Abstract

Several recent studies have shown that respiration modulates oscillatory neuronal activity in the neocortex and hippocampus on a cycle-by-cycle basis. It was suggested that this respiratory influence on neuronal activity affects cognitive functions, including memory. Sharp-wave ripples (SWRs) are high-frequency local field potential activity patterns characteristic for the hippocampus and implicated in memory consolidation and recall. Here we show that the timing of SWR events is modulated by the respiratory cycle, with a significantly increased probability of SWRs during the early expiration phase. This influence of respiration on SWR occurrence was eliminated when olfactory bulb activity was inhibited. Our findings represent a possible neuronal mechanism for a direct influence of the respiratory cycle on memory function.

Highlights

  • In their 2006 opinion piece, Fontanini and Bower suggested that respiration-locked neuronal oscillations, which the olfactory bulb (OB) generates with almost every breath, might propagate throughout the entire neocortex via the olfactory system, creating a direct link between respiration and cortical neuronal rhythms[1]

  • In this study we provide the first evidence that hippocampal Sharp-wave ripples (SWRs) generation is modulated by respiration and that the influence of respiration on SWRs requires normal OB activity

  • Our evidence is based on experiments involving the simultaneous observation of hippocampal SWR activity and respiratory behavior in awake, head-fixed mice

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Summary

Introduction

In their 2006 opinion piece, Fontanini and Bower suggested that respiration-locked neuronal oscillations, which the olfactory bulb (OB) generates with almost every breath, might propagate throughout the entire neocortex via the olfactory system, creating a direct link between respiration and cortical neuronal rhythms[1]. In a recent study Zelano and colleagues showed that memory recall in humans is modulated by their respiratory phase, with subjects showing the most reliable memory recall of memorized items when they were presented during the inspiratory phase[27]. This effect occurred only when subjects were breathing through the nose, suggesting that respiration-locked OB activity was a necessary factor[27]. We asked whether hippocampal SWR activity is modulated by respiration and whether respiratory influence on SWR activity required OB activation To this end we performed extracellular recordings in the dorsal hippocampal CA1 region in awake head-fixed mice while simultaneously monitoring respiration. The role of olfactory bulb activity was evaluated using designer receptors exclusively activated by designer drugs (DREADDs)[28] to inhibit respiration-locked activity in the OB

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