jeffrey L.
Salama, Guy
Gradinaru, Viviana
Shivkumar, Kalyanam
Identification of peripheral neural circuits that regulate heart rate using optogenetic and viral vector strategies
title Identification of peripheral neural circuits that regulate heart rate using optogenetic and viral vector strategies
title_full Identification of peripheral neural circuits that regulate heart rate using optogenetic and viral vector strategies
title_fullStr Identification of peripheral neural circuits that regulate heart rate using optogenetic and viral vector strategies
title_full_unstemmed Identification of peripheral neural circuits that regulate heart rate using optogenetic and viral vector strategies
title_short Identification of peripheral neural circuits that regulate heart rate using optogenetic and viral vector strategies
title_sort identification of peripheral neural circuits that regulate heart rate using optogenetic and viral vector strategies
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6486614/
https://www.ncbi.nlm.nih.gov/pubmed/31028266
http://dx.doi.org/10.1038/s41467-019-09770-1
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