Causal relations between cortical network oscillations and breathing frequency

Abstract

Nasal breathing generates a rhythmic signal which entrains cortical network oscillations in widespread brain regions on a cycle-to-cycle time scale. It is unknown, however, how respiration and neuronal network activity interact on a larger time scale: are breathing frequency and typical neuronal oscillation patterns correlated? Is there any directionality or causal relationship? To address these questions, we recorded field potentials from the posterior parietal cortex of mice together with respiration during REM sleep. In this state, the parietal cortex exhibits prominent theta and gamma oscillations while behavioral activity is minimal, reducing confounding signals. We found that the instantaneous breathing rate strongly correlates with the instantaneous frequency and amplitude of both theta and gamma oscillations. Granger causality analysis revealed specific directionalities for different rhythms: changes in theta activity precede and cause changes in breathing rate, suggesting control of breathing frequency by the functional state of the brain. On the other hand, the instantaneous breathing rate Granger-causes changes in gamma oscillations, suggesting that gamma is influenced by a peripheral reafference signal. These findings show that breathing causally relates to different patterns of rhythmic brain activity, revealing new and complex interactions between elementary physiological functions and neuronal information processing. Significance StatementThe study of the interactions between respiration and brain activity has been focused on phase-entrainment relations, in which cortical networks oscillate phase-locked to breathing cycles. Here we discovered new and much broader interactions which link respiration rate (frequency) to different patterns of oscillatory brain activity. Specifically, we show that the instantaneous breathing rate strongly correlates with the instantaneous frequency and amplitude of theta and gamma oscillations, two major network patterns associated with cognitive functions. Interestingly, causality analyses reveal that changes in breathing rate follow theta, suggesting a central drive, while in contrast, gamma activity follows changes in breathing rate, suggesting the role of a reafferent signal. Our results reveal new mechanisms by which nasal breathing patterns may influence brain functions.