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Neurons in the Nucleus papilio contribute to the control of eye movements during REM sleep.

ABSTRACT: Rapid eye movements (REM) are characteristic of the eponymous phase of sleep, yet the underlying motor commands remain an enigma. Here, we identified a cluster of Calbindin-D28K-expressing neurons in the Nucleus papilio (NP^Calb), located in the dorsal paragigantocellular nucleus, which are active during REM sleep and project to the three contralateral eye-muscle nuclei. The firing of opto-tagged NP^Calb neurons is augmented prior to the onset of eye movements during REM sleep. Optogenetic activation of NP^Calb neurons triggers eye movements selectively during REM sleep, while their genetic ablation or optogenetic silencing suppresses them. None of these perturbations led to a change in the duration of REM sleep episodes. Our study provides the first evidence for a brainstem premotor command contributing to the control of eye movements selectively during REM sleep in the mammalian brain.

SUBMITTER: Gutierrez Herrera C

PROVIDER: S-EPMC6864097 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Neurons in the Nucleus papilio contribute to the control of eye movements during REM sleep.

Gutierrez Herrera C C Girard F F Bilella A A Gent T C TC Roccaro-Waldmeyer D M DM Adamantidis A A Celio M R MR

Nature communications 20191119 1

Rapid eye movements (REM) are characteristic of the eponymous phase of sleep, yet the underlying motor commands remain an enigma. Here, we identified a cluster of Calbindin-D28K-expressing neurons in the Nucleus papilio (NP<sup>Calb</sup>), located in the dorsal paragigantocellular nucleus, which are active during REM sleep and project to the three contralateral eye-muscle nuclei. The firing of opto-tagged NP<sup>Calb</sup> neurons is augmented prior to the onset of eye movements during REM slee ...[more]

PMID: 31745081

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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.

Dataset Information

Neurons in the Nucleus papilio contribute to the control of eye movements during REM sleep.

Publications

Neurons in the Nucleus papilio contribute to the control of eye movements during REM sleep.

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