Cited by 113Neuroscience of respiration and sleepHeart Rate Variability and Autonomic ControlObstructive Sleep Apnea Research

Slow breathing and hypoxic challenge: cardiorespiratory consequences and their central neural substrates.

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Critchley, Hugo D., Nicotra, Alessia, Chiesa, Patrizia A., Nagai, Yoko, Gray, Marcus A., Minati, Ludovico, Bernardi, Luciano·2015·PLOS ONE

Abstract

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 O2) 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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Authors
Critchley, H. D., Nicotra, A., Chiesa, P. A., Nagai, Y., Gray, M. A., Minati, L., & Bernardi, L.
Affiliations
  • Brighton and Sussex Medical School (GB)
  • Imperial College Healthcare NHS Trust (GB)
  • The University of Queensland (AU)
  • Fondazione Santa Lucia (IT)
  • Fondazione IRCCS Istituto Neurologico Carlo Besta (IT)
  • University of Pavia (IT)
Corresponding author
Critchley, Hugo D.
Venue
PLOS ONE
Published
2015-05-14
Volume
10
Issue
5
Pages
e0127082
ISSN
1932-6203 (ISSN-L)
OpenAlex
W2125852331
Cited by
113
References
44
Citations by year
2026: 8 · 2025: 12 · 2024: 8 · 2023: 9 · 2022: 14 · 2021: 10 · 2020: 15 · 2019: 12 · 2018: 6 · 2017: 10 · 2016: 7 · 2015: 2
FWCI
4.62
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • IRIS Research product catalog (Sapienza University of Rome) (submittedVersion, cc-by)
  • Sussex Research Online (University of Sussex) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • Wellcome Trust
  • University of Sussex
  • Dr Mortimer and Theresa Sackler Foundation
Topics
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
  • Health Sciences › Medicine › Physiology › Obstructive Sleep Apnea Research
Keywords
slow-paced breathing, hypoxia, cardiorespiratory control, brainstem, insula, heart rate variability, tidal volume, dorsal pons, periaqueductal gray, amygdala, corticostriatal circuits, yoga, blood pressure, ventilatory response
MeSH terms
Adult, Hypoxia, Blood Pressure, Brain, Female, Heart Rate, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Oxygen, Respiration, Pulmonary Ventilation, Tidal Volume, Young Adult

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