Preprint
Human forebrain neural synchronization and entrainment to breathing during wakefulness, sleep, and external mechanical ventilation
Research square
05/14/2025
DOI: 10.21203/rs.3.rs-6568046/v1
PMCID: PMC12136201
PMID: 40470175
Abstract
The ability of the forebrain to track and integrate respiratory signals, a process known as breathing interoception, is critical for detecting respiratory threats and ensuring survival, yet its neural mechanisms remain largely unknown. Using human intracranial recordings, we identified widespread synchronization between forebrain neural oscillations and breathing rhythms across wakefulness, sleep, and external mechanical ventilation. During wakefulness, localized sites within known interoceptive regions such as insula, somatosensory cortex, anterior cingulate cortex, and amygdala robustly synchronized with breathing, highlighting their critical roles in breathing interoception. During sleep, forebrain synchronization shifted from cortex to amygdala and hippocampus, suggesting redistributed processing that may support vigilance and memory consolidation. In contrast to rodents, nasal airflow was not required for this synchronization, implicating multiple afferent pathways in respiratory interoception and possible unique evolutionary changes in humans. When breathing was driven by an external mechanical ventilator, the imposed breathing rhythm directly entrained forebrain activity, indicating a causal link. Notably, ventilator-driven slow, deep breathing entrained more forebrain sites, suggesting a potential mechanism through which breath-based practices might influence emotion and cognition. Together, these findings redefine breathing interoception as a pervasive influence within the forebrain, with implications for understanding disorders of respiratory awareness, emotional regulation, and cognitive health.
Details
- Title: Subtitle
- Human forebrain neural synchronization and entrainment to breathing during wakefulness, sleep, and external mechanical ventilation
- Creators
- Brian Dlouhy - University of IowaMd Rakibul Mowla - University of IowaAriane Rhone - University of IowaSukhbinder Kumar - University of IowaChristopher Kovach - University of IowaJunjie Liu - University of IowaAubrey Chan - University of IowaHiroto Kawasaki - University of IowaRashmi Mueller - University of IowaJustin Kuhn - University of IowaRyan Frede - University of IowaMichael Ciliberto - University of IowaTheresa Czech - University of IowaSreenath Ganganna - University of IowaJames OwensAnia Dabrowski - University of IowaBrittany Sprigg - University of IowaMark Granner - University of IowaKristina Simonyan - Harvard UniversityBryan Krause - University of Wisconsin–MadisonMatthew Banks - University of Wisconsin–MadisonKirill Nourski - University of IowaMatthew Howard - University of IowaPaul Davenport - University of FloridaKyle Pattinson - University of OxfordGeorge Richerson - University of IowaJohn Wemmie - University of Iowa
- Resource Type
- Preprint
- Publication Details
- Research square
- DOI
- 10.21203/rs.3.rs-6568046/v1
- PMID
- 40470175
- PMCID
- PMC12136201
- NLM abbreviation
- Res Sq
- ISSN
- 2693-5015
- eISSN
- 2693-5015
- Language
- English
- Date posted
- 05/14/2025
- Academic Unit
- Roy J. Carver Department of Biomedical Engineering; Neurology; Molecular Physiology and Biophysics; Psychiatry; Clinical Research Unit; Stead Family Department of Pediatrics; Iowa Neuroscience Institute; Anesthesia; Neurology (Pediatrics); Neurosurgery; Otolaryngology; Internal Medicine
- Record Identifier
- 9984826346502771
Metrics
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