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 language | English (US) |
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Pages (from-to) | 12448-12467 |
Number of pages | 20 |
Journal | Journal of Neuroscience |
Volume | 36 |
Issue number | 49 |
DOIs | |
State | Published - Dec 7 2016 |
Funding
This work was funded by National Institutes of Health Grants R00-DC-012803 (to C.Z.), and R21-DC-012014 and R01-DC-013243 (to J.A.G.), and a National Science Foundation Graduate Research Fellowship Program grant (to H.J.). We thank Enelsa Lopez, Jeremy Eagles, and all of the clinical staff in the Comprehensive Epilepsy Center at Northwestern Memorial Hospital for their invaluable help with technical aspects of intracranial EEG data collection. We also thank Thorsten Kahnt and Marc Slutzky for their comments on the manuscript.
Keywords
- Amygdala
- Hippocampus
- Local field potential
- Piriform cortex
- Respiration
- Respiratory oscillations
ASJC Scopus subject areas
- General Neuroscience