Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep

Vyazovskiy, Vladyslav V.; Cirelli, Chiara; Pfister-Genskow, Martha; Faraguna, Ugo; Tononi, Giulio

doi:10.1038/nn2035

Cited by 718 publications

(821 citation statements)

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“…EEG power density (0.1-4 Hz) was monitored as an indicator of sleep need [Borbely and Achermann, 1999]. Figure 5A shows the gradual decrease in SWA during RS relative to SD, consistent with results in both rats and humans [Tobler and Borbely, 1986, 1990;Franken et al, 1991;Borbely and Achermann, 1999;Cirelli et al, 2004;Vyazovskiy et al, 2007Vyazovskiy et al, , 2008. GAPDH levels began to increase within 2 h RS relative to SD ( y P < 0.05, Fig.…”

Section: Sd Differentially Affects Gapdh and Actin Expressionsupporting

confidence: 82%

Rapid alterations in cortical protein profiles underlie spontaneous sleep and wake bouts

Vázquez

Hall

Witkowska

et al. 2008

J of Cellular Biochemistry

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Existing data indicate that sleep-wakefulness is an essential behavior. The biological function(s) of sleep, however, remains unknown, due, in part, to the lack of information available at the intracellular level. Preliminary microarray analyses show that changes in behavioral state influence regional mRNA profiles; however, the impact of sleep on protein signatures is virtually unexplored. In these studies, cortical protein profiles were examined after timed bouts of spontaneous sleep-wakefulness. Within minutes of each behavioral state examined, a small number of spots showing unique expression were detected. Mass spectroscopy analyses of sleep-and wake-related spots identified proteins associated with multiple functional categories. Two sleep-associated proteins were further validated using a sleep deprivation paradigm. We found preliminary evidence for two different post-transcriptional mechanisms-one (GAPDH) in which the amount of protein was increased in the recovery sleep following prolonged waking, while the other (actin) suggested that post-translational modifications may underlie sleep. The similarities between the effects of sleep on both protein and mRNA profiles indicate that dynamic intracellular changes underlie sleep-wake states and are consistent with roles for sleep in multiple biological functions. J. Cell. Biochem. 105: 1472Biochem. 105: -1484Biochem. 105: , 2008. ß 2008 Wiley-Liss, Inc. KEY WORDS: TWO-DIMENSIONAL ELECTROPHORESIS (2DE); MASS SPECTROMETRY; SPONTANEOUS SLEEP-WAKE BOUTS; SLEEP-ASSOCIATED PROTEIN EXPRESSIONS leep-wake behavior is a complex and tightly regulated Achermann, 1999, 2000] amalgam of physiological processes that involves reciprocal interactions between numerous brain regions that is coordinated by multiple neurotransmitter/peptide systems [Lin, 2000;Jones, 2004]. Sleep is exhibited by all animals studied thus far [Campbell and Tobler, 1984;Tobler, 2000] and constitutes a significant percentage of a 24 h period [Carskadon and Dement, 2000;Ohayon et al., 2004]. Alternations between sleep and wakefulness are regulated by a combination of circadian (sleep timing) [Edgar, 1995] and homeostatic factors (sleep need) [Borbely, 1982]. The homeostatic regulation of sleep is based on the observation that following sleep deprivation (SD), there is an increase in sleep time and intensity that is proportional to the sleep lost, suggesting that a need for sleep accumulates during waking in both rodents and humans [Tobler and Borbely, 1986;Riedner et al., 2007;Vyazovskiy et al., 2007]. In humans, SD results in marked cognitive and physiological impairments [Drummond and Brown, 2001;Durmer and Dinges, 2005], while prolonged SD in rats [Rechtschaffen, 1998] and flies [Shaw et al., 2002] is fatal. The biological function(s) of sleep, however, remains poorly characterized, though most agree that sleep serves a restorative function [Benington and Heller, 1995]. Proposed roles for sleep include the maintenance of body temperature [McGinty and Szymusiak, 1990;Wehr, 1992], energy ...

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Section: Sd Differentially Affects Gapdh and Actin Expressionsupporting

confidence: 82%

Rapid alterations in cortical protein profiles underlie spontaneous sleep and wake bouts

Vázquez

Hall

Witkowska

et al. 2008

J of Cellular Biochemistry

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“…To conclude, our data clearly reveal some interactions between synaptic activity and circadian oscillators and implicate oligophrenin-1 in its regulation, delineating a new means of communication between synapse and nucleus 24,36,40 . These findings are further indication 36,41 that cognitive ability is influenced by circadian rhythms, and promise to provide insight into normal plasticity and the etiology of intellectual disability.…”

Section: Discussionmentioning

confidence: 55%

A circadian clock in hippocampus is regulated by interaction between oligophrenin-1 and Rev-erbα

et al. 2011

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“…Molecular and electrophysiological markers of synaptic potentiation increase after waking in rat cortex and hippocampus, while markers of synaptic depression do so after sleep. 5,6 Moreover, in rats and humans, procedures presumably leading to synaptic potentiation or depression result in SWA increases and decreases, respectively. [7][8][9][10][11][12] More specifically, a study in humans using highdensity EEG found that performing a visuomotor learning task produced a local increase in SWA during subsequent sleep.…”

Section: Sleep Is Present and Homeostatically Regu-lated In All Animamentioning

confidence: 99%

Effects of Skilled Training on Sleep Slow Wave Activity and Cortical Gene Expression in the Rat

Hanlon

Faraguna

Vyazovskiy

et al. 2009

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SO FAR. IN MAMMALS, THE BEST CHARACTERIZED marker of sleep homeostasis is slow wave activity (SWA), the power density in the electroencephalogram (EEG) between 0.5 and 4 Hz during NREM sleep. SWA is high at sleep onset and declines during sleep, suggesting that it may reflect the accumulation of sleep pressure as a function of duration and/or intensity of prior waking. 1,2 Why and how SWA should reflect sleep homeostasis, however, is still unclear.We hypothesized that SWA is high at sleep onset because it reflects the occurrence, during waking, of widespread synaptic potentiation in cortical and subcortical areas. 3,4 This increase would be detrimental in the long term, because stronger synapses need more energy, space, and cellular supplies, and may lead to saturation of the ability to learn. Sleep would thus be crucial to renormalize synaptic strength to an energetically sustainable level. Molecular and electrophysiological markers of synaptic potentiation increase after waking in rat cortex and hippocampus, while markers of synaptic depression do so after sleep. 5,6 Moreover, in rats and humans, procedures presumably leading to synaptic potentiation or depression result in SWA increases and decreases, respectively. 7-12 More specifically, a study in humans using highdensity EEG found that performing a visuomotor learning task produced a local increase in SWA during subsequent sleep. 7 The increase was restricted to the right parietal cortical areas presumably modified by learning. 13 Moreover, it was specific for NREM sleep, reversible within the first 90 minutes of sleep, and correlated with the improvement in performance after sleep. 7 However, there is no direct evidence that the motor adaptation task used in that study activates neurons in parietal cortex, nor that it causes synaptic potentiation specifically in that region.Previous studies have suggested that activity-dependent genes activated during a specific waking experience may be reactivated during sleep, perhaps to potentiate the same synapses previously engaged during waking. 14 Ribeiro and colleagues found that the exposure to a new environment for 3 hours 15 results in the immediate cortical and hippocampal induction, during waking, of plasticity-related gene zif-268, 16 followed by its downregulation during NREM sleep, and then again by its increased expression during REM sleep (relative to NREM sleep). Intriguingly ~ 3 min of NREM sleep were enough to downregulate waking-induced zif-268 expression, and ~ 2 min of REM sleep were sufficient to detect its selective reinduction, even if both NREM and REM rats were awake during the last 30 min before sacrifice. Another study 17 recently found, using fluorescent in situ hybridization, that the number of hippocampal CA1 neurons showing induction of Arc and/or Homer1a was similar during "rest" periods before and after the exploration of a new environment. However, more cells were active during both exploration and post-task rest than during exploration and pre-task rest. Based on these findings, it h...

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Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep

Cited by 718 publications

References 49 publications

Rapid alterations in cortical protein profiles underlie spontaneous sleep and wake bouts

Rapid alterations in cortical protein profiles underlie spontaneous sleep and wake bouts

A circadian clock in hippocampus is regulated by interaction between oligophrenin-1 and Rev-erbα

Effects of Skilled Training on Sleep Slow Wave Activity and Cortical Gene Expression in the Rat

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