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Focus on the REM Sleep Behavior Disorder (RBD)

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Focus on the REM Sleep Behavior Disorder (RBD) Sleep phenotyping of the animal models of neurodegenerative diseases: Focus on the REM sleep behavior disorder (RBD) Pierre-Hervé Luppi, Team "Physiopathology of the neuronal network of the sleep-waking cycle” Centre of Neuroscience of Lyon UMR 5292 CNRS/U1028 INSERM , Lyon, France Michel Jouvet: the father of paradoxical (REM) sleep and RBD! 16 November 1925- 3 October 2017 CNRS Research Director (full time researcher) 2011- Head of the Team “Physiopathology of the neuronal network of the sleep-waking cycle" of the Center of Neuroscience of Lyon, UMR 5292 CNRS/U1028 INSERM, Université Claude Bernard Lyon 1, France. 2002-2010: Director of the CNRS laboratory UMR5167, University Claude Bernard Lyon I. 1999 – 2001 Director of Research (DR2), CNRS, INSERM U52, University Claude Bernard Lyon I. 1989 – 1999 CR1 CNRS, INSERM U52, University Claude Bernard Lyon I. 1984 – 1989 PhD in Neurosciences, University Claude Bernard Lyon I. Michel Jouvet, Advisor. 1990-911983 – 1984Visiting DEA (Master) scientist Neuroscience, (6 months in Universitytotal) at the Claude Department Bernard of Lyon I. MentalMichel Jouvet,Health Sciences,Advisor. Hahnemann University, Philadelphia, USA (Pr. ASTON-JONES), Study of the afferents to the locus coeruleus. 1992 Invited scientist (6 months), at the Brain Research Institute, UCLA, Los Angeles, USA. (Dr. MICHAEL CHASE), Study of the glycinergic neurons responsible for muscle atonia of paradoxical sleep. What is paradoxical (REM) sleep (PS)? Waking SWS or nonREM sleep EEG EEG EMG EMG EOG EOG Paradoxical (REM) sleep EEG EMG EOG total sleep 12h50 (SWS 10h50 min - PS2h00 min) Hypnogram of 24h PS SWS W 07h00 19h00 07h00 A paradoxical (REM) sleep (PS)-like state with muscle atonia is still present in ªpontine catsº: muscle atonia of PS is generated by a brainstem circuit Jouvet, 1962, Arch. Ital. Biol. SLD The SLD generates PS SLD: sublaterodorsal tegmental nucleus ± SubC: subcoeruleus nucleus Peri-LCa: nucleus peri-LC alpha A: intact animal PIA: pontine inhibitory area B: total decortication (pontine cat) NPO: nucleus pontis oralis C: mesencephalic section The lesion of SLD in cats induces PS without atonia (RWA) and REM sleep behavior disorder (RBD) like behavior: Sastre et coll., 1979, Physiology & Behavior These results indicate that motoneurones 1) are tonically inhibited during PS by a pathway arising from the SLD 2) are phasically excited by a pathway (originating from the cortex?) Rem Behavior Disorder Courtesy of Dario Arnaldi University of Genoa, IT Mark Mahowald and Carlos Schenck 1985 REM sleep behaviour disorder (RBD): Is the motor cortex inducing the movements? Which type of neurons degenerate? SLD? CORTICAL ACTIVATION Motor cortex SLD W-on neurons PS-on neurons Inhibitory pathways SWS-on neurons PS-off neurons Excitatory pathways MUSCLE ATONIA Identification of the neuronal circuit responsible for muscle atonia and movements during PS is required What is the Neurotransmitter of the PS-on neurons of the SLD ? Glutamate, acetylcholine or GABA? « In situ » hybridization of vesicular glutamate transporter 2 (vGlut2), GAD67 or ChAt immunohistochemistry combined with CFos immunohistochemistry after PS hypersomnia SLD section stained with vGlut2 and CFos PS deprivation Control PS Mean PS quantities SWS - Control : 14,6% W PS Deprivation SWS - Deprivation : 0% l W CFos/vGlut2 neurons Rebound PS SWS - Rebound : 50,4% W 13 h 16 h Conclusion: SLD PS-on neurons express only vGlut 2 and are glutamatergic Clement et al., 2011 Ascending and descending projections of the SLD PS-on neurons GiV ITha The SLD neurons activated during PS project caudally to the ventral gigantocellular nucleus (GiV) but not rostrally to the thalamic intralaminar nuclei (Itha) Neuronal circuit responsible for muscle atonia during PS CORTICAL ACTIVATION Motor cortex IntralaminarIntralaminar thalamic nuclei SLD Glutamate GiV Gly/GABA? Spinal motoneurons W-on neurons PS-on neurons Inhibitory pathways SWS-on neurons PS-off neurons Excitatory pathways MUSCLE ATONIA REM sleep behaviour disorder (RBD): SLD glutamatergic descending neurons degenerate? Inactivation of SLD glutamatergic neurons with adeno-associated virus (AAVs) carrying short-hairpin RNA (shRNA) targeting vesicular glutamate transporter 2 Control shRNA vglut2 Location with mCherry of AAVs inJection sites centered on the SLD of control (n=5) and vGluT2- rats (n=5) Expression of vGluT2 mRNAs within SLD Note the lack of cell body labeling in the SLD of vGluT2- versus ctrl mice. The new genetic method used induces a permanent inactivation of glutamatergic transmission in neurons of the SLD in ratsCollaboration with Michael Lazarus, Tsukuba, Valencia Garcia et al., Brain, 2017 Daily percentage of vigilance states and number of sleep bouts in vGluT2- vs control rats 30 days post shRNA injection. W, PS and SWS quantities (24h) Number of SWS and PS episodes The removal of vGluT2 from glutamatergic SLD neurons induces only a 30% decrease in PS quantities in vGluT2- rats Glutamatergic neurons of the SLD are not the only neurons generating PS? Collaboration with Michael Lazarus, Tsukuba, Valencia Garcia et al., Brain, 2017 The inactivation of glutamate transmission of SLD neurons in rats using short hairpin RNA for vglut2 induces REM sleep without atonia (RWA) and RBD like behaviors Collaboration with Michael Lazarus, Tsukuba, Valencia Garcia et al., Brain, 2017 How SLD glutamatergic neurons generate muscle atonia? A. Control Paradoxical sleep EEG EOG PGO EMG ControlStrychnine Membrane -60 potential B. Strychnine -70 30 s EEG EOG SWS PGO PS EMG Membrane -60 potential (SoJa et al., 1991) -70 Effect of strychnine (glycine antagonist) application during PS on spinal motoneurons in cats Glycinergic premotoneurons are hyperpolarizing motoneurones during PS Localisation of the glycine neurons specifically active during PS hypersomnia? Glycine transporter 2 (GlyT2) is a specific marker of glycine neurons Expression of GlyT2 mRNAs in GiV and spinal cord neurons Only the glycine neurons of the ventral gigantocellular reticular nucleus (GiV) are specifically active during PS rebound Localisation of the neurons active during PS hypersomnia and projecting to the lumbar motoneurons Neurons of the GiV specifically activated during PS send direct projections to lumbar motoneurons Résultats The glycinergic neurons responsible for PS atonia are likely also GABAergic Gi V Fos/GAD « in situ » GiV PSC PSD PSR Sapin et al., 2009 Neuronal circuit responsible for muscle atonia during PS: role of the GABA/glycinergic neurons of the Giv? CORTICAL ACTIVATION Motor cortex SLD Glutamate GiV Gly/GABA Spinal motoneurons W-on neurons PS-on neurons Inhibitory pathways SWS-on neurons PS-off neurons Excitatory pathways MUSCLE ATONIA REM sleep behaviour disorder (RBD): GiV GABA/glycinergic descending neurons degenerate? Inactivation of the vesicular GABA/glycine transporter (vGAT) in GiV neurons using transfection with adenoviral vector of short hairpin RNA targeting the vGAT mRNA GiV GiV Neurons lack expression of vGAT mRNA in the RMg, GiA and GiV in shRNA inJected rats Valencia Garcia et al., Nat. Com., 2018 Second model of RBD: VGAT knockout in the GiV induces PS without atonia and RBD. Collaboration with Michael Lazarus, Tsukuba, Valencia Garcia et al., Nat. Com., 2018 In summary: The glutamatergic neurons of the SLD and the GABA/glycinergic neurons of the GiV are responsible for muscle atonia during PS Their degeneration can be responsible for RBD What is generating the movements? Motor cortex? CORTICAL ACTIVATION Motor cortex IntralaminarIntralaminar thalamic nuclei SLD GlutamateX GiV Gly/GABAX Spinal motoneurons W-on neurons PS-on neurons Inhibitory pathways SWS-on neurons PS-off neurons Excitatory pathways MUSCLE ATONIA Review ARticle Alternative hypothesis published: 01 November 2010 doi: 10.3389/fneur.2010.00140 Beyond dreams: do sleep-related movements contribute to brain development? Mark S. Blumberg* Department of Psychology and Delta Center, The University of Iowa, Iowa City, IA, USA In newborn rats, motor cortex is not mature and the animals still show muscle twitches after mesencephalic section Adult cats with mesencephalic section still show REMs and muscle twitching Hypothesis: A brainstem system generate the movement and the sensory feedback from the vigorous movements trigger the violent dreams of RBD without intervention of the motor cortex Study of the distribution and number of neurons activated in the cortex during PS hypersomnia and waking Control 10% of PS Vigilance states PSC quantities (%) PSD 72h 6h PSR PS deprivation 0% # # #** # PS72h hypersomnia6h 32% * W SWS PS 72h 6h Immunohistochemistry Waking 100% of FOS, Arc, Cox-2 « in situ » Hybridation of Bdnf 3h Renouard et al., 2015 Distribution of FOS+ neurons in the hippocampus during PS hypersomnia PS Hypersomnia Waking # Number of FOS+ PSC 250 ** # neurones PSD + + 200 #+ PSR # ** **+ 150 # W # # 100 #** 50 * 0 Dentate gyrus CA3 CA1 PS hypersomnia induces an increase in the number of Fos+ neurons specifically in the dentate gyrus Renouard et al., 2015 Distribution of FOS+ neurons in the somatosensory cortex during PS hypersomnia PS deprivation Waking PS hypersomnia NombreNumber de neurones of FOS+ 4000 neuronsPSC + ## PSD **+ SS 3500 PSR EV 3000 2500 2000 1500 1000 * 500 # # 0Somatosens cortex somatosensorielory cortex Cortical activity is suppressed globally during sleep, being lowest during REM sleep RBD-associated behaviors are reported to occur more frequently during phasic REM sleep Manni et al Sleep 2009; Frauscher et al 2009 Activation
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