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The Transition Between Slow-Wave Sleep and REM Sleep Constitutes an Independent Sleep Stage Organized by Cholinergic Mechanisms in the Rostrodorsal Pontine Tegmentum.

ABSTRACT: There is little information on either the transition state occurring between slow-wave sleep (SWS) and rapid eye movement (REM) sleep, as well as about its neurobiological bases. This transition state, which is known as the intermediate state (IS), is well-defined in rats but poorly characterized in cats. Previous studies in our laboratory demonstrated that cholinergic stimulation of the perilocus coeruleus α nucleus (PLCα) in the pontine tegmentum of cats induced two states: wakefulness with muscle atonia and a state of dissociated sleep we have called the SPGO state. The SPGO state has characteristics in common with the IS, such including the presence of ponto-geniculo-occipital waves (PGO) and EEG synchronization with δ wave reduction. Therefore, the aims of the present study were (1) to characterize the IS in the cat and, (2), to study the analogy between the SPGO and the different sleep stages showing PGO activity, including the IS. Polygraphic recordings of 10 cats were used. In seven cats carbachol microinjections (20-30 nL, 0.01-0.1 M) were delivered in the PLCα. In the different states, PGO waves were analyzed and power spectra obtained for the δ, θ, α, and β bands of the EEG from the frontal and occipital cortices, and for the θ hippocampal band. Statistical comparisons were made between the values obtained from the different states. The results indicate that the IS constitutes a state with characteristics that are distinct from both the preceding SWS and the following REM sleep, and that SPGO presents a high analogy with the IS. Therefore, the SPGO state induced by administering carbachol in the PLCα nucleus seems to be an expression of the physiological IS of the cat. Consequently, we propose that the PLCα region, besides being involved in the mechanisms of muscle atonia, may also be responsible for organizing the transition from SWS to REM sleep.

SUBMITTER: Carrera-Canas C

PROVIDER: S-EPMC6663996 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The activity of hypoglossal motoneurons plays an important role in the maintenance of upper airway patency. Both withdrawal of noradrenergic excitatory drive and increase of cholinergic inhibition markedly decrease excitability of hypoglossal motoneurons during sleep and especially during rapid-eye-movement (REM) stage. This leads to increased collapsibility of upper airway during sleep, which is the major neurological factor of obstructive sleep apnea (OSA) pathophysiology. Anatomical and functional data suggest that noradrenergic A7 neurons are the main source of noradrenergic drive to hypoglossal motoneurons. However, it is unknown whether the behavior of A7 neurons during sleep-wake cycle is in accord with their proposed involvement in sleep-related depression of hypoglossal motoneuron activity. Therefore, we sought to assess the behavior of A7 neurons during sleep and wakefulness in naturally sleeping head-restrained rats. We have found that, similar to other pontine noradrenergic neurons, the putative A7 noradrenergic neurons fired with relatively long-lasting action potentials with a low-frequency regular discharge. Importantly, noradrenergic A7 neurons were predominantly silent during REM sleep. The REM-off activity of the A7 neurons supports our hypothesis that these neurons may significantly contribute to the withdrawal of excitatory noradrenergic drive from upper airway motoneurons during REM sleep and, consequently, play an essential role in maintaining upper airway patency and pathophysiology of OSA. Therefore, noradrenergic A7 neurons may serve as an additional target for designing pharmacological approaches to treat OSA.NEW & NOTEWORTHY Noradrenergic A7 neurons are mostly silent during REM sleep. This is in accord with their role in the control of upper airway muscles and important contribution to OSA pathophysiology. Therefore, a modulation of A7 neuron activity can serve as a novel therapeutic target for pharmacological treatment of OSA.

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The Transition Between Slow-Wave Sleep and REM Sleep Constitutes an Independent Sleep Stage Organized by Cholinergic Mechanisms in the Rostrodorsal Pontine Tegmentum.

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