Selective slow‐wave sleep deprivation and time‐of‐night effects on cognitive performance upon awakening

Ferrara, Michele; Gennaro, Luigi De; Casagrande, Maria; Bertini, Mario

doi:10.1111/1469-8986.3740440

Cited by 61 publications

(21 citation statements)

References 11 publications

(17 reference statements)

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“…Previous studies of experimental SWS suppression have focused on subjective sleepiness and measures of cognitive performance and have suggested that SWS may be important for waking neurobehavioral function (1,16). In the present study, we were able to induce a selective and profound reduction in SWS and to observe a clear adverse impact on daytime glucose tolerance with a clear increase in a well validated marker of diabetes risk.…”

Section: Discussionsupporting

confidence: 50%

Slow-wave sleep and the risk of type 2 diabetes in humans

Tasali

Leproult²,

Ehrmann³

et al. 2008

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

808

617

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There is convincing evidence that, in humans, discrete sleep stages are important for daytime brain function, but whether any particular sleep stage has functional significance for the rest of the body is not known. Deep non-rapid eye movement (NREM) sleep, also known as slow-wave sleep (SWS), is thought to be the most ''restorative'' sleep stage, but beneficial effects of SWS for physical well being have not been demonstrated. The initiation of SWS coincides with hormonal changes that affect glucose regulation, suggesting that SWS may be important for normal glucose tolerance. If this were so, selective suppression of SWS should adversely affect glucose homeostasis and increase the risk of type 2 diabetes. Here we show that, in young healthy adults, all-night selective suppression of SWS, without any change in total sleep time, results in marked decreases in insulin sensitivity without adequate compensatory increase in insulin release, leading to reduced glucose tolerance and increased diabetes risk. SWS suppression reduced delta spectral power, the dominant EEG frequency range in SWS, and left other EEG frequency bands unchanged. Importantly, the magnitude of the decrease in insulin sensitivity was strongly correlated with the magnitude of the reduction in SWS. These findings demonstrate a clear role for SWS in the maintenance of normal glucose homeostasis. Furthermore, our data suggest that reduced sleep quality with low levels of SWS, as occurs in aging and in many obese individuals, may contribute to increase the risk of type 2 diabetes.aging ͉ sleep quality ͉ sleep disordered breathing ͉ delta waves ͉ insulin resistance H uman sleep is composed of rapid-eye-movement (REM) sleep and stages 1, 2, 3, and 4 of non-REM (NREM) sleep. The deeper stages of NREM sleep, i.e., stages 3 and 4, also known as slow-wave sleep (SWS), are thought to be the most ''restorative.'' There is indeed evidence that SWS plays a role in waking neurobehavioral function (1), particularly in memory consolidation (2, 3), but whether SWS is also important for peripheral physiological function is not known. The initiation of SWS is temporally associated with transient metabolic, hormonal, and neurophysiologic changes, all of which could potentially affect glucose homeostasis. These include decreased brain glucose utilization, stimulation of growth hormone release, inhibition of corticotropic activity, decreased sympathetic nervous activity, and increased vagal tone. We therefore hypothesized that SWS plays a role in glucose regulation and that suppression of SWS may adversely affect glucose homeostasis.To test this hypothesis, we developed an experimental model in young healthy lean individuals that was designed to selectively suppress SWS and assessed the impact of this intervention on glucose homeostasis. The EEG was continuously monitored, and SWS was suppressed by delivering acoustic stimuli of varying frequencies and intensities. The intervention was designed to substitute deep NREM sleep, i.e., stages 3 and 4, with shallow NREM slee...

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Section: Discussionsupporting

confidence: 50%

Slow-wave sleep and the risk of type 2 diabetes in humans

Tasali

Leproult²,

Ehrmann³

et al. 2008

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

808

617

View full text Add to dashboard Cite

show abstract

“…Previous research has demonstrated a relationship between poor sleep quality and impaired performance, [6][7][8][37][38][39] yet here, caffeine resulted in higher accuracy scores on the n-back task relative to placebo. The most likely explanation for this unexpected finding is that residual caffeine may have directly ameliorated some of the effects of poor sleep.…”

Section: Discussionmentioning

confidence: 54%

Naturalistic Effects of Five Days of Bedtime Caffeine Use on Sleep, Next-Day Cognitive Performance, and Mood

Keenan

Tiplady

Priestley

et al. 2014

Journal of Caffeine Research

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Background: Disruptive effects of caffeine on sleep have previously been reported, although measures of next-day mood and performance have rarely been included. The present study aims to evaluate the effects of caffeine on sleep and associated next-day effects in a naturalistic field setting. Methods: Nineteen participants (daily caffeine intake 0-141 mg), assessed as good sleepers, took part in a randomized, placebo-controlled, double-blind, 2-week crossover study to assess the effects of bedtime caffeine use (250 mg) on sleep and next-day cognitive performance and mood, which were assessed on a mobile phone in the morning and afternoon. Sleep was assessed objectively (actiwatch) and subjectively (sleep diary). Results: Caffeine's effects on sleep were largely restricted to the first day of administration, with actigraphically measured reduced sleep efficiency, increased activity score and fragmentation index, decreased self-rated sleep quality, and an increased occurrence of participants waking early; only decreased sleep efficiency remained over the week. Effects on next-day performance and mood were evident over the whole week, although despite disrupting sleep, accuracy on a working memory task was higher after caffeine than placebo administration. Conclusions: Caffeine disrupted sleep, although when assessing next-day performance, which may have been affected by the presence of residual caffeine, performance appeared better after caffeine compared to placebo, although this was most likely due to prevention of the effects of overnight withdrawal from caffeine rather than representing a net benefit. Furthermore, partial tolerance developed to the effects of caffeine on sleep.

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“…On the other hand, Ryman et al (1985) reported that 3 h of sleep after only 17 h of continuous work did not improve performance. Other studies have concluded that 1-2 full nights of sleep are needed to recover cognitively from sleep loss due to sleep fragmentation or partial sleep deprivation (Bonnet and Arand, 1998;Ferrara et al, 2000;Dinges et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

Frontal Lobe Metabolic Decreases with Sleep Deprivation not Totally Reversed by Recovery Sleep

Gillin

Buchsbaum

et al. 2006

Neuropsychopharmacol

141

100

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We studied the effects of total sleep deprivation and recovery sleep in normal subjects using position emission tomography with 18F-deoxyglycose. Sleep deprivation resulted in a significant decrease in relative metabolism of the frontal cortex, thalamus, and striatum. Recovery sleep was found to have only a partial restorative effect on frontal lobe function with minimal reversal of subcortical deficits. Sleep may be especially important for maintenance of frontal lobe activity.

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Selective slow‐wave sleep deprivation and time‐of‐night effects on cognitive performance upon awakening

Cited by 61 publications

References 11 publications

Slow-wave sleep and the risk of type 2 diabetes in humans

Slow-wave sleep and the risk of type 2 diabetes in humans

Naturalistic Effects of Five Days of Bedtime Caffeine Use on Sleep, Next-Day Cognitive Performance, and Mood

Frontal Lobe Metabolic Decreases with Sleep Deprivation not Totally Reversed by Recovery Sleep

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