The deep and slow breathing characterizing rest favors brain respiratory-drive

Abstract

A respiration-locked activity in the olfactory brain, mainly originating in the mechano-sensitivity of olfactory sensory neurons to air pressure, propagates from the olfactory bulb to the rest of the brain. Interestingly, changes in nasal airflow rate result in reorganization of olfactory bulb response. Therefore, if the respiratory drive of the brain originates in nasal airflow movements, then it should vary with respiration dynamics that occur spontaneously during natural conditions. We took advantage of the spontaneous variations of respiration dynamics during the different waking and sleep states to explore respiratory drive in various brain regions. We analyzed their local field potential activity relative to respiratory signal. We showed that respiration regime was state-specific, and that quiet waking was the only vigilance state during which all the recorded structures can be respiration-driven whatever the respiration frequency. We used a CO2-enriched air to change the respiratory regime associated to each state and, using a respiratory cycle-by-cycle analysis, we evidenced that the large and strong brain entrainment during quiet waking was the consequence of its associated respiration regime consisting in an optimal trade-off between deepness and duration of inspiration. These results show for the first time that changes in respiration regime alter the cortical dynamics and that the respiratory regime associated with rest is optimal for respiration to drive the brain.

Respiratory coupling between prefrontal cortex and hippocampus of rats anaesthetized with urethane in theta and non‐theta states

“…The animals were breathing spontaneously. The respiratory rate was below 2 Hz (Figure 1), similar to that in unanaesthetized rats during sleep (Cavelli et al, 2020; Girin et al, 2021; Mofleh & Kocsis, 2021), 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 dia autospectra (Figure 2a). Notably, RRO frequency was below that in waking (Mofleh & Kocsis, 2021), even in ‘active states’ under urethane.…”

“…Respiratory‐related oscillations (RROs) are generated in the olfactory bulb (OB), monitoring the nasal airflow, and are then conveyed to forebrain networks, including prefrontal cortex (PFC) and HC (Tort et al, 2018). 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 (Cavelli et al, 2020; Girin et al, 2021; Mofleh & Kocsis, 2021) and in studies focusing on selected states (Biskamp et al, 2017; Rojas‐Libano et al, 2018; Viczko et al, 2014). It is strongest in waking, especially at rest associated with non‐theta activity in the HC.…”

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.…”