Synchronization of frontal brain networks by the respiratory rhythm during exploratory behavior in rats

Abstract

Breathing is a fundamental physiological process, yet its significance extends beyond cellular respiration. The rhythmic control of respiration has been associated with cognitive enhancement, increased self-awareness, and relaxation. However, how the breathing pattern relates to the brain and behavior remains unclear. Rodents synchronize sensorimotor rhythms to respiration during active sensing, such as head and whisker movements, suggesting that the breathing cycle could be relevant for environmental neural coding. Here, we characterize how the breathing cycle modulates frontal brain activity during active spontaneous behavior in rats investigating social and object stimuli. To do so, we looked for episodes in which the brain and breathing synchronize in these contexts, called respiratory-coupled oscillations (RCOs). We conducted our experiments in an apparatus composed of two opposing platforms separated by a gap (gap paradigm), where they could interact spontaneously with an object or social stimulus at different times. During the experiments, we simultaneously recorded video, intranasal pressure, and frontal brain electrical activity. First, we analyzed the behavioral variables by tracking the head positions over time to extract occupancy and head speed during resting and active states. During activity, animals were more prone to stay over the gap in social than object contexts. These events were characterized by rats guiding their heads toward the opposite platform while maintaining high respiratory rates (> 5 Hz) characteristic of active sniffing. We performed coherence analysis to measure RCOs in the local-field potentials of the olfactory bulb (OB) and medial-orbital (MO), pre-limbic (PRL), and anterior cingulate (CG) cortices. This revealed levels of coherence to breathing in all brain regions, both in resting and active states, with values generally decreasing from the anterior-most (OB) to the posterior-most regions (CG). Our results show that these areas are distinctly modulated by the breathing cycle across exploratory contexts. We conclude that the breathing cycle is relevant to rat exploratory behavior and that the RCOs could mediate the coordination between respiration, behavior, and cognition.