Slow Oscillations in the Mouse Hippocampus Entrained by Nasal Respiration

Abstract

Different types of network oscillations occur in different behavioral, cognitive, or vigilance states. The rodent hippocampus expresses prominent θ oscillations at frequencies between 4 and 12 Hz, which are superimposed by phase-coupled γ oscillations (30-100 Hz). These patterns entrain multineuronal activity over large distances and have been implicated in sensory information processing and memory formation. Here we report a new type of oscillation at near-θ frequencies (2-4 Hz) in the hippocampus of urethane-anesthetized mice. The rhythm is highly coherent with nasal respiration and with rhythmic field potentials in the olfactory bulb: hence, we called it hippocampal respiration-induced oscillations. Despite the similarity in frequency range, several features distinguish this pattern from locally generated θ oscillations: hippocampal respiration-induced oscillations have a unique laminar amplitude profile, are resistant to atropine, couple differently to γ oscillations, and are abolished when nasal airflow is bypassed by tracheotomy. Hippocampal neurons are entrained by both the respiration-induced rhythm and concurrent θ oscillations, suggesting a direct interaction between endogenous activity in the hippocampus and nasal respiratory inputs. Our results demonstrate that nasal respiration strongly modulates hippocampal network activity in mice, providing a long-range synchronizing signal between olfactory and hippocampal networks.