Local aspects of sleep and wakefulness

doi:10.1016/j.conb.2017.05.008

Current Opinion in Neurobiology

Volume 44, June 2017, Pages 222-227

https://doi.org/10.1016/j.conb.2017.05.008 Get rights and content

Highlights

•
Slow waves of NREM sleep can occur locally and asynchronously across brain regions.
•
Their regional distribution and amplitude is in part mediated by experience-dependent changes in synaptic strength.
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Local low-frequency oscillations (<10 Hz) can occur also in REM sleep and during wakefulness.
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Local low-frequency oscillations during wake lead to region-specific cognitive errors.
•
Local changes in SWA in posterior brain regions account for changes in consciousness during sleep.

Slow waves, the hallmark of NREM (Non Rapid Eye Movement) sleep, are not uniformly distributed across the cortical surface, but can occur locally and asynchronously across brain regions. Their regional distribution and amplitude is affected by brain maturation and by time spent awake, mediated in part by experience-dependent changes in synaptic strength. Recent studies have shown that local low-frequency oscillations (<10 Hz) can also occur in REM sleep and during wakefulness, leading to region-specific cognitive errors. Local decreases and increases of slow wave activity in posterior brain regions have been linked to the occurrence of dreaming and to unconscious sleep, respectively. Finally, the coexistence of local sleep-like and wake-like patterns in different brain areas is characteristic of several sleep disorders and may offer insights into these conditions.

Section snippets

The EEG of slow wave sleep

For the purpose of this review, we will mostly focus on slow waves as the principal marker of Non-Rapid Eye Movement (NREM) sleep. Slow waves occur when neurons become bistable and undergo a slow oscillation in membrane potential between two states (<1 Hz): a depolarized ‘up-state’ during which neurons fire (‘on-period’), corresponding to the transition between the negative and the positive deflection of the EEG wave, and a hyperpolarized ‘down-state’ characterized by neuronal silence

Local aspects of sleep

Perhaps the most remarkable example of ‘local’ sleep is observed in some species of dolphins, like bottlenose dolphins, in which slow wave sleep can occur in only one hemisphere during swimming, while the other hemisphere displays low-voltage fast ‘desynchronized’ EEG activity typical of wakefulness [5]. Similar unihemispheric sleep patterns have been observed in several species of whales, manatees, some seals as well as several birds [6, 7]. Although unihemispheric sleep does not occur in

Local sleep and plasticity

Local aspects of sleep can also be affected by prior experience and learning. In an early study, Huber et al. [16] showed that a motor learning task involving the right parietal region produced a local increase in SWA in this area during subsequent NREM sleep, compared to when the same task was performed without a learning component. Moreover, the local increase in SWA was correlated with task performance the next day and showed a homeostatic decline in the course of the first 90 min of sleep.

Local sleep in wakefulness

When individuals remain awake for extended periods of time, they become sleepy and show behavioral changes and cognitive impairment. Under conditions of sleep deprivation, the waking EEG typically shows increased low-frequency power in the theta range (5–7 Hz) reflecting the duration of prior wakefulness [27, 28, 29]. A recent study using local field potentials and multi-unit recordings has shown that when rats are kept awake beyond the usual duration, cortical neurons tend to fall silent for

Local sleep in state transitions

State transitions, in which sleep and wakefulness replace each other, provide an excellent opportunity to observe local sleep. Indeed, several recent studies have shown that the transition to sleep is not a spatially and temporally uniform process, but shows regionally specific features. In addition, recent work using refined techniques of signal analysis has started to shed light on how local sleep patterns relate to cognitive activities during state transitions. In the falling asleep period,

Local sleep and consciousness

How does regionally heterogeneous SWA affect conscious experiences during sleep? It is now well established that dreaming can occur not only in REM sleep, but also in NREM sleep. Particularly at the end of the night, when SWA is reduced, dream reports from NREM and REM sleep become virtually indistinguishable, suggesting that slow waves may interfere with consciousness [42]. Several lines of evidence suggest that this is indeed so. Earlier studies using transcranial magnetic stimulation (TMS)

Local sleep and sleep disorders

The study of the mechanisms underlying local sleep patterns has direct implications for clinical conditions. Indeed, several sleep disorders are characterized by a so-called ‘state dissociation’, in which behavioral features of more than one state coexist [51]. Sleepwalking and other disorders of arousal, for instance, result from incomplete awakenings during slow wave sleep, and are characterized by impaired cognition, different degrees of retrograde amnesia and variable motor activity.

Conclusion

It is now well established that sleep occurs and is regulated locally. Recent studies have shown that local aspects of sleep, such as low-frequency oscillations typical of NREM sleep, can also occur during extended periods of wakefulness and even during REM sleep. The occurrence of such local low-frequency oscillations is in part modulated by prior experience and learning, and may account for cognitive impairment and regionally specific performance errors during sleep deprivation in both humans

Funding

This work was supported by the Swiss National Science Foundation Grants139778 (FS), 145571 (FS), the Swiss Foundation for Medical Biological Grants151743 and 145763 (FS), the Divesa foundation Switzerland (FS), the Pierre-Mercier foundation for Science (FS), the bourse pro-femmes of the CHUV and University of Lausanne, Switzerland (FS), NIH/NIMH grant R01MH099231 (GT), NIH/NINDS grant P01NS083514 (GT), and NIH/NCCAMP01AT004952 (GT).

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

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View full text

Local aspects of sleep and wakefulness

Highlights

Section snippets

The EEG of slow wave sleep

Local aspects of sleep

Local sleep and plasticity

Local sleep in wakefulness

Local sleep in state transitions

Local sleep and consciousness

Local sleep and sleep disorders

Conclusion

Funding

References and recommended reading

J. Neurophysiol.

Nat. Sci. Sleep

Eur. J. Neurosci.

Curr. Top. Med. Chem.

Curr. Biol.

Nature

Neuroscientist

Proc. Natl. Acad. Sci. U. S. A.

Nature

Science

Proc. Natl. Acad. Sci. U. S. A.

Neuroscience

Cogn. Neurosci.

Sci. Rep.

Biol. Psychol.

Neurology

Sleep

The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications

From waking to sleeping: neuronal and chemical substrates

Trends Pharmacol. Sci.

Mathematical models of sleep regulation

Front. Biosci.

Interhemispheric asymmetry of the electroencephalographic sleep patterns in dolphins

Brain Res.

Local sleep homeostasis in the avian brain: convergence of sleep function in mammals and birds?

Proc. Biol. Sci.

Night watch in one brain hemisphere during sleep associated with the first-night effect in humans

Curr. Biol.

Fronto-occipital EEG power gradients in human sleep

J. Sleep Res.

Regional slow waves and spindles in human sleep

Neuron

Dissociated wake-like and sleep-like electro-cortical activity during sleep

Neuroimage

Activation of the motor cortex during phasic rapid eye movement sleep

Ann. Neurol.

Effects of skilled training on sleep slow wave activity and cortical gene expression in the rat

Sleep