The microstructure of REM sleep: Why phasic and tonic?

Simor, Péter; Wijk, Gwen van der; Nobili, Lino; Peigneux, Philippe

doi:10.1016/j.smrv.2020.101305

Cited by 130 publications

(108 citation statements)

References 136 publications

(178 reference statements)

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“…Our observation of different REM sleep microstates associated with various levels of cortical activation echoes previous reports about REM sleep heterogeneity, usually presented as a dichotomy between phasic and tonic REM sleep (Simor et al, 2020). The lower arousal thresholds and the higher g activity in phasic versus tonic REM sleep have led to the concept that phasic REM sleep represents a more "internally focused" but cognitively active state, which could explain the occurrence of dreams (Gross and Gotman, 1999;Wehrle et al, 2007;Ermis et al, 2010;Simor et al, 2016).…”

Section: Phasic Versus Tonic Rem Sleepsupporting

confidence: 87%

Rapid Eye Movement Sleep Sawtooth Waves Are Associated with Widespread Cortical Activations

et al. 2020

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Sawtooth waves (STW) are bursts of frontocentral slow oscillations recorded in the scalp electroencephalogram (EEG) during rapid eye movement (REM) sleep. Little is known about their cortical generators and functional significance. Stereo-EEG performed for presurgical epilepsy evaluation offers the unique possibility to study neurophysiology in situ in the human brain. We investigated intracranial correlates of scalp-detected STW in 26 patients (14 women) undergoing combined stereo-EEG/ polysomnography. We visually marked STW segments in scalp EEG and selected stereo-EEG channels exhibiting normal activity for intracranial analyses. Channels were grouped in 30 brain regions. The spectral power in each channel and frequency band was computed during STW and non-STW control segments. Ripples (80-250 Hz) were automatically detected during STW and control segments. The spectral power in the different frequency bands and the ripple rates were then compared between STW and control segments in each brain region. An increase in 2-4 Hz power during STW segments was found in all brain regions, except the occipital lobe, with large effect sizes in the parietotemporal junction, the lateral and orbital frontal cortex, the anterior insula, and mesiotemporal structures. A widespread increase in high-frequency activity, including ripples, was observed concomitantly, involving the sensorimotor cortex, associative areas, and limbic structures. This distribution showed a high spatiotemporal heterogeneity. Our results suggest that STW are associated with widely distributed, but locally regulated REM sleep slow oscillations. By driving fast activities, STW may orchestrate synchronized reactivations of multifocal activities, allowing tagging of complex representations necessary for REM sleep-dependent memory consolidation.

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Section: Phasic Versus Tonic Rem Sleepsupporting

confidence: 87%

Rapid Eye Movement Sleep Sawtooth Waves Are Associated with Widespread Cortical Activations

et al. 2020

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“…In human, phasic REM sleep showed higher threshold for awakening than tonic REM sleep, and event related potentials elicited by external stimuli was reduced in phasic REM sleep (Brankačk et al, 2012), but partially reinstated during tonic REM sleep, suggesting tonic REM sleep may be more vulnerable for detecting potential danger cues. In spontaneous oscillation activity, tonic REM sleep showed higher activity in theta, beta, and alpha band, and lower activity in delta and gamma band compared to phasic REM (Simor et al, 2020). In our research, we found that tonic REM showed decreased oscillation power at 0.50 Hz and increased oscillation power at 1.50-7.25 Hz and 9.50-12.00 Hz than phasic REM.…”

Section: Discussionsupporting

confidence: 46%

“…Phasic REM sleep showed higher threshold for awakening than tonic REM sleep (Brankačk et al, 2012). In spontaneous oscillation activity, tonic REM sleep showed elevated high alpha and beta band, while phasic REM sleep showed the predominance of slow delta, theta, and higher gamma band (Ermis et al, 2010;Simor et al, 2020). Mice are the most common animal model for studying the mechanism of sleep and sleep associated cortical dynamics (Liu et al, 2016;McKillop et al, 2018;Kam et al, 2019), but there is still lack of methods to measure eye movements in mice during sleep.…”

Section: Introductionmentioning

confidence: 99%

Tracking Eye Movements During Sleep in Mice

et al. 2021

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Eye movement is not only for adjusting the visual field and maintaining the stability of visual information on the retina, but also provides an external manifestation of the cognitive status of the brain. Recent studies showed similarity in eye movement patterns between wakefulness and rapid eye movement (REM) sleep, indicating that the brain status of REM sleep likely resembles that of awake status. REM sleep in humans could be divided into phasic REM and tonic REM sleep according to the difference in eye movement frequencies. Mice are the most commonly used animal model for studying neuronal and molecular mechanisms underlying sleep. However, there was a lack of details for eye movement patterns during REM sleep, hence it remains unknown whether REM sleep can be further divided into different stages in mice. Here we developed a device combining electroencephalogram (EEG), electromyogram (EMG) as well as eye movements recording in mice to study the eye movement patterns during sleep. We implanted a magnet beneath the conjunctiva of eye and tracked eye movements using a magnetic sensor. The magnetic signals showed strong correlation with video-oculography in head-fixed mice, indicating that the magnetic signals reflect the direction and magnitude of eye movement. We also found that the magnet implanted beneath the conjunctiva exhibited good biocompatibility. Finally, we examined eye movement in sleep–wake cycle, and discriminated tonic REM and phasic REM according to the frequency of eye movements, finding that compared to tonic REM, phasic REM exhibited higher oscillation power at 0.50 Hz, and lower oscillation power at 1.50–7.25 Hz and 9.50–12.00 Hz. Our device allowed to simultaneously record EEG, EMG, and eye movements during sleep and wakefulness, providing a convenient and high temporal-spatial resolution tool for studying eye movements in sleep and other researches in mice.

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“…More generally, our findings demonstrate the importance of not relying solely on sleep stage correlations when probing sleep and memory associations (Lim et al, 2020;Muehlroth & Werkle-Bergner, 2020;Simor et al, 2020). By simply assessing time spent in SWS, no consideration is given to specific neurophysiological events.…”

Section: Discussionmentioning

confidence: 70%

Slow oscillation‐spindle coupling is negatively associated with emotional memory formation following stress

Denis

Kim

Kark

et al. 2021

Eur J of Neuroscience

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Both stress and sleep enhance emotional memory. They also interact, with the largest effect of sleep on emotional memory being seen when stress occurs shortly before or after encoding. Slow wave sleep (SWS) is critical for long-term episodic memory, facilitated by the temporal coupling of slow oscillations and sleep spindles. Prior work in humans has shown these associations for neutral information in non-stressed participants. Whether coupling interacts with stress to facilitate emotional memory formation is unknown. Here, we addressed this question by reanalyzing an existing dataset of 64 individuals. Participants underwent a psychosocial stressor (32) or comparable control (32) prior to the encoding of 150-line drawings of neutral, positive, and negative images. All participants slept overnight with polysomnography, before being given a surprise memory test the following day. In the stress group, time spent in SWS was positively correlated with memory for images of all valences. Results were driven by those who showed a high cortisol response to the stressor, compared to low responders. The amount of slow oscillation-spindle coupling during SWS was negatively associated with neutral and emotional memory in the stress group only. The association with emotional memory was significantly stronger than for neutral memory within the stress group. These results suggest that stress around the time of initial memory formation impacts the relationship between slow wave sleep and memory..

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The microstructure of REM sleep: Why phasic and tonic?

Cited by 130 publications

References 136 publications

Rapid Eye Movement Sleep Sawtooth Waves Are Associated with Widespread Cortical Activations

Rapid Eye Movement Sleep Sawtooth Waves Are Associated with Widespread Cortical Activations

Tracking Eye Movements During Sleep in Mice

Slow oscillation‐spindle coupling is negatively associated with emotional memory formation following stress

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