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Research Articles, Behavioral/Cognitive

A Discrete Glycinergic Neuronal Population in the Ventromedial Medulla That Induces Muscle Atonia during REM Sleep and Cataplexy in Mice

Shuntaro Uchida, Shingo Soya, Yuki C. Saito, Arisa Hirano, Keisuke Koga, Makoto Tsuda, Manabu Abe, Kenji Sakimura and Takeshi Sakurai
Journal of Neuroscience 17 February 2021, 41 (7) 1582-1596; DOI: https://doi.org/10.1523/JNEUROSCI.0688-20.2020
Shuntaro Uchida
1Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan
2International Institute for Integrative Sleep Medicine (WPI-IIIS), University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan
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Shingo Soya
1Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan
2International Institute for Integrative Sleep Medicine (WPI-IIIS), University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan
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  • ORCID record for Shingo Soya
Yuki C. Saito
2International Institute for Integrative Sleep Medicine (WPI-IIIS), University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan
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Arisa Hirano
1Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan
2International Institute for Integrative Sleep Medicine (WPI-IIIS), University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan
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Keisuke Koga
5Department of Life Innovation, Graduate School of Pharmaceutical Sciences, Kyushu University, Fukuoka 812-8582, Japan
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Makoto Tsuda
5Department of Life Innovation, Graduate School of Pharmaceutical Sciences, Kyushu University, Fukuoka 812-8582, Japan
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Manabu Abe
3Department of Cellular Neurobiology, Brain Research Institute, Niigata University, Asahimachi, Chuoku Niigata 951-8585, Japan
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Kenji Sakimura
3Department of Cellular Neurobiology, Brain Research Institute, Niigata University, Asahimachi, Chuoku Niigata 951-8585, Japan
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Takeshi Sakurai
1Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan
2International Institute for Integrative Sleep Medicine (WPI-IIIS), University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan
4Japan Life Science Center for Tsukuba Advanced Research Alliance (TARA), University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan
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Abstract

During rapid eye movement (REM) sleep, anti-gravity muscle tone and bodily movements are mostly absent, because somatic motoneurons are inhibited by descending inhibitory pathways. Recent studies showed that glycine/GABA neurons in the ventromedial medulla (VMM; GlyVMM neurons) play an important role in generating muscle atonia during REM sleep (REM-atonia). However, how these REM-atonia-inducing neurons interconnect with other neuronal populations has been unknown. In the present study, we first identified a specific subpopulation of GlyVMM neurons that play an important role in induction of REM-atonia by virus vector-mediated tracing in male mice in which glycinergic neurons expressed Cre recombinase. We found these neurons receive direct synaptic input from neurons in several brain stem regions, including glutamatergic neurons in the sublaterodorsal tegmental nucleus (SLD; GluSLD neurons). Silencing this circuit by specifically expressing tetanus toxin light chain (TeTNLC) resulted in REM sleep without atonia. This manipulation also caused a marked decrease in time spent in cataplexy-like episodes (CLEs) when applied to narcoleptic orexin-ataxin-3 mice. We also showed that GlyVMM neurons play an important role in maintenance of sleep. This present study identified a population of glycinergic neurons in the VMM that are commonly involved in REM-atonia and cataplexy.

SIGNIFICANCE STATEMENT We identified a population of glycinergic neurons in the ventral medulla that plays an important role in inducing muscle atonia during rapid eye movement (REM) sleep. It sends axonal projections almost exclusively to motoneurons in the spinal cord and brain stem except to those that innervate extraocular muscles, while other glycinergic neurons in the same region also send projections to other regions including monoaminergic nuclei. Furthermore, these neurons receive direct inputs from several brainstem regions including glutamatergic neurons in the sublaterodorsal tegmental nucleus (SLD). Genetic silencing of this pathway resulted in REM sleep without atonia and a decrease of cataplexy when applied to narcoleptic mice. This work identified a neural population involved in generating muscle atonia during REM sleep and cataplexy.

  • atonia
  • cataplexy
  • glycine
  • narcolepsy
  • neural circuit
  • REM sleep

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The Journal of Neuroscience: 41 (7)
Journal of Neuroscience
Vol. 41, Issue 7
17 Feb 2021
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A Discrete Glycinergic Neuronal Population in the Ventromedial Medulla That Induces Muscle Atonia during REM Sleep and Cataplexy in Mice
Shuntaro Uchida, Shingo Soya, Yuki C. Saito, Arisa Hirano, Keisuke Koga, Makoto Tsuda, Manabu Abe, Kenji Sakimura, Takeshi Sakurai
Journal of Neuroscience 17 February 2021, 41 (7) 1582-1596; DOI: 10.1523/JNEUROSCI.0688-20.2020

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A Discrete Glycinergic Neuronal Population in the Ventromedial Medulla That Induces Muscle Atonia during REM Sleep and Cataplexy in Mice
Shuntaro Uchida, Shingo Soya, Yuki C. Saito, Arisa Hirano, Keisuke Koga, Makoto Tsuda, Manabu Abe, Kenji Sakimura, Takeshi Sakurai
Journal of Neuroscience 17 February 2021, 41 (7) 1582-1596; DOI: 10.1523/JNEUROSCI.0688-20.2020
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Keywords

  • atonia
  • cataplexy
  • glycine
  • narcolepsy
  • neural circuit
  • REM sleep

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