title: Slow breathing and hypoxic challenge: cardiorespiratory consequences and their central neural substrates.
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.
authors.affiliation: Brighton and Sussex Medical School, University of Sussex, Brighton, United Kingdom; Sackler Centre for Consciousness Science, University of Sussex, Brighton, United Kingdom.
authors.forename: Hugo D
authors.initials: HD
authors.lastname: Critchley
authors.affiliation: Imperial College Healthcare NHS Trust, London, United Kingdom.
authors.forename: Alessia
authors.initials: A
authors.lastname: Nicotra
authors.affiliation: Department of Psychology, Sapienza University of Rome, Rome, Italy; Ghermann Laboratory, University of Queensland, Queensland, Australia.
authors.forename: Patrizia A
authors.initials: PA
authors.lastname: Chiesa
authors.affiliation: Brighton and Sussex Medical School, University of Sussex, Brighton, United Kingdom.
authors.forename: Yoko
authors.initials: Y
authors.lastname: Nagai
authors.affiliation: IRCCS, Fondazione Santa Lucia, Rome, Italy.
authors.forename: Marcus A
authors.initials: MA
authors.lastname: Gray
authors.affiliation: IRCCS, Fondazione Neurologico Carlo Besta, Milano, Italy.
authors.forename: Ludovico
authors.initials: L
authors.lastname: Minati
authors.affiliation: Department of Internal Medicine, University of Pavia and Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.
authors.forename: Luciano
authors.initials: L
authors.lastname: Bernardi
mesh_terms: D000328:Adult; D001794:Blood Pressure; D001921:Brain / Q000502:physiology*; D005260:Female; D006339:Heart Rate; D006801:Humans; D000860:Hypoxia / Q000378:metabolism / Q000503:physiopathology*; D008279:Magnetic Resonance Imaging; D008297:Male; D008875:Middle Aged; D010100:Oxygen / Q000378:metabolism*; D012123:Pulmonary Ventilation; D012119:Respiration; D013990:Tidal Volume; D055815:Young Adult
chemical_list: D010100:Oxygen