Breathing coordinates cortical and subcortical network dynamics

Abstract

During offline states, cortical and hippocampal networks are dominated by nonlinear dynamics, such as hippocampal ripples and neocortical DOWN/UP states. The coordination of these network dynamics underlies memory reactivation and information transfer and is believed to be critical for the consolidation of memories. However, the mechanisms underlying such persistent coordination of the dynamics across global brain networks are poorly understood. A global pacemaker has been postulated as an effective solution to the coupling of distinct nonlinear network dynamics, but the neural implementation of such a mechanism remains elusive. Here we address the hypothesis that respiration acts as an oscillatory master clock, persistently coupling distributed brain circuit dynamics. Using large-scale recordings from the prefrontal cortex, hippocampus, amygdala, nucleus accumbens, and thalamus in behaving mice, we demonstrate that respiration entrains the activity in all these regions, giving rise to global synchronization. In parallel, it mediates the interaction of local network dynamics, including hippocampal ripples and cortical DOWN/UP states, as well as gamma oscillations, during quiescence and sleep, effectively providing the substrate for coherent systems memory consolidation across distributed brain structures. Further, using pharmacological manipulations and analytical methods, we identify a novel joint circuit mechanism underlying the respiratory entrainment of the limbic circuits, in the form of an intracerebral respiratory corollary discharge (RCD) and a respiratory olfactory reafference (ROR), suggesting a distributed predictive signaling mechanism across cortical and subcortical networks. These results highlight breathing, a perennial brain rhythm, as an oscillatory scaffold for the functional coordination of the limbic circuit, enabling the segregation and integration of information flow across neuronal networks and coordinating memory consolidation processes.

Publication
In Neurizons 2020