Nasal respiration entrains neocortical long‐range gamma coherence during wakefulness

Abstract

Recent studies have shown that slow cortical potentials in archi‐, paleo‐ and neocortex can phase‐lock with nasal respiration. In some of these areas, gamma activity (γ: 30–100 Hz) is also coupled to the animal's respiration. It has been hypothesized that these functional relationships play a role in coordinating distributed neural activity. In a similar way, inter‐cortical interactions at γ frequency have also been associated as a binding mechanism by which the brain generates temporary opportunities necessary for implementing cognitive functions. The aim of the present study is to explore whether nasal respiration entrains inter‐cortical functional interactions at γ frequency during both wakefulness and sleep. Six adult cats chronically prepared for electrographic recordings were employed in this study. Our results show that during wakefulness, slow cortical respiratory potentials are present in the olfactory bulb and several areas of the neocortex. We also found that these areas exhibit cross‐frequency coupling between respiratory phase and γ oscillation amplitude. We demonstrate that respiratory phase modulates the inter‐cortical gamma coherence between neocortical electrode pairs. On the contrary, slow respiratory oscillation and γ cortical oscillatory entrainments disappear during non‐rapid eye movement and rapid eye movement sleep. These results suggest that a single unified phenomenon involves cross‐frequency coupling and long‐range γ coherence across the neocortex. This fact could be related to the temporal binding process necessary for cognitive functions during wakefulness.

Communication Through Coherence by Means of Cross-frequency Coupling

“…In addition to these findings in humans, Bosman et al (2012) provided preliminary evidence from two macaque monkeys showing that V1-V4 coherence at 70-80 Hz depends on the time from the peaks of the 3-5 Hz-filtered LFP component. Furthermore, we have also recently shown that the phase of respiratory activity modulates low gamma synchrony in the awake cat (Cavelli et al, 2019). Altogether, the current and previous evidence suggests that the rhythmic modulation of phase synchrony may be a general brain mechanism preserved across species.…”

Respiratory coupling between prefrontal cortex and hippocampus of rats anesthetized with urethane in theta and non-theta states

“…The respiratory rate was below 2 Hz (Fig. 1), similar to that in unanesthetized rats during sleep 7,34,35 , and remained stable over alternating theta and non-theta states (1.80±0.14 and 1.73±0.14 Hz, respectively; Table 1), resulting in a single sharp peak in the diaphragmal (dia) autospectra (Fig. 2A).…”

“…Lack of RRO under urethane was occasionally reported in previous studies, but only in deep anesthesia characterized by slow neocortical up-down transitions 36, 46 , i.e. a pattern similar to natural slow wave sleep, where however RRO remains absent after switching to theta-rich REM sleep 7,34,35 . Under urethane anesthesia, both OB-PFC and OB-HC coherences showed strong correlations with dia-OB coherence in both theta and non-theta states, again violating the correspondence, commonly expected on the basis of EEG signals, between urethane-theta and AW-REM on one hand and between urethane non-theta and QW-SWS on the other.…”

“…Respiratory related oscillations (RRO) are generated in the olfactory bulb (OB), monitoring the nasal airflow, and are then conveyed to forebrain networks, including prefrontal cortex (PFC) and HC 1 . Relatively stable slow (~2 Hz) RRO, present outside of the transient sniffing episodes, strongly depends on sleep-wake states, as shown in studies monitoring respiration along with polysomnography over all sleep-wake states in the same animal 7,34,35 as well as in studies focusing on selected states 2, 8, 36 . It is strongest in waking, especially at rest associated with non-theta activity in the HC.…”

“…Respiratory modulation of forebrain activity, long considered hard to reliably separate from breathing artifacts, has been firmly established in recent years 1 , using a variety of advanced techniques, including single unit firing [2][3][4] , phase modulation of local gamma activity 2,3,[5][6][7] , and current source density analysis 4,8 . Many of these observations in awake or sleeping animals were preceded, supplemented, or verified under urethane anesthesia 9,10 , which besides providing a stable preparation, allows additional manipulations, e.g.…”