Nasal Respiration is Necessary for the Generation of γ Oscillation in the Olfactory Bulb

Abstract γ oscillations (30–120 Hz) are generated intrinsically within local networks in the mammalian olfactory bulb (OB). The OB directly receives peripheral input from olfactory sensory neurons (OSNs) that can respond to nasal airflow, and centrifugal input from neuromodulatory systems whose activities are affected by the behavioral states of animal. How peripheral and centrifugal input dynamically modulate γ oscillations is unclear. By simultaneously recording respiration signal and local field potentials (LFPs) in the OB of freely moving mice throughout at least one sleep–wake cycle, we observed that γ oscillations were highest during awake exploratory (AE) state, and successively lower during awake resting (AR) state, rapid eye movement (REM) and non-REM (NREM) sleep. γ activity was further enhanced when animals were exposed to stress condition, which indicated that behavioral states may modulate γ oscillations. Moreover, γ amplitude was phase-locked to respiration-entrained rhythms (RR). RR-high γ (55–120 Hz) coupling strength was strongest during AR state, while RR-low γ (30–55 Hz) coupling strength was strongest during REM sleep. However, in the absence of nasal respiratory input, γ oscillations dramatically decreased or disappeared, and γ power was no longer modulated by behavioral states. Conversely, hippocampal γ oscillations were not altered by nasal respiratory input. These results reveal that nasal respiratory input is necessary for the generation and modulation of γ oscillations in the OB, suggesting that nasal respiration may modulate neural activity and further influence olfactory function.