A role for the cortex in sleep-wake regulation

Krone, Lukas B.; Yamagata, Tomoko; Blanco‐Duque, Cristina; Guillaumin, Mathilde C. C.; Kahn, Martin; Akerman, Colin J.; Hoerder‐Suabedissen, Anna; Molnár, Zoltán; Vyazovskiy, Vladyslav V.

doi:10.1101/2020.03.17.996090

Cited by 5 publications

(4 citation statements)

References 42 publications

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“…Second, it remains to be addressed why wake experience had effects on some characteristics of sleep, such as SWA or sleep latency, and not others, such as sleep fragmentation. While it can be expected that SWA or sleep latency is directly proportional to preceding spontaneous wake duration or sleep deprivation [ 11 , 46 – 48 ], this is not always the case. We have shown earlier that the levels of SWA during NREM sleep do not increase linearly with the increase in wake time, but saturate after a few hours [ 6 ].…”

Section: Discussionmentioning

confidence: 99%

Waking experience modulates sleep need in mice

et al. 2021

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Background Homeostatic regulation of sleep is reflected in the maintenance of a daily balance between sleep and wakefulness. Although numerous internal and external factors can influence sleep, it is unclear whether and to what extent the process that keeps track of time spent awake is determined by the content of the waking experience. We hypothesised that alterations in environmental conditions may elicit different types of wakefulness, which will in turn influence both the capacity to sustain continuous wakefulness as well as the rates of accumulating sleep pressure. To address this, we compared the effects of repetitive behaviours such as voluntary wheel running or performing a simple touchscreen task, with wakefulness dominated by novel object exploration, on sleep timing and EEG slow-wave activity (SWA) during subsequent NREM sleep. Results We find that voluntary wheel running is associated with higher wake EEG theta-frequency activity and results in longer wake episodes, as compared with exploratory behaviour; yet, it does not lead to higher levels of EEG SWA during subsequent NREM sleep in either the frontal or occipital derivation. Furthermore, engagement in a touchscreen task, motivated by food reward, results in lower SWA during subsequent NREM sleep in both derivations, as compared to exploratory wakefulness, even though the total duration of wakefulness is similar. Conclusion Overall, our study suggests that sleep-wake behaviour is highly flexible within an individual and that the homeostatic processes that keep track of time spent awake are sensitive to the nature of the waking experience. We therefore conclude that sleep dynamics are determined, to a large degree, by the interaction between the organism and the environment.

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Section: Discussionmentioning

confidence: 99%

Waking experience modulates sleep need in mice

et al. 2021

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“…This could be regulated by layer V pyramidal neurons. Genetically silencing these neurons blocks the increase in EEG delta power following SD without changing the amount of sleep 79 . By contrast, the SOM/GABA component could be needed for sleep itself.…”

Section: Discussionmentioning

confidence: 99%

Sleep deprivation triggers somatostatin neurons in prefrontal cortex to initiate nesting and sleep via the preoptic and lateral hypothalamus

Tossell

Soto

et al. 2020

Preprint

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AbstractAnimals undertake specific behaviors before sleep. Little is known about whether these innate behaviors, such as nest building, are actually an intrinsic part of the sleep-inducing circuitry. We found, using activity-tagging genetics, that mouse prefrontal cortex (PFC) somatostatin/GABAergic (SOM/GABA) neurons, which become activated during sleep deprivation, induce nest building when opto-activated. These tagged neurons induce sustained global NREM sleep if their activation is prolonged metabotropically. Sleep-deprivation-tagged PFC SOM/GABA neurons have long-range projections to the lateral preoptic (LPO) and lateral hypothalamus (LH). Local activation of tagged PFC SOM/GABA terminals in LPO and the LH induced nesting and NREM sleep respectively. Our findings provide a circuit link for how the PFC responds to sleep deprivation by coordinating sleep preparatory behavior and subsequent sleep.

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“…The cortex—where mammalian sleep is most often measured—is a brain region where neural mechanisms underlying sleep duration and sleep depth coincide: many neuromodulatory nuclei associated with sleep/wake transitions send direct projections to the cortex ( Björklund and Lindvall, 1978 ; Woolf, 1991 ; Loughlin et al, 1986 ; Panula et al, 1989 ), and the cortex plays an instrumental role in generating and propagating SWA during sleep ( Volgushev et al, 2006 ; Sanchez-Vives and McCormick, 2000 ; Niethard et al, 2018 ; Stroh et al, 2013 ; Luczak et al, 2007 ; Massimini et al, 2004 ; Krone, 2020 ; Sanchez-Vives and Mattia, 2014 ; Lemieux et al, 2014 ). Further, cortical SWA intensity can be locally regulated, leading to heterogeneity of SWA across cortex ( Huber et al, 2004 ; Funk et al, 2016 ; Siclari and Tononi, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Cortical astrocytes independently regulate sleep depth and duration via separate GPCR pathways

Vaidyanathan

Collard

Yokoyama

et al. 2021

eLife

100

106

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Non-rapid eye movement (NREM) sleep, characterized by slow-wave electrophysiological activity, underlies several critical functions, including learning and memory. However, NREM sleep is heterogeneous, varying in duration, depth, and spatially across the cortex. While these NREM sleep features are thought to be largely independently regulated, there is also evidence that they are mechanistically coupled. To investigate how cortical NREM sleep features are controlled, we examined the astrocytic network, comprising a cortex-wide syncytium that influences population-level neuronal activity. We quantified endogenous astrocyte activity in mice over natural sleep and wake, then manipulated specific astrocytic G-protein-coupled receptor (GPCR) signaling pathways in vivo. We find that astrocytic Gi- and Gq-coupled GPCR signaling separately control NREM sleep depth and duration, respectively, and that astrocytic signaling causes differential changes in local and remote cortex. These data support a model in which the cortical astrocyte network serves as a hub for regulating distinct NREM sleep features.

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A role for the cortex in sleep-wake regulation

Cited by 5 publications

References 42 publications

Waking experience modulates sleep need in mice

Waking experience modulates sleep need in mice

Sleep deprivation triggers somatostatin neurons in prefrontal cortex to initiate nesting and sleep via the preoptic and lateral hypothalamus

Cortical astrocytes independently regulate sleep depth and duration via separate GPCR pathways

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