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Slow Breathing and Hypoxic Challenge: Cardiorespiratory Consequences and Their Central Neural Substrates

Controlled slow breathing (at 6/min, a rate frequently adopted during yoga practice) can benefit cardiovascular function, including responses to hypoxia. We tested the neural substrates of cardiorespiratory control in humans during volitional controlled breathing and hypoxic challenge using function...

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Autores principales: Critchley, Hugo D., Nicotra, Alessia, Chiesa, Patrizia A., Nagai, Yoko, Gray, Marcus A., Minati, Ludovico, Bernardi, Luciano
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4431729/
https://www.ncbi.nlm.nih.gov/pubmed/25973923
http://dx.doi.org/10.1371/journal.pone.0127082
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author Critchley, Hugo D.
Nicotra, Alessia
Chiesa, Patrizia A.
Nagai, Yoko
Gray, Marcus A.
Minati, Ludovico
Bernardi, Luciano
author_facet Critchley, Hugo D.
Nicotra, Alessia
Chiesa, Patrizia A.
Nagai, Yoko
Gray, Marcus A.
Minati, Ludovico
Bernardi, Luciano
author_sort Critchley, Hugo D.
collection PubMed
description Controlled slow breathing (at 6/min, a rate frequently adopted during yoga practice) can benefit cardiovascular function, including responses to hypoxia. We tested the neural substrates of cardiorespiratory control in humans during volitional controlled breathing and hypoxic challenge using functional magnetic resonance imaging (fMRI). Twenty healthy volunteers were scanned during paced (slow and normal rate) breathing and during spontaneous breathing of normoxic and hypoxic (13% inspired O(2)) air. Cardiovascular and respiratory measures were acquired concurrently, including beat-to-beat blood pressure from a subset of participants (N = 7). Slow breathing was associated with increased tidal ventilatory volume. Induced hypoxia raised heart rate and suppressed heart rate variability. Within the brain, slow breathing activated dorsal pons, periaqueductal grey matter, cerebellum, hypothalamus, thalamus and lateral and anterior insular cortices. Blocks of hypoxia activated mid pons, bilateral amygdalae, anterior insular and occipitotemporal cortices. Interaction between slow breathing and hypoxia was expressed in ventral striatal and frontal polar activity. Across conditions, within brainstem, dorsal medullary and pontine activity correlated with tidal volume and inversely with heart rate. Activity in rostroventral medulla correlated with beat-to-beat blood pressure and heart rate variability. Widespread insula and striatal activity tracked decreases in heart rate, while subregions of insular cortex correlated with momentary increases in tidal volume. Our findings define slow breathing effects on central and cardiovascular responses to hypoxic challenge. They highlight the recruitment of discrete brainstem nuclei to cardiorespiratory control, and the engagement of corticostriatal circuitry in support of physiological responses that accompany breathing regulation during hypoxic challenge.
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spelling pubmed-44317292015-05-27 Slow Breathing and Hypoxic Challenge: Cardiorespiratory Consequences and Their Central Neural Substrates Critchley, Hugo D. Nicotra, Alessia Chiesa, Patrizia A. Nagai, Yoko Gray, Marcus A. Minati, Ludovico Bernardi, Luciano PLoS One Research Article Controlled slow breathing (at 6/min, a rate frequently adopted during yoga practice) can benefit cardiovascular function, including responses to hypoxia. We tested the neural substrates of cardiorespiratory control in humans during volitional controlled breathing and hypoxic challenge using functional magnetic resonance imaging (fMRI). Twenty healthy volunteers were scanned during paced (slow and normal rate) breathing and during spontaneous breathing of normoxic and hypoxic (13% inspired O(2)) air. Cardiovascular and respiratory measures were acquired concurrently, including beat-to-beat blood pressure from a subset of participants (N = 7). Slow breathing was associated with increased tidal ventilatory volume. Induced hypoxia raised heart rate and suppressed heart rate variability. Within the brain, slow breathing activated dorsal pons, periaqueductal grey matter, cerebellum, hypothalamus, thalamus and lateral and anterior insular cortices. Blocks of hypoxia activated mid pons, bilateral amygdalae, anterior insular and occipitotemporal cortices. Interaction between slow breathing and hypoxia was expressed in ventral striatal and frontal polar activity. Across conditions, within brainstem, dorsal medullary and pontine activity correlated with tidal volume and inversely with heart rate. Activity in rostroventral medulla correlated with beat-to-beat blood pressure and heart rate variability. Widespread insula and striatal activity tracked decreases in heart rate, while subregions of insular cortex correlated with momentary increases in tidal volume. Our findings define slow breathing effects on central and cardiovascular responses to hypoxic challenge. They highlight the recruitment of discrete brainstem nuclei to cardiorespiratory control, and the engagement of corticostriatal circuitry in support of physiological responses that accompany breathing regulation during hypoxic challenge. Public Library of Science 2015-05-14 /pmc/articles/PMC4431729/ /pubmed/25973923 http://dx.doi.org/10.1371/journal.pone.0127082 Text en © 2015 Critchley et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Critchley, Hugo D.
Nicotra, Alessia
Chiesa, Patrizia A.
Nagai, Yoko
Gray, Marcus A.
Minati, Ludovico
Bernardi, Luciano
Slow Breathing and Hypoxic Challenge: Cardiorespiratory Consequences and Their Central Neural Substrates
title Slow Breathing and Hypoxic Challenge: Cardiorespiratory Consequences and Their Central Neural Substrates
title_full Slow Breathing and Hypoxic Challenge: Cardiorespiratory Consequences and Their Central Neural Substrates
title_fullStr Slow Breathing and Hypoxic Challenge: Cardiorespiratory Consequences and Their Central Neural Substrates
title_full_unstemmed Slow Breathing and Hypoxic Challenge: Cardiorespiratory Consequences and Their Central Neural Substrates
title_short Slow Breathing and Hypoxic Challenge: Cardiorespiratory Consequences and Their Central Neural Substrates
title_sort slow breathing and hypoxic challenge: cardiorespiratory consequences and their central neural substrates
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4431729/
https://www.ncbi.nlm.nih.gov/pubmed/25973923
http://dx.doi.org/10.1371/journal.pone.0127082
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