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Breathing above the brain stem: volitional control and attentional modulation in humans
Open accessAbstract
Whereas the neurophysiology of respiration has traditionally focused on automatic brain stem processes, higher brain mechanisms underlying the cognitive aspects of breathing are gaining increasing interest. Therapeutic techniques have used conscious control and awareness of breathing for millennia with little understanding of the mechanisms underlying their efficacy. Using direct intracranial recordings in humans, we correlated cortical and limbic neuronal activity as measured by the intracranial electroencephalogram (iEEG) with the breathing cycle. We show this to be the direct result of neuronal activity, as demonstrated by both the specificity of the finding to the cortical gray matter and the tracking of breath by the gamma-band (40–150 Hz) envelope in these structures. We extend prior observations by showing the iEEG signal to track the breathing cycle across a widespread network of cortical and limbic structures. We further demonstrate a sensitivity of this tracking to cognitive factors by using tasks adapted from cognitive behavioral therapy and meditative practice. Specifically, volitional control and awareness of breathing engage distinct but overlapping brain circuits. During volitionally paced breathing, iEEG-breath coherence increases in a frontotemporal-insular network, and during attention to breathing, we demonstrate increased coherence in the anterior cingulate, premotor, insular, and hippocampal cortices. Our findings suggest that breathing can act as an organizing hierarchical principle for neuronal oscillations throughout the brain and detail mechanisms of how cognitive factors impact otherwise automatic neuronal processes during interoceptive attention. NEW & NOTEWORTHY Whereas the link between breathing and brain activity has a long history of application to therapy, its neurophysiology remains unexplored. Using intracranial recordings in humans, we show neuronal activity to track the breathing cycle throughout widespread cortical/limbic sites. Volitional pacing of the breath engages frontotemporal-insular cortices, whereas attention to automatic breathing modulates the cingulate cortex. Our findings imply a fundamental role of breathing-related oscillations in driving neuronal activity and provide insight into the neuronal mechanisms of interoceptive attention.
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“However, there is also evidence that voluntary breathing might not be essential to realize the basic physiological benefits of these techniques; spontaneous slow breathing without cognitive motor intent may be sufficient (Hirsch and Bishop, 1981; Herrero et al., 2018).”
From Hypothesis: Pulmonary Afferent Activity Patterns During Slow, Deep Breathing Contribute to the Neural Induction of Physiological Relaxation (2019) · cites this paper as Herrero et al., 2018
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“The respiratory rate is a marker of emotional stress because it is partially regulated by brain area activities involved in emotional processing [105].”
From Therapy Dog Welfare Revisited: A Review of the Literature (2021) · cites this paper as [105]
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“Second, coupling between respiration and neural activity has also been observed in motor regions in both rodents 141 and humans 137 .”
From Interoceptive rhythms in the brain (2023) · cites this paper as [137]
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“The involvement of large portions of the limbic system (amygdala, hippocampus, insula, cingulate) is confirmed in human intra-cranial recordings 136,137 .”
From Interoceptive rhythms in the brain (2023) · cites this paper as [137]
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“First, respiratory-related activity is observed in the somatosensory cortex, both in humans 137,140 and in different parts of the rodent or cat somatosensory cortex: the whisker barrel cortex 118,141 , trunk 122,123 and nose 142 representation.”
From Interoceptive rhythms in the brain (2023) · cites this paper as [137]
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Metadata
- Authors
- Herrero, J. L., Khuvis, S., Yeagle, E., Cerf, M., & Mehta, A. D.
- Affiliations
- Feinstein Institute for Medical Research (US)
- Northwestern University (US)
- Corresponding author
- Mehta, Ashesh D.
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 2018-01-01
- Volume
- 119
- Issue
- 1
- Pages
- 145-159
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- PMC
- PMC5866472
- OpenAlex
- W2760226235
- Cited by
- 338
- References
- 86
- Citations by year
- 2026: 32 · 2025: 54 · 2024: 46 · 2023: 55 · 2022: 51 · 2021: 34 · 2020: 29 · 2019: 21 · 2018: 16
- FWCI
- 11.07
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neurophysiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- HHS | NIH | National Institute of Neurological Disorders and Stroke (NINDS) (NIH/NINDS U01 NS098976-01)
- HHS | NIH | National Institute of Mental Health (NIMH) (NIH/NIMH R01 MH111439, NIMH 1R21MH114166-01)
- Human Frontier Science Program (HFSP) (LT000151/2012-L/6)
- 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 › Psychiatry and Mental health › Psychosomatic Disorders and Their Treatments
- Keywords
- breathing, respiration, brainstem, volitional control, interoceptive attention, intracranial EEG, gamma oscillations, neural oscillations, insula, anterior cingulate cortex, hippocampus, premotor cortex, cognitive behavioral therapy, meditation, intracranial recordings
- MeSH terms
- Adult, Attention, Brain Stem, Cerebral Cortex, Female, Humans, Male, Respiration, Gamma Rhythm
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