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Hypothesis: Pulmonary Afferent Activity Patterns During Slow, Deep Breathing Contribute to the Neural Induction of Physiological Relaxation

Control of respiration provides a powerful voluntary portal to entrain and modulate central autonomic networks. Slowing and deepening breathing as a relaxation technique has shown promise in a variety of cardiorespiratory and stress-related disorders, but few studies have investigated the physiologi...

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Autores principales: Noble, Donald J., Hochman, Shawn
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6753868/
https://www.ncbi.nlm.nih.gov/pubmed/31572221
http://dx.doi.org/10.3389/fphys.2019.01176
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author Noble, Donald J.
Hochman, Shawn
author_facet Noble, Donald J.
Hochman, Shawn
author_sort Noble, Donald J.
collection PubMed
description Control of respiration provides a powerful voluntary portal to entrain and modulate central autonomic networks. Slowing and deepening breathing as a relaxation technique has shown promise in a variety of cardiorespiratory and stress-related disorders, but few studies have investigated the physiological mechanisms conferring its benefits. Recent evidence suggests that breathing at a frequency near 0.1 Hz (6 breaths per minute) promotes behavioral relaxation and baroreflex resonance effects that maximize heart rate variability. Breathing around this frequency appears to elicit resonant and coherent features in neuro-mechanical interactions that optimize physiological function. Here we explore the neurophysiology of slow, deep breathing and propose that coincident features of respiratory and baroreceptor afferent activity cycling at 0.1 Hz entrain central autonomic networks. An important role is assigned to the preferential recruitment of slowly-adapting pulmonary afferents (SARs) during prolonged inhalations. These afferents project to discrete areas in the brainstem within the nucleus of the solitary tract (NTS) and initiate inhibitory actions on downstream targets. Conversely, deep exhalations terminate SAR activity and activate arterial baroreceptors via increases in blood pressure to stimulate, through NTS projections, parasympathetic outflow to the heart. Reciprocal SAR and baroreceptor afferent-evoked actions combine to enhance sympathetic activity during inhalation and parasympathetic activity during exhalation, respectively. This leads to pronounced heart rate variability in phase with the respiratory cycle (respiratory sinus arrhythmia) and improved ventilation-perfusion matching. NTS relay neurons project extensively to areas of the central autonomic network to encode important features of the breathing pattern that may modulate anxiety, arousal, and attention. In our model, pronounced respiratory rhythms during slow, deep breathing also support expression of slow cortical rhythms to induce a functional state of alert relaxation, and, via nasal respiration-based actions on olfactory signaling, recruit hippocampal pathways to boost memory consolidation. Collectively, we assert that the neurophysiological processes recruited during slow, deep breathing enhance the cognitive and behavioral therapeutic outcomes obtained through various mind-body practices. Future studies are required to better understand the physio-behavioral processes involved, including in animal models that control for confounding factors such as expectancy biases.
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spelling pubmed-67538682019-09-30 Hypothesis: Pulmonary Afferent Activity Patterns During Slow, Deep Breathing Contribute to the Neural Induction of Physiological Relaxation Noble, Donald J. Hochman, Shawn Front Physiol Physiology Control of respiration provides a powerful voluntary portal to entrain and modulate central autonomic networks. Slowing and deepening breathing as a relaxation technique has shown promise in a variety of cardiorespiratory and stress-related disorders, but few studies have investigated the physiological mechanisms conferring its benefits. Recent evidence suggests that breathing at a frequency near 0.1 Hz (6 breaths per minute) promotes behavioral relaxation and baroreflex resonance effects that maximize heart rate variability. Breathing around this frequency appears to elicit resonant and coherent features in neuro-mechanical interactions that optimize physiological function. Here we explore the neurophysiology of slow, deep breathing and propose that coincident features of respiratory and baroreceptor afferent activity cycling at 0.1 Hz entrain central autonomic networks. An important role is assigned to the preferential recruitment of slowly-adapting pulmonary afferents (SARs) during prolonged inhalations. These afferents project to discrete areas in the brainstem within the nucleus of the solitary tract (NTS) and initiate inhibitory actions on downstream targets. Conversely, deep exhalations terminate SAR activity and activate arterial baroreceptors via increases in blood pressure to stimulate, through NTS projections, parasympathetic outflow to the heart. Reciprocal SAR and baroreceptor afferent-evoked actions combine to enhance sympathetic activity during inhalation and parasympathetic activity during exhalation, respectively. This leads to pronounced heart rate variability in phase with the respiratory cycle (respiratory sinus arrhythmia) and improved ventilation-perfusion matching. NTS relay neurons project extensively to areas of the central autonomic network to encode important features of the breathing pattern that may modulate anxiety, arousal, and attention. In our model, pronounced respiratory rhythms during slow, deep breathing also support expression of slow cortical rhythms to induce a functional state of alert relaxation, and, via nasal respiration-based actions on olfactory signaling, recruit hippocampal pathways to boost memory consolidation. Collectively, we assert that the neurophysiological processes recruited during slow, deep breathing enhance the cognitive and behavioral therapeutic outcomes obtained through various mind-body practices. Future studies are required to better understand the physio-behavioral processes involved, including in animal models that control for confounding factors such as expectancy biases. Frontiers Media S.A. 2019-09-13 /pmc/articles/PMC6753868/ /pubmed/31572221 http://dx.doi.org/10.3389/fphys.2019.01176 Text en Copyright © 2019 Noble and Hochman. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Noble, Donald J.
Hochman, Shawn
Hypothesis: Pulmonary Afferent Activity Patterns During Slow, Deep Breathing Contribute to the Neural Induction of Physiological Relaxation
title Hypothesis: Pulmonary Afferent Activity Patterns During Slow, Deep Breathing Contribute to the Neural Induction of Physiological Relaxation
title_full Hypothesis: Pulmonary Afferent Activity Patterns During Slow, Deep Breathing Contribute to the Neural Induction of Physiological Relaxation
title_fullStr Hypothesis: Pulmonary Afferent Activity Patterns During Slow, Deep Breathing Contribute to the Neural Induction of Physiological Relaxation
title_full_unstemmed Hypothesis: Pulmonary Afferent Activity Patterns During Slow, Deep Breathing Contribute to the Neural Induction of Physiological Relaxation
title_short Hypothesis: Pulmonary Afferent Activity Patterns During Slow, Deep Breathing Contribute to the Neural Induction of Physiological Relaxation
title_sort hypothesis: pulmonary afferent activity patterns during slow, deep breathing contribute to the neural induction of physiological relaxation
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6753868/
https://www.ncbi.nlm.nih.gov/pubmed/31572221
http://dx.doi.org/10.3389/fphys.2019.01176
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