Neuronal Activity in the Cerebellum During the Sleep-Wakefulness Transition in Mice

Zhang, Libin; Zhang, Jie; Sun, Mengjia; Chen, Hao; Yan, Jie; Luo, Fenlan; Yao, Zhong-Xiang; Wu, Yamin; Hu, Bo

doi:10.1007/s12264-020-00511-9

Cited by 36 publications

(51 citation statements)

References 66 publications

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“…The presence of large amplitude, phasic events in the cerebellum of cats (Harlay et al, 1974;Pellet and Harley, 1977) and rats (Marks et al, 1980), mainly during REM sleep epochs, has also been attributed to the transmission of pontogeniculo-occipital waves (PGO waves; Farber et al, 1980;Velluti et al, 1985). Finally, recent studies have highlighted cerebellar roles in the generation of sleep spindles in monkeys (Xu et al, 2020) and sleep-wake transitions in mice (Zhang et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Delta Oscillations Coordinate Intracerebellar and Cerebello-Hippocampal Network Dynamics during Sleep

2022

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During sleep, the widespread coordination of neuronal oscillations across both cortical and subcortical brain regions is thought to support various physiological functions. However, how sleep-related activity within the brain's largest sensorimotor structure, the cerebellum, is multiplexed with well-described sleep-related mechanisms in regions such as the hippocampus remains unknown. We therefore simultaneously recorded from the dorsal hippocampus and three distinct regions of the cerebellum (Crus I, lobule VI, and lobules II/III) in male mice during natural sleep. Local field potential (LFP) oscillations were found to be coordinated between these structures in a sleep stage-specific manner. During non-REM sleep, prominent δ frequency coherence was observed between lobule VI and hippocampus, whereas non-REM-associated hippocampal sharp-wave ripple activity evoked discrete LFP modulation in all recorded cerebellar regions, with the shortest latency effects in lobule VI. We also describe discrete phasic sharp potentials (PSPs), which synchronize across cerebellar regions and trigger sharp-wave ripple suppression. During REM, cerebellar δ phase significantly modulated hippocampal theta frequency, and this effect was greatest when PSPs were abundant. PSPs were phase-locked to cerebellar δ oscillation peak and hippocampal theta oscillation trough, respectively. Within all three cerebellar regions, prominent LFP oscillations were observed at both low (δ, <4 Hz) and very high frequencies (∼250 Hz) during non-REM and REM sleep. Intracerebellar cross-frequency analysis revealed that δ oscillations modulate those in the very high-frequency range. Together, these results reveal multiple candidate physiological mechanisms to support “offline,” bidirectional interaction within distributed cerebello-hippocampal networks.SIGNIFICANCE STATEMENTSleep is associated with widespread coordination of activity across a range of brain regions. However, little is known about how activity within the largest sensorimotor region of the brain, the cerebellum, is both intrinsically organized and links with higher-order structures, such as the hippocampus, during sleep. By making multisite local field potential recordings in naturally sleeping mice, we reveal and characterize multiple sleep stage-specific physiological mechanisms linking three distinct cerebellar regions with the hippocampus. Central to these physiological mechanisms is a prominent δ (<4 Hz) oscillation, which temporally coordinates both intracerebellar and cerebello-hippocampal network dynamics. Understanding this distributed network activity is important for gaining insight into cerebellar contributions to sleep-dependent processes, such as memory consolidation.

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Section: Introductionmentioning

confidence: 99%

Delta Oscillations Coordinate Intracerebellar and Cerebello-Hippocampal Network Dynamics during Sleep

2022

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“…A previous study on cerebelloctomized cats reported a small decrease in wakefulness and NREM sleep, and an increase in REM sleep, which revealed that the cerebellum may participate in fine-tuning and regulation of the sleep-wake cycle (Cunchillos and De Andrés, 1982). At present, the available evidence on the role of the sleep-wake cycle in cerebellar processing is mainly from animal studies (Barik and de Beaurepaire, 2005;Zhang et al, 2020), and to date the clinical management of the sleep-wake cycle is also challenging. This highlights an important area clinically, which can be further explored through future studies.…”

Section: Introductionmentioning

confidence: 99%

A Narrative Review of Cerebellar Malfunctions and Sleep Disturbances

Song

Zhu

2021

Front. Neurosci.

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Cerebellar malfunctions significantly impact the regulation of the sleep–wakefulness transition. The possible mechanism for this effect is still unknown. Evidence on the role of cerebellar processing in the sleep–wake cycle is derived mainly from animal studies, and clinical management of the sleep–wake cycle is also challenging. The purpose of this review is to investigate the role of cerebellar activity during normal sleep and the association between cerebellar dysfunction and sleep disorders. Large-scale, multicenter trials are still needed to confirm these findings and provide early identification and intervention strategies to improve cerebellar function and the sleep quality of patients.

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“…Additionally, the ventral thalamus, an important component of the ascending arousal system, was proven to receive afferents from several cerebellar nuclei (Gornati et al, 2018;Houck & Person, 2015). Studies using mice reported an increased firing rate of Purkinje cells in the cerebellum before the transition from sleep to wakefulness (Zhang et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Functional connectivity of the human hypothalamus during wakefulness and nonrapid eye movement sleep

Jiang

Zou

Liu

et al. 2021

Human Brain Mapping

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Animal experiments indicate that the hypothalamus plays an essential role in regulating the sleep-wake cycle. A recent neuroimaging study conducted under resting wakefulness conditions suggested the presence of a wake-promoting region and a sleep-promoting region in the human posterior hypothalamus and anterior hypothalamus, respectively, and interpreted their anticorrelated organization in resting-state functional networks as evidence for their opposing roles in sleep-wake regulation.However, whether and how the functional networks of the two hypothalamic regions reorganize according to their wake-or sleep-promoting roles during sleep are unclear. Here, we constructed functional networks of the posterior and anterior hypothalamus during wakefulness and nonrapid eye movement (NREM) sleep using simultaneous electroencephalography and functional magnetic resonance imaging data collected from 62 healthy participants. The functional networks of the posterior and anterior hypothalamus exhibited inversely correlated organizations during both wakefulness and NREM sleep. The connectivity strength of the posterior hypothalamic functional network was stronger during wakefulness than during stable sleep.From wakefulness to sleep, the anterior cingulate gyrus, paracingulate gyrus, insular cortex, and fontal operculum cortex showed decreased positive connectivity, while the precentral gyrus and postcentral gyrus showed decreased negative connectivity with the posterior hypothalamus. Additionally, the insular cortex and frontal operculum cortex showed negative connectivity during wakefulness and positive connectivity during sleep with the anterior hypothalamus, exhibiting an increasing trend. These findings provide insights into the correspondence between the functional network organizations and hypothalamic sleep-wake regulation in humans.

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Neuronal Activity in the Cerebellum During the Sleep-Wakefulness Transition in Mice

Cited by 36 publications

References 66 publications

Delta Oscillations Coordinate Intracerebellar and Cerebello-Hippocampal Network Dynamics during Sleep

Delta Oscillations Coordinate Intracerebellar and Cerebello-Hippocampal Network Dynamics during Sleep

A Narrative Review of Cerebellar Malfunctions and Sleep Disturbances

Functional connectivity of the human hypothalamus during wakefulness and nonrapid eye movement sleep

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