Cargando…

The interdependence of excitation and inhibition for the control of dynamic breathing rhythms

The preBötzinger Complex (preBötC), a medullary network critical for breathing, relies on excitatory interneurons to generate the inspiratory rhythm. Yet, half of preBötC neurons are inhibitory, and the role of inhibition in rhythmogenesis remains controversial. Using optogenetics and electrophysiol...

Descripción completa

Detalles Bibliográficos
Autores principales: Baertsch, Nathan Andrew, Baertsch, Hans Christopher, Ramirez, Jan Marino
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5827754/
https://www.ncbi.nlm.nih.gov/pubmed/29483589
http://dx.doi.org/10.1038/s41467-018-03223-x
_version_ 1783302530158034944
author Baertsch, Nathan Andrew
Baertsch, Hans Christopher
Ramirez, Jan Marino
author_facet Baertsch, Nathan Andrew
Baertsch, Hans Christopher
Ramirez, Jan Marino
author_sort Baertsch, Nathan Andrew
collection PubMed
description The preBötzinger Complex (preBötC), a medullary network critical for breathing, relies on excitatory interneurons to generate the inspiratory rhythm. Yet, half of preBötC neurons are inhibitory, and the role of inhibition in rhythmogenesis remains controversial. Using optogenetics and electrophysiology in vitro and in vivo, we demonstrate that the intrinsic excitability of excitatory neurons is reduced following large depolarizing inspiratory bursts. This refractory period limits the preBötC to very slow breathing frequencies. Inhibition integrated within the network is required to prevent overexcitation of preBötC neurons, thereby regulating the refractory period and allowing rapid breathing. In vivo, sensory feedback inhibition also regulates the refractory period, and in slowly breathing mice with sensory feedback removed, activity of inhibitory, but not excitatory, neurons restores breathing to physiological frequencies. We conclude that excitation and inhibition are interdependent for the breathing rhythm, because inhibition permits physiological preBötC bursting by controlling refractory properties of excitatory neurons.
format Online
Article
Text
id pubmed-5827754
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-58277542018-03-02 The interdependence of excitation and inhibition for the control of dynamic breathing rhythms Baertsch, Nathan Andrew Baertsch, Hans Christopher Ramirez, Jan Marino Nat Commun Article The preBötzinger Complex (preBötC), a medullary network critical for breathing, relies on excitatory interneurons to generate the inspiratory rhythm. Yet, half of preBötC neurons are inhibitory, and the role of inhibition in rhythmogenesis remains controversial. Using optogenetics and electrophysiology in vitro and in vivo, we demonstrate that the intrinsic excitability of excitatory neurons is reduced following large depolarizing inspiratory bursts. This refractory period limits the preBötC to very slow breathing frequencies. Inhibition integrated within the network is required to prevent overexcitation of preBötC neurons, thereby regulating the refractory period and allowing rapid breathing. In vivo, sensory feedback inhibition also regulates the refractory period, and in slowly breathing mice with sensory feedback removed, activity of inhibitory, but not excitatory, neurons restores breathing to physiological frequencies. We conclude that excitation and inhibition are interdependent for the breathing rhythm, because inhibition permits physiological preBötC bursting by controlling refractory properties of excitatory neurons. Nature Publishing Group UK 2018-02-26 /pmc/articles/PMC5827754/ /pubmed/29483589 http://dx.doi.org/10.1038/s41467-018-03223-x 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
Baertsch, Nathan Andrew
Baertsch, Hans Christopher
Ramirez, Jan Marino
The interdependence of excitation and inhibition for the control of dynamic breathing rhythms
title The interdependence of excitation and inhibition for the control of dynamic breathing rhythms
title_full The interdependence of excitation and inhibition for the control of dynamic breathing rhythms
title_fullStr The interdependence of excitation and inhibition for the control of dynamic breathing rhythms
title_full_unstemmed The interdependence of excitation and inhibition for the control of dynamic breathing rhythms
title_short The interdependence of excitation and inhibition for the control of dynamic breathing rhythms
title_sort interdependence of excitation and inhibition for the control of dynamic breathing rhythms
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5827754/
https://www.ncbi.nlm.nih.gov/pubmed/29483589
http://dx.doi.org/10.1038/s41467-018-03223-x
work_keys_str_mv AT baertschnathanandrew theinterdependenceofexcitationandinhibitionforthecontrolofdynamicbreathingrhythms
AT baertschhanschristopher theinterdependenceofexcitationandinhibitionforthecontrolofdynamicbreathingrhythms
AT ramirezjanmarino theinterdependenceofexcitationandinhibitionforthecontrolofdynamicbreathingrhythms
AT baertschnathanandrew interdependenceofexcitationandinhibitionforthecontrolofdynamicbreathingrhythms
AT baertschhanschristopher interdependenceofexcitationandinhibitionforthecontrolofdynamicbreathingrhythms
AT ramirezjanmarino interdependenceofexcitationandinhibitionforthecontrolofdynamicbreathingrhythms