Abstract

Network dynamics have been proposed as a mechanistic substrate for the information transfer across cortical and hippocampal circuits. However, little is known about the mechanisms that synchronize and coordinate these processes across widespread brain regions during offline states. Here we address the hypothesis that breathing acts as an oscillatory pacemaker, persistently coupling distributed brain circuit dynamics. Using large-scale recordings from a number of cortical and subcortical brain regions in behaving mice, we uncover the presence of an intracerebral respiratory corollary discharge, that modulates neural activity across these circuits. During offline states, the respiratory modulation underlies the coupling of hippocampal sharp-wave ripples and cortical DOWN/UP state transitions, which mediates systems memory consolidation. These results highlight breathing, a perennial brain rhythm, as an oscillatory scaffold for the functional coordination of the limbic circuit that supports the segregation and integration of information flow across neuronal networks during offline states.

Highlights

  • Network dynamics have been proposed as a mechanistic substrate for the information transfer across cortical and hippocampal circuits

  • Given the nuclear nature and lack of lamination of these structures, which obfuscates the interpretation of slow local field potentials (LFP) oscillations, we examined the modulation of single-unit activity by the phase of breathing, revealing that a large proportion of basolateral amygdala (BLA), nucleus accumbens (NAc), and thalamic neurons were significantly modulated by respiration, notably firing in distinct phases of the breathing cycle (Fig. 3j–n)

  • The propagation of information across distinct neuronal networks is facilitated by the coordination of these dynamics between brain regions[5,7]

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Summary

Introduction

Network dynamics have been proposed as a mechanistic substrate for the information transfer across cortical and hippocampal circuits. Using multiregional recordings of local field potentials (LFP) and large-scale neural population activity we performed an anatomicallyresolved, in vivo, functional dissection of the offline state dynamics in the medial prefrontal cortex (mPFC), hippocampus, basolateral amygdala (BLA), nucleus accumbens (NAc), visual cortex, and thalamic nuclei Using this approach, combined with pharmacological manipulation, we describe the widespread respiratory entrainment of the limbic circuit and we suggest the existence of an intracerebral centrifugal respiratory corollary discharge that mediates the inter-regional synchronization of the limbic circuit

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