Respiratory phase orchestrates human olfactory cortical dynamics
Alisa Y Hathaway1, Todd P Coleman2
1Department of Electrical Engineering, Stanford University, Stanford, CA 94305.
Abstract:
Olfaction is fundamental to perception, memory, and emotion, yet the neural basis of human odor processing remains poorly understood. We demonstrate that odor-evoked brain activity is organized by respiratory phase-not absolute time-revealing that natural breathing structures olfactory cortical dynamics. Using simultaneous nasal respiration and electroencephalography recordings in [Formula: see text] participants, we delivered naturalistic odors (peppermint, oregano, and grapefruit) synchronized to individual breathing cycles. Odor presentation elicited respiratory phase-locked event-related spectral perturbations (RPL-ERSPs) in frontal and temporal regions, emerging during the first breath after stimulus onset. The most discriminative neural signatures were theta-band activity during inhalation and alpha-band activity during exhalation, patterns that were obscured in traditional time-locked analyses due to natural variability in breath duration. Leave-one-subject-out cross-validation of RPL-ERSPs achieved reliable odor detection (peppermint: AUC [Formula: see text] 0.79; oregano: AUC [Formula: see text] 0.67; grapefruit: AUC [Formula: see text] 0.62), establishing that phase-locked features generalize across individuals. To connect neural responses to perceptual experience without relying on odor naming-which can be disproportionately impaired in some populations-we quantified odor recognition using free-response descriptions scored with a semantic-similarity approach. Behavioral recognition strength paralleled the neural decoding hierarchy across odors, establishing the perceptual validity of RPL-ERSPs. RPL-ERSPs revealed rapid habituation, with decoding performance declining over repeated presentations, due to selective degradation of the most informative phase-locked features. These findings establish respiratory rhythm as a temporal scaffold for human olfactory cortical processing, positioning RPL-ERSPs as a sensitive, task-free approach for assessing olfactory function. We provide an open-source, respiration-synchronized olfactometer design to enable replication and adoption.
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