Nasal respiration entrains human limbic oscillations and modulates cognitive function

Christina Zelano*, Heidi Jiang, Guangyu Zhou, Nikita Arora, Stephan Schuele, Joshua Rosenow, Jay A. Gottfried

*Corresponding author for this work

Research output: Contribution to journalArticle

73 Scopus citations

Abstract

The need to breathe links the mammalian olfactory system inextricably to the respiratory rhythms that draw air through the nose. In rodents and other small animals, slow oscillations of local field potential activity are driven at the rate of breathing (~2-12 Hz) in olfactory bulb and cortex, and faster oscillatory bursts are coupled to specific phases of the respiratory cycle. These dynamic rhythms are thought to regulate cortical excitability and coordinate network interactions, helping to shape olfactory coding, memory, and behavior. However, while respiratory oscillations are a ubiquitous hallmark of olfactory system function in animals, direct evidence for such patterns is lacking in humans. In this study, we acquired intracranial EEG data from rare patients (Ps) with medically refractory epilepsy, enabling us to test the hypothesis that cortical oscillatory activity would be entrained to the human respiratory cycle, albeit at the much slower rhythm of ~0.16-0.33 Hz. Our results reveal that natural breathing synchronizes electrical activity in human piriform (olfactory) cortex, as well as in limbic-related brain areas, including amygdala and hippocampus. Notably, oscillatory power peaked during inspiration and dissipated when breathing was diverted from nose to mouth. Parallel behavioral experiments showed that breathing phase enhances fear discrimination and memory retrieval. Our findings provide a unique framework for understanding the pivotal role of nasal breathing in coordinating neuronal oscillations to support stimulus processing and behavior.

Original languageEnglish (US)
Pages (from-to)12448-12467
Number of pages20
JournalJournal of Neuroscience
Volume36
Issue number49
DOIs
StatePublished - Dec 7 2016

    Fingerprint

Keywords

  • Amygdala
  • Hippocampus
  • Local field potential
  • Piriform cortex
  • Respiration
  • Respiratory oscillations

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this