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The supramammillary nucleus and the claustrum activate the cortex during REM sleep.

ABSTRACT: Evidence in humans suggests that limbic cortices are more active during rapid eye movement (REM or paradoxical) sleep than during waking, a phenomenon fitting with the presence of vivid dreaming during this state. In that context, it seemed essential to determine which populations of cortical neurons are activated during REM sleep. Our aim in the present study is to fill this gap by combining gene expression analysis, functional neuroanatomy, and neurochemical lesions in rats. We find in rats that, during REM sleep hypersomnia compared to control and REM sleep deprivation, the dentate gyrus, claustrum, cortical amygdaloid nucleus, and medial entorhinal and retrosplenial cortices are the only cortical structures containing neurons with an increased expression of Bdnf, FOS, and ARC, known markers of activation and/or synaptic plasticity. Further, the dentate gyrus is the only cortical structure containing more FOS-labeled neurons during REM sleep hypersomnia than during waking. Combining FOS staining, retrograde labeling, and neurochemical lesion, we then provide evidence that FOS overexpression occurring in the cortex during REM sleep hypersomnia is due to projections from the supramammillary nucleus and the claustrum. Our results strongly suggest that only a subset of cortical and hippocampal neurons are activated and display plasticity during REM sleep by means of ascending projections from the claustrum and the supramammillary nucleus. Our results pave the way for future studies to identify the function of REM sleep with regard to dreaming and emotional memory processing.

SUBMITTER: Renouard L

PROVIDER: S-EPMC4640625 | biostudies-literature | 2015 Apr

REPOSITORIES: biostudies-literature

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The supramammillary nucleus and the claustrum activate the cortex during REM sleep.

Renouard Leslie L Billwiller Francesca F Ogawa Keiko K Clément Olivier O Camargo Nutabi N Abdelkarim Mouaadh M Gay Nadine N Scoté-Blachon Céline C Touré Rouguy R Libourel Paul-Antoine PA Ravassard Pascal P Salvert Denise D Peyron Christelle C Claustrat Bruno B Léger Lucienne L Salin Paul P Malleret Gael G Fort Patrice P Fort Patrice P Luppi Pierre-Hervé PH

Science advances 20150403 3

Evidence in humans suggests that limbic cortices are more active during rapid eye movement (REM or paradoxical) sleep than during waking, a phenomenon fitting with the presence of vivid dreaming during this state. In that context, it seemed essential to determine which populations of cortical neurons are activated during REM sleep. Our aim in the present study is to fill this gap by combining gene expression analysis, functional neuroanatomy, and neurochemical lesions in rats. We find in rats th ...[more]

PMID: 26601158

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Project description:We experience disturbed sleep in a new place, and this effect is known as the first-night effect (FNE) in sleep research. We previously demonstrated that the FNE is associated with a surveillance system in one brain hemisphere during NREM sleep, which manifests as interhemispheric asymmetry in sleep depth in the default-mode network (DMN) and increased vigilance toward monitoring external stimuli. This surveillance system may be useful for protecting vulnerable sleepers from abnormal events in unfamiliar environments. The present study investigated whether a similar surveillance system is exhibited during rapid eye movement (REM) sleep. The impacts of the FNE could be different between the phasic period, in which eyes move rapidly, and the tonic period, in which eye movement ceases, of REM sleep; without the FNE, vigilance to external stimuli is generally reduced during the phasic period but not the tonic period. Thus, REM sleep was split into phasic and tonic periods. First, we replicated previous findings showing interhemispheric asymmetry in delta activity in the DMN associated with the FNE during NREM sleep. However, during REM sleep, interhemispheric asymmetry in delta activity or theta activities, two oscillatory activities during REM sleep, was not found during the phasic or tonic periods. Next, we tested whether vigilance, as measured by evoked brain responses (P2) to deviant tones, associated with the FNE was increased in one hemisphere during REM sleep. The P2 amplitudes during the phasic period were augmented by the FNE on day 1 and were significantly larger than those on day 2 when the FNE was not present. In contrast, the P2 amplitudes during the tonic period were not different across days. The P2 amplitudes showed no interhemispheric asymmetry during the phasic or tonic periods. These results suggest that while the surveillance system exhibits interhemispheric asymmetry in sleep depth and vigilance during NREM sleep, this system shows no interhemispheric asymmetry in oscillatory activities and exhibits increased vigilance in both hemispheres only during the phasic period of REM sleep. Therefore, the surveillance system associated with the FNE may involve different mechanisms during NREM and REM sleep.

Project description:It is widely accepted that cortical neurons are similarly more activated during waking and paradoxical sleep (PS; aka REM) than during slow-wave sleep (SWS). However, we recently reported using Fos labeling that only a few limbic cortical structures including the retrosplenial cortex (RSC) and anterior cingulate cortex (ACA) contain a large number of neurons activated during PS hypersomnia. Our aim in the present study was to record local field potentials and unit activity from these two structures across all vigilance states in freely moving male rats to determine whether the RSC and the ACA are electrophysiologically specifically active during basal PS episodes. We found that theta power was significantly higher during PS than during active waking (aWK) similarly in the RSC and hippocampus (HPC) but not in ACA. Phase-amplitude coupling between HPC theta and gamma oscillations strongly and specifically increased in RSC during PS compared with aWK. It did not occur in ACA. Further, 68% and 43% of the units recorded in the RSC and ACA were significantly more active during PS than during aWK and SWS, respectively. In addition, neuronal discharge of RSC but not of ACA neurons increased just after the peak of hippocampal theta wave. Our results show for the first time that RSC neurons display enhanced spiking in synchrony with theta specifically during PS. We propose that activation of RSC neurons specifically during PS may play a role in the offline consolidation of spatial memories, and in the generation of vivid perceptual scenery during dreaming.SIGNIFICANCE STATEMENT Fifty years ago, Michel Jouvet used the term paradoxical to define REM sleep because of the simultaneous occurrence of a cortical activation similar to waking accompanied by muscle atonia. However, we recently demonstrated using functional neuroanatomy that only a few limbic structures including the retrosplenial cortex (RSC) and anterior cingulate cortex (ACA) are activated during PS. In the present study, we show for the first time that the RSC and ACA contain neurons firing more during PS than in any other state. Further, RSC neurons are firing in phase with the hippocampal theta rhythm. These data indicate that the RSC is very active during PS and could play a key role in memory consolidation taking place during this state.

Dataset Information

The supramammillary nucleus and the claustrum activate the cortex during REM sleep.

Publications

The supramammillary nucleus and the claustrum activate the cortex during REM sleep.

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