Is REM sleep a paradoxical state?: Different neurons are activated in the cingulate cortices and the claustrum during wakefulness and paradoxical sleep hypersomnia

Maciel, Renato; Yamazaki, Risa; Wang, Dianru; Laet, Anna De; Cabrera, Sébastien; Agnorelli, Claudio; Arthaud, Sébastien; Libourel, Paul-Antoine; Fort, Patrice; Lee, Hyun Sook; Queiroz, Cláudio Marcos Teixeira de; Luppi, Pierre‐Hervé

doi:10.1016/j.bcp.2021.114514

Cited by 18 publications

(9 citation statements)

References 21 publications

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“…This is in contrast to the quiescence of brain structures, including the prefrontal cortex (PFC), that is associated with the pruning of dendritic spines (11,14), synaptic weakening (15), and forgetting during REM sleep (16)(17)(18). These apparent controversies are the result of the heterogeneity of (sub)cellular activity in limbic (19,20) or cortical structures (4,11,(21)(22)(23), limited cellular resolution of human brain imaging technologies (4)(5)(6), and the lack of selectivity of REM sleep-deprivation procedures (8,24). In this work, we investigated the mechanisms encoding emotional memories during REM sleep within dorsal PFC (dPFC) microcircuits-a critical brain structure for executive functions (25) and discrimination of danger from safety (26).…”

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confidence: 99%

Paradoxical somatodendritic decoupling supports cortical plasticity during REM sleep

Aime

Calcini

Borsa

et al. 2022

Science

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Rapid eye movement (REM) sleep is associated with the consolidation of emotional memories. Yet, the underlying neocortical circuits and synaptic mechanisms remain unclear. We found that REM sleep is associated with a somatodendritic decoupling in pyramidal neurons of the prefrontal cortex. This decoupling reflects a shift of inhibitory balance between parvalbumin neuron–mediated somatic inhibition and vasoactive intestinal peptide–mediated dendritic disinhibition, mostly driven by neurons from the central medial thalamus. REM-specific optogenetic suppression of dendritic activity led to a loss of danger-versus-safety discrimination during associative learning and a lack of synaptic plasticity, whereas optogenetic release of somatic inhibition resulted in enhanced discrimination and synaptic potentiation. Somatodendritic decoupling during REM sleep promotes opposite synaptic plasticity mechanisms that optimize emotional responses to future behavioral stressors.

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confidence: 99%

Paradoxical somatodendritic decoupling supports cortical plasticity during REM sleep

Aime

Calcini

Borsa

et al. 2022

Science

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“…Salivarius has a large number of urea catabolism genes capable of activating urease activity, using urea-derived ammonium as its primary source of nitrogen in the intestine, which may contribute to ammonia accumulation and consequently to hyperammonemia 28 . Hyperammonemia induces astrocyte swelling and subsequent low-grade cerebral edema, and further interferes with the inhibition and activation of associated neural nuclei in the parietal cingulate and bilateral anterior, which play signi cant roles in the REM sleep regulation 29,30 . In the rat model of MHE, Llansola et al reported that hyperammonemia led to signi cantly decreased REM sleep phases and increased sleep fragmentation 31 .…”

Section: Discussionmentioning

confidence: 99%

Altered intestinal microbiota are associated with sleep disturbances in patients with minimal hepatic encephalopathy caused by hepatitis B-related liver cirrhosis

Luo

et al. 2021

Preprint

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Objective Minimal hepatic encephalopathy (MHE) caused by liver cirrhosis is quite prevalent, and approximately one-half of MHE patients have experience sleep disturbances. This study systematically evaluated the association between sleep disturbances and altered intestinal microbiota in patients with MHE caused by hepatitis B-related liver cirrhosis. Methods Ninety-eight and 45 MHE patients were respectively included in the exploration and validation cohorts. The Chinese version of the Pittsburgh Sleep Quality Index (PSQI) questionnaire was used to evaluate sleep disturbances. The intestinal microbiota of self-collected fecal samples was analyzed using the amplicon sequencing of bacterial 16S ribosomal RNA gene. Results MHE patients with sleep disturbances were characterized by lower bacterial diversities and distinct microbial composition in comparison to those without sleep disturbances. The relative abundances of Salivarius, Veillonella, Klebsiella, and Eubacterium were independent predictors of sleep disturbances in MHE patients. In MHE patients with sleep disturbances, the relative abundances of Salivarius and Veillonella were positively correlated with PSQI scores, respectively. Functional modules involved in lipopolysaccharide biosynthesis, as well as protein digestion and absorption, were increased in the microbiome of MHE patients with sleep disturbances. Conclusion Salivarius and Veillonella may be potential diagnostic biomarkers and therapeutic targets for sleep disturbances in MHE patients.

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“…However, using cFos staining, it has been recently shown that only a few limbic cortical areas are activated during PS hypersomnia in rats and mice: the dentate gyrus (DG), claustrum, cortical amygdaloid nucleus, anterior cingulate cortex (ACA), medial entorhinal cortex (MEC) and retrosplenial cortex (RSC). Interestingly, the DG was the only cortical structure containing more Fos‐labelled neurons during PS hypersomnia than during W (Maciel et al, 2021; Renouard et al, 2015; Yamasaki et al, 2021). In line with these results, it has been shown that the RSC contains a large number of neurons specifically activated during PS and phase‐locked with theta (Koike et al, 2017).…”

Section: Cortical Activation During Psmentioning

confidence: 99%

Is paradoxical sleep setting up innate and acquired complex sensorimotor and adaptive behaviours?: A proposed function based on literature review

Casaglia

Luppi

2022

Journal of Sleep Research

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Summary We summarize here the progress in identifying the neuronal network as well as the function of paradoxical sleep and the gaps of knowledge that should be filled in priority. The core system generating paradoxical sleep localized in the brainstem is now well identified, and the next step is to clarify the role of the forebrain in particular that of the hypothalamus including the melanin‐concentrating hormone neurons and of the basolateral amygdala. We discuss these two options, and also the discovery that cortical activation during paradoxical sleep is restricted to a few limbic cortices activated by the lateral supramammillary nucleus and the claustrum. Such activation nicely supports the findings recently obtained showing that neuronal reactivation occurs during paradoxical sleep in these structures, and induces both memory consolidation of important memory and forgetting of less relevant ones. The question that still remains to be answered is whether paradoxical sleep is playing more crucial roles in processing emotional and procedural than other types of memories. One attractive hypothesis is that paradoxical sleep is responsible for erasing negative emotional memories, and that this function is not properly functioning in depressed patients. On the other hand, the presence of a muscle atonia during paradoxical sleep is in favour of a role in procedural memory as new types of motor behaviours can be tried without harm during the state. In a way, it also fits with the proposed role of paradoxical sleep in setting up the sensorimotor system during development.

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Is REM sleep a paradoxical state?: Different neurons are activated in the cingulate cortices and the claustrum during wakefulness and paradoxical sleep hypersomnia

Cited by 18 publications

References 21 publications

Paradoxical somatodendritic decoupling supports cortical plasticity during REM sleep

Paradoxical somatodendritic decoupling supports cortical plasticity during REM sleep

Altered intestinal microbiota are associated with sleep disturbances in patients with minimal hepatic encephalopathy caused by hepatitis B-related liver cirrhosis

Is paradoxical sleep setting up innate and acquired complex sensorimotor and adaptive behaviours?: A proposed function based on literature review

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