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Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep
Abstract
Plastic changes occurring during wakefulness aid in the acquisition and consolidation of memories. For some memories, further consolidation requires sleep, but whether plastic processes during wakefulness and sleep differ is unclear. We show that, in rat cortex and hippocampus, GluR1-containing AMPA receptor (AMPAR) levels are high during wakefulness and low during sleep, and changes in the phosphorylation states of AMPARs, CamKII and GSK3beta are consistent with synaptic potentiation during wakefulness and depression during sleep. Furthermore, slope and amplitude of cortical evoked responses increase after wakefulness, decrease after sleep and correlate with changes in slow-wave activity, a marker of sleep pressure. Changes in molecular and electrophysiological indicators of synaptic strength are largely independent of the time of day. Finally, cortical long-term potentiation can be easily induced after sleep, but not after wakefulness. Thus, wakefulness appears to be associated with net synaptic potentiation, whereas sleep may favor global synaptic depression, thereby preserving an overall balance of synaptic strength.
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“Levels of postsynaptic glutamatergic AMPA receptors containing the glutamate receptor (GluR1)-1 subunit reliably indicate synaptic plasticity and were revealed to be high during wakefulness and distinctly lower (by 40%) during sleep (1264).”
From About Sleep's Role in Memory (2013) · cites this paper as [1264]
In the citing paper
“Indeed, in rats, slope and amplitude of the electrically evoked cortical potential as indicators of synaptic strength progressively increased during sustained wakefulness and decreased after sleep, and these changes were correlated with SWA (1264).”
From About Sleep's Role in Memory (2013) · cites this paper as [1264]
In the citing paper
“Prolonged waking decreases the ability to induce further LTP in various models, which in turn should inhibit learning (Vyazovskiy et al., 2008);”
From Biological rhythms, higher brain function, and behavior: Gaps, opportunities, and challenges (2009) · cites this paper as Vyazovskiy et al., 2008
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Vyazovskiy, V. V., Faraguna, U., Cirelli, C., & Tononi, G. (2009) · Journal of Neurophysiology · doi:10.1152/jn.91157.2008 · Cited by 145
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BackgroundResultDevelopmental aspects of sleep slow waves
Ringli, M., & Huber, R. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53839-0.00005-3 · Cited by 143
Effects of Skilled Training on Sleep Slow Wave Activity and Cortical Gene Expression in the Rat
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Identification of Neurons with a Privileged Role in Sleep Homeostasis in Drosophila melanogaster
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“Indeed, as in rats (Cirelli et al., 2004; Vyazovskiy et al., 2008), wakefulness and sleep are associated with the expression of genes involved in synaptic potentiation and longterm depression, respectively, in the telencephalon of whitecrowned sparrows (Jones et al., 2008b).”
BackgroundInfluentialSleep Behavior and Sleep Regulation from Infancy through Adolescence: Normative Aspects
Jenni, O. G., & Carskadon, M. A. (2007) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2007.05.001 · Cited by 132
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BackgroundPhagocytic elimination of synapses by microglia during sleep
Choudhury, M. E., Miyanishi, K., Takeda, H., Islam, A., Matsuoka, N., Kubo, M., Matsumoto, S., Kunieda, T., Nomoto, M., Yano, H., et al. (2019) · Glia · doi:10.1002/glia.23698 · Cited by 128
“Synapse numbers and activity are reduced during sleep (de Vivo et al., 2017; Diering et al., 2017; Hayashi et al., 2013; Maret, Faraguna, Nelson, Cirelli, & Tononi, 2011; Vyazovskiy et al., 2008).”
BackgroundLinking Network Activity to Synaptic Plasticity during Sleep: Hypotheses and Recent Data
Puentes-Mestril, C., & Aton, S. J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00061 · Cited by 130
“What Is the Evidence for Sleep-Dependent Reductions in Synaptic Strength? Since SHY was first proposed, data to support the hypothesis have come from biochemical (Vyazovskiy et al., 2008), electrophysiological (Vyazovskiy et al.”
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Benca, R., Duncan, M. J., Frank, E., McClung, C., Nelson, R. J., & Vicentic, A. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2009.09.005 · Cited by 125
“Prolonged waking decreases the ability to induce further LTP in various models, which in turn should inhibit learning (Vyazovskiy et al., 2008); this is supported by studies in normal humans demonstrating that sleep deprivation impairs the ability to acquire new memories (Yoo et al., 2007).”
ResultYang, G., & Gan, W. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20996 · Cited by 131
“On the other hand, sleep may be involved in synaptic downscaling that may be important for brain function during subsequent wakefulness (Vyazovskiy et al., 2008; Gilestro et al., 2009; Liu et al., 2010).”
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“Numerous studies show a close relationship between sleep SWA and synaptic strength (Esser et al., 2007; Vyazovskiy et al., 2008; Vyazovskiy et al., 2007).”
InfluentialRelations between sleep patterns early in life and brain development: A review
Lokhandwala, S., & Spencer, R. M. C. (2022) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2022.101130 · Cited by 151
“Elegant work done in rat models has shown that there is increased intracortical connectivity during wakefulness and decreased connectivity during sleep (Diering et al., 2017; Vyazovskiy et al., 2008).”
BackgroundSleep promotes cortical response potentiation following visual experience
Aton, S. J., Suresh, A., Broussard, C., & Frank, M. G. (2014) · SLEEP · doi:10.5665/sleep.3830 · Cited by 122
Hippocampal memory consolidation during sleep: a comparison of mammals and birds
Rattenborg, N. C., Martínez-González, D., Roth, T. C., & Витальевич, П. В. (2010) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2010.00165.x · Cited by 128
“During wakefulness, engagement with the environment is thought to cause long-term potentiation and a concomitant increase in synaptic strength and number throughout the neocortex (Vyazovskiy et al., 2008; Liu et al., 2010).”
BackgroundSleep, clocks, and synaptic plasticity
Frank, M. G., & Cantera, R. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.06.005 · Cited by 125
TheDrosophilaFragile X Mental Retardation Gene Regulates Sleep Need
Bushey, D., Tononi, G., & Cirelli, C. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4830-08.2009 · Cited by 120
“Moreover, in adult rats, established molecular and/or electrophysiological markers of synaptic strength are high after wakefulness and low after sleep in cortex and hippocampus (Vyazovskiy et al., 2008).”
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“The synaptic homeostasis hypothesis (Tononi and Cirelli, 2003) proposes that, whereas sensory experience at wake leads to strengthening of the associated neocortical synapses, slowwave sleep (SWS) leads to a net depression of synaptic weights (Vyazovskiy et al., 2008; Liu et al., 2010).”
BackgroundBenedetti, F., Riccaboni, R., Locatelli, C., Poletti, S., Dallaspezia, S., & Colombo, C. (2014) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.13m08455 · Cited by 116
Vassalli, A., & Franken, P. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1700983114 · Cited by 124
“SD indeed is found to impair LTP capacity (47, 48) that only sleep can restore.”
BackgroundConsequences of sleep deprivation on neurotransmitter receptor expression and function
Longordo, F., Kopp, C., & Lüthi, A. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06719.x · Cited by 120
“In addition, a recent study using synaptoneurosomes, a tissue fraction rich in both membrane-bound and cytosolic synaptic proteins, showed that a substantial number of postsynaptic components of the excitatory synapse vary as a function of the recent sleep-wake behavior (Vyazovskiy et al., 2008).”
BackgroundNetwork homeostasis: a matter of coordination
Maffei, A., & Fontanini, A. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.05.012 · Cited by 116
Sleep slow oscillation and plasticity
Timofeev, I., & Chauvette, S. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.03.019 · Cited by 121
“Levels of GluA1containing AMPARs are 30–40% higher after wakefulness than after sleep in rats [51].”
BackgroundNeuroimaging, cognition, light and circadian rhythms
Gaggioni, G., Maquet, P., Schmidt, C., Dijk, D., & Vandewalle, G. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00126 · Cited by 125
“…(Basheer et al., 2004) and cytokines (Krueger, 2008)), from an increase in extracellular glutamate level (Dash et al., 2009), and/or from an experiencedependent increase of average brain synaptic strength, excitability and size during wakefulness (Vyazovskiy et al., 2008; Bushey et al., 2011).”
BackgroundElectrophysiological correlates of sleep homeostasis in freely behaving rats
Vyazovskiy, V. V., Cirelli, C., & Tononi, G. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53839-0.00002-8 · Cited by 117
“To address this possibility, we used an LTP induction paradigm as in (Racine et al., 1995; Vyazovskiy et al., 2008).”
InfluentialTime to Be SHY? Some Comments on Sleep and Synaptic Homeostasis
Tononi, G., & Cirelli, C. (2012) · Neural Plasticity · doi:10.1155/2012/415250 · Cited by 124
“Moreover, in the rat cortex, the wake-related increase in the slope of local field potentials discussed above correlates with the increase in SWA: the steeper the slope at the end of wake, the higher SWA at sleep onset [5].”
BackgroundInfluentialPrimed to Sleep: The Dynamics of Synaptic Plasticity Across Brain States
Seibt, J., & Frank, M. G. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00002 · Cited by 120
Huang, S., Treviño, M., He, K., Ardiles, Á. O., Pasquale, R. D., Guo, Y., Palacios, A. G., Huganir, R. L., & Kirkwood, A. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.023 · Cited by 112
“Whether neuromodulators play a role in natural instances of synaptic scaling, as during sleep (Vyazovskiy et al., 2008) or in response to altered sensory experience (Desai et al., 2002; Goel et al., 2006) remains to be determined.”
BackgroundSleep and Synaptic Renormalization: A Computational Study
Olcese, U., Esser, S. K., & Tononi, G. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00593.2010 · Cited by 117
“…link 91 between plasticity and sleep SWA is shown, for example, by the observation that electrophysiological 92 markers of synaptic strength, such as the amplitude and slope of field potentials evoked during 93 wakefulness, correlate with SWA values during subsequent sleep (Vyazovskiy et al. 2008).”
BackgroundInfluentialOrbán, C., Kong, R., Li, J., Chee, M. W. L., & Yeo, B. T. T. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000602 · Cited by 104
“Examples include diurnal variation in synaptic protein levels and synaptic strength [6–8], the amplitude and slope of cortical or motor-evoked responses [6,9,10], and theta power [11,12], as well as changes in cerebral blood flow (CBF) [13–15], task-related blood oxygen level–dependent (BOLD) activation [16– 18], rest…”
BackgroundMolecular and anatomical signatures of sleep deprivation in the mouse brain
Thompson, C. L. (2010) · Frontiers in Neuroscience · doi:10.3389/fnins.2010.00165 · Cited by 114
“, whole cerebral cortex) consisting of numerous heterogenous cell types and regions which may both IntroductIon Sleep is necessary for normal neural function, including synaptic plasticity and homeostatic synaptic downscaling (reviewed in Tononi and Cirelli, 2006; Vyazovskiy et al., 2008).”
BackgroundSleep function: current questions and new approaches
Vassalli, A., & Dijk, D. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06767.x · Cited by 110
Frank, M. G., & Heller, H. C. (2018) · Handbook of experimental pharmacology · doi:10.1007/164_2018_140 · Cited by 121
Interplay between population firing stability and single neuron dynamics in hippocampal networks
Slomowitz, E., Styr, B., Vertkin, I., Milshtein-Parush, H., Nelken, I., Slutsky, M., & Slutsky, I. (2015) · eLife · doi:10.7554/elife.04378 · Cited by 108
Perspectives in affective disorders: Clocks and sleep
Wirz‐Justice, A., & Benedetti, F. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14362 · Cited by 111
Microglia-mediated synaptic pruning is impaired in sleep-deprived adolescent mice
Tuan, L., & Lee, L. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104517 · Cited by 107
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“The hypothesis was supported by studies that applied TMS before sleep onset to manipulate slow wave oscillations during sleep [43,44].”
Altered sleep homeostasis correlates with cognitive impairment in patients with focal epilepsy
Boly, M., Jones, B., Findlay, G., Plumley, E., Mensen, A., Hermann, B. P., Tononi, G., & Maganti, R. K. (2017) · Brain · doi:10.1093/brain/awx017 · Cited by 108
“In both humans and animals, wakefulness leads to a net, global increase in synaptic strength throughout the cerebral cortex, which is followed by a global increase in sleep SWA power that is proportional to the duration of waking activities (Vyazovskiy et al., 2008; Hung et al., 2013).”
BackgroundSleep Promotes Downward Firing Rate Homeostasis
Pacheco, A. T., Bottorff, J., Gao, Y. B., & Turrigiano, G. G. (2020) · Neuron · doi:10.1016/j.neuron.2020.11.001 · Cited by 103
Cerebral blood flow changes after a day of wake, sleep, and sleep deprivation
Elvsåshagen, T., Mutsaerts, H. J. M. M., Zak, N., Norbom, L. B., Quraishi, S. H., Pedersen, P. Ø., Malt, U. F., Westlye, L. T., Someren, E. J. W. V., Bjørnerud, A., et al. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.11.032 · Cited by 100
“This hypothesis is supported by a growing body of animal and human evidence (Vyazovskiy et al., 2008; Liu et al., 2010; Maret et al., 2011; Gilestro et al., 2009; Bushey et al., 2011; Huber et al., 2013; Hung et al., 2013) and suggests that learning and experience during wake promote synaptic strengthening, whereas sl…”
Salehinejad, M. A., Ghanavati, E., Reinders, J., Hengstler, J. G., Kuo, M.-F., & Nitsche, M. A. (2022) · eLife · doi:10.7554/elife.69308 · Cited by 94
“These sleepdependent changes of cortical excitability are in line with the synaptic homeostasis hypothesis postulating that synaptic strength is increasingly potentiated during wakefulness and saturated if wakefulness is extended (Tononi and Cirelli, 2003; Vyazovskiy et al., 2008).”
BackgroundResultInfluentialLocal sleep homeostasis in the avian brain: convergence of sleep function in mammals and birds?
Lesku, J. A., Vyssotski, A. L., Martinez-Gonzalez, D., Wilzeck, C., & Rattenborg, N. C. (2011) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2010.2316 · Cited by 112
Implicit Vocabulary Learning during Sleep Is Bound to Slow-Wave Peaks
Züst, M. A., Ruch, S., Wiest, R., & Henke, K. (2019) · Current Biology · doi:10.1016/j.cub.2018.12.038 · Cited by 103
“Hence, slow-wave sleep appears to entail windows of opportunity for synaptic potentiation besides its known role in synaptic depression emphasized in the synaptic homeostasis theory of sleep [14, 63].”
Ketamine: differential neurophysiological dynamics in functional networks in the rat brain
Ahnaou, A., Huysmans, H., Biermans, R., Manyakov, N. V., & Drinkenburg, W. H. I. M. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.198 · Cited by 97
Sleep regulation of the distribution of cortical firing rates
Levenstein, D., Watson, B. O., Rinzel, J., & Buzsáki, G. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.02.013 · Cited by 101
Sleep: a synchrony of cell activity‐driven small network states
Krueger, J. M., Huang, Y. H., Rector, D. M., & Buysse, D. J. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12238 · Cited by 98
“tors (AMPARs) as well as LTD-like molecular signatures, including decreased phosphorylation of the AMPAR subunit GluR1 and CaMKII (Vyazovskiy et al., 2008; Hagewoud et al., 2010).”
BackgroundInfluentialSzabo, S. T., Machado‐Vieira, R., Yuan, P., Wang, Y., Wei, Y., Falke, C., Cirelli, C., Tononi, G., Manji, H. K., & Du, J. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.08.015 · Cited by 98
“Consistent with previous study (Vyazovskiy et al., 2008), phosphorylation of GluA1S831 had a very strong trend to increase by 150% in sleep-deprived animals (N=8 for each group, student’s t test, p=0.”
BackgroundResultInfluentialSpano, G. M., Banningh, S. W., Marshall, W., de Vivo, L., Bellesi, M., Loschky, S. S., Tononi, G., & Cirelli, C. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0380-19.2019 · Cited by 99
“For instance, it was found that mean expression levels of synaptic AMPA receptors are higher after wake than after sleep in rat cortex and hippocampus and in mouse whole forebrain (Vyazovskiy et al., 2008; Diering et al., 2017).”
BackgroundPlasticity during sleep is linked to specific regulation of cortical circuit activity
Niethard, N., Burgalossi, A., & Born, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00065 · Cited by 89
“Importantly, whereas sleep globally reduced levels of AMPA receptors (Vyazovskiy et al., 2008), a small fraction of spines showed increased AMPA receptor levels after sleep.”
BackgroundErasing Synapses in Sleep: Is It Time to Be SHY?
Frank, M. G. (2012) · Neural Plasticity · doi:10.1155/2012/264378 · Cited by 117
“They might also contribute to relative (sleep versus wake) differences in synaptic proteins, plasticity molecules, and dendritic spine morphology obtained from rodents sacrificed after long periods of waking and sleep [20, 21, 31].”
BackgroundInfluentialBERSAGLIERE, A., & ACHERMANN, P. (2010) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2009.00775.x · Cited by 102
Circadian dynamics in measures of cortical excitation and inhibition balance
Chellappa, S. L., Gaggioni, G., Ly, J. Q. M., Papachilleos, S., Borsu, C., Brzozowski, A., Rosanova, M., Sarasso, S., Luxen, A., Middleton, B., et al. (2016) · Scientific Reports · doi:10.1038/srep33661 · Cited by 84
Microglia modulate hippocampal synaptic transmission and sleep duration along the light/dark cycle
Corsi, G., Picard, K., Castro, M. A. D., Garofalo, S., Tucci, F., Chece, G., Percio, C. D., Golia, M. T., Raspa, M., Scavizzi, F., et al. (2021) · Glia · doi:10.1002/glia.24090 · Cited by 91
“…on neurons along with the expression levels of AMPA receptors can change across the light/dark cycle, resulting in an increased frequency and/or amplitude of the mEPSC during the dark phase (Vyazovskiy et al., 2008; Liu et al., 2010; Maret et al., 2011; Yang et al., 2014; Bridi et al., 2020).”
BackgroundCircadian rhythms and memory: not so simple as cogs and gears
Eckel‐Mahan, K. L., & Storm, D. R. (2009) · EMBO Reports · doi:10.1038/embor.2009.123 · Cited by 99
“Interestingly, in vivo cortical LTP in rodents is partly occluded after hours of wakefulness, when the net synaptic facilitation is high; however, it is again inducible after several hours of sleep, during which cortical and hippocampal synaptic strength undergoes a net depression”
BackgroundCasarotto, S., Canali, P., Rosanova, M., Pigorini, A., Fecchio, M., Mariotti, M., Lucca, A., Colombo, C., Benedetti, F., & Massimini, M. (2012) · Brain Topography · doi:10.1007/s10548-012-0256-8 · Cited by 90
“IRS was computed on single-trial TEPs averaged in space across the ROI channels: specifically, it was defined as the mean first derivative of the rising side of the positive wave (Vyazovskiy et al. 2008) of the early TMS-evoked component (Fig.”
MethodMemory encoding is impaired after multiple nights of partial sleep restriction
Cousins, J. N., Sasmita, K., & Chee, M. W. L. (2017) · Journal of Sleep Research · doi:10.1111/jsr.12578 · Cited by 95
“Impaired learning after sleep deprivation (Hagewoud et al., 2010; Li et al., 2009) has been linked to a reduced capacity for long-term potentiation in animal studies (Campbell et al., 2002; Vyazovskiy et al., 2008).”
BackgroundUsami, K., Matsumoto, R., Kobayashi, K., Hitomi, T., Shimotake, A., Kikuchi, T., Matsuhashi, M., Kunieda, T., Mikuni, N., Miyamoto, S., et al. (2015) · Human Brain Mapping · doi:10.1002/hbm.22948 · Cited by 87
“It is reported that SWA decreases homeostatically in the course of NREM sleep [Riedner et al., 2007] and that spindles characterizing sleep Stage II become more diffuse in late sleep [Nir et al., 2011].”
MethodInfluentialMairesse, J., Silletti, V., Laloux, C., Zuena, A. R., Giovine, A., Consolazione, M., Camp, G. V., Malagodi, M., Gaetani, S., Cianci, S., et al. (2012) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145711001970 · Cited by 93
“and mood disorders is strengthened by the evidence that the sleep/wake cycle critically regulates synaptic plasticity in the hippocampus and cerebral cortex, with wakefulness and sleep being associated with synaptic potentiation and depression, respectively (Vyazovskiy et al. 2008).”
Selbach, O., Bohla, C., Barbara, A. B., Doreulee, N., Eriksson, K. S., Sergeeva, O. A., & Haas, H. L. (2009) · Acta Physiologica · doi:10.1111/j.1748-1716.2009.02021.x · Cited by 88
“Similar signatures may thus apply to a joint recruitment and stabilization of synaptic weight changes (Vyazovskiy et al. 2008, Aton et al. 2009) in other wake-active regions of the brain (Bayer et al. 2004, Lambe et al. 2007).”
BackgroundInfluentialThe Roles of Cortical Slow Waves in Synaptic Plasticity and Memory Consolidation
Miyamoto, D., Hirai, D., & Murayama, M. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00092 · Cited by 97
Contribution of sedative-hypnotic agents to delirium via modulation of the sleep pathway
Sanders, R. D., & Maze, M. (2010) · Canadian Journal of Anesthesia/Journal canadien d anesthésie · doi:10.1007/s12630-010-9421-2 · Cited by 89
Synaptic plasticity model of therapeutic sleep deprivation in major depression
Wolf, E., Kühn, M., Normann, C., Mainberger, F., Maier, J. G., Maywald, S., Bredl, A., Klöppel, S., Biber, K. P. H., van Calker, D., et al. (2015) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2015.11.003 · Cited by 88
TMS-EEG: An emerging tool to study the neurophysiologic biomarkers of psychiatric disorders
Cao, K.-X., Ma, M.-L., Wang, C.-Z., Iqbal, J., Si, J., Xue, Y.-X., & Yang, J. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108574 · Cited by 91
Brain repair after stroke—a novel neurological model
Small, S. L., Buccino, G., & Solodkin, A. (2013) · Nature Reviews Neurology · doi:10.1038/nrneurol.2013.222 · Cited by 88
Gorgoni, M., D’Atri, A., Lauri, G., Rossini, P. M., Ferlazzo, F., & Gennaro, L. D. (2013) · Neural Plasticity · doi:10.1155/2013/103949 · Cited by 95
“Vyazovskiy and co-workers [41] found that synaptic strength, in terms of amplitude and slope of local field power”
InfluentialHow Aging Affects Sleep-Dependent Memory Consolidation?
Harand, C., Bertran, F., Doidy, F., Guénolé, F., Desgranges, B., Eustache, F., & Rauchs, G. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00008 · Cited by 83
“This hypothesis has found experimental support in animals (Vyazovskiy et al., 2008; Bushey et al., 2011) and in humans (Huber et al., 2004; Van Der Werf et al., 2009).”
ResultSleep Deprivation Therapy for Depression
Dallaspezia, S., & Benedetti, F. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_363 · Cited by 86
Physiologically based arousal state estimation and dynamics
Abeysuriya, R., RENNIE, C. J., & Robinson, P. A. (2015) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2015.06.002 · Cited by 82
Circadian regulation of membrane physiology in neural oscillators throughout the brain
Paul, J. R., Davis, J. A., Goode, L. K., Becker, B., Fusilier, A. R., Meador-Woodruff, A., & Gamble, K. L. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14343 · Cited by 81
Feld, G. B., & Jan Born, A. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0490-9 · Cited by 84
The History and Current State of Antidepressant Clinical Trial Design
Gelenberg, A. J., Thase, M. E., Meyer, R. E., Goodwin, F. K., Katz, M. M., KRAEMER, H. C., Potter, W. Z., Shelton, R. C., D, M. F. M., Khan, A., et al. (2008) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.v69n1001 · Cited by 78
The why and how of sleep-dependent synaptic down-selection
Cirelli, C., & Tononi, G. (2022) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2021.02.007 · Cited by 74
“Another mechanism may include the wake-dependent phosphorylation of GluA1 at Ser845 [58,59], which makes these receptors resistant to downscaling [57].”
BackgroundInfluentialDo seizures and epileptic activity worsen epilepsy and deteriorate cognitive function?
AVANZINI, G., Depaulis, A., Tassinari, A., & de Curtis, M. (2013) · Epilepsia · doi:10.1111/epi.12418 · Cited by 82
“The plausibility of this hypothesis has been recently demonstrated by B€olsterli et al. (2011), who analyzed the time course of the slope of EEG slow waves, a sensitive measure of cortical synaptic strength (Vyazovskiy et al., 2008) in children with ESES and control subjects.”
BackgroundLongordo, F., Fan, J., Steimer, T. J., Kopp, C., & Lüthi, A. (2011) · SLEEP · doi:10.1093/sleep/34.5.679 · Cited by 78
Animal Studies on the Role of Sleep in Memory: From Behavioral Performance to Molecular Mechanisms
Havekes, R., Meerlo, P., & Abel, T. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2015_369 · Cited by 78
“…animals are kept awake by introducing novel objects and new nesting material, or by actually taking them out of their cage, handling them, and exposing them to novel environments (Cirelli and Tononi 2000; Cirelli et al. 2006; Kopp et al. 2006; Vyazovskiy et al. 2008; Longordo et al. 2009a, b).”
Christensen, J., Li, C. N., & Mychasiuk, R. (2022) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x221082786 · Cited by 78
History and future of comparative analyses in sleep research
Lesku, J. A., Roth, T. C., Rattenborg, N. C., Amlaner, C. J., & Lima, S. L. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.04.002 · Cited by 78
“…be expected to engage in less sleep than those in the wild, as the need for sleep is determined (in part) by the duration and intensity of wakefulness (Huber et al., 2007; Vyazovskiy et al., 2008), such that the more sterile laboratory environment might be less stimulating than a more wild setting.”
BackgroundInfluentialEnergy-Efficient Information Transfer by Visual Pathway Synapses
Harris, J. J., Jolivet, R., Engl, E., & Attwell, D. (2015) · Current Biology · doi:10.1016/j.cub.2015.10.063 · Cited by 82
Pennybaker, S. J., Niciu, M. J., Luckenbaugh, D. A., & Zarate, C. A. (2016) · Journal of Affective Disorders · doi:10.1016/j.jad.2016.10.026 · Cited by 76
“Increased slow-wave sleep is considered a biomarker of enhanced synaptic plasticity (Vyazovskiy et al., 2008), which has been implicated in ketamine’s antidepressant mechanism of action (Bjorkholm and Monteggia, 2016; Duncan et al., 2013).”
BackgroundSleep and Synaptic Plasticity in the Developing and Adult Brain
Frank, M. G. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_305 · Cited by 80
“These include exogenous, transcallosal electrical stimulation (Vyazovskiy et al. 2008), intracranial infusions of chemicals that cause cortical spreading depression (Faraguna et al.”
BackgroundKetamine, Sleep, and Depression: Current Status and New Questions
Duncan, W. C., & Zarate, C. A. (2013) · Current Psychiatry Reports · doi:10.1007/s11920-013-0394-z · Cited by 76
Sleep and homeostatic control of plasticity
Lanza, G., DelRosso, L. M., & Ferri, R. (2022) · Handbook of clinical neurology · doi:10.1016/b978-0-12-819410-2.00004-7 · Cited by 78
Sleep and protein synthesis-dependent synaptic plasticity: impacts of sleep loss and stress
Grønli, J., Soule, J. D., & Bramham, C. R. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00224 · Cited by 79
“Matching these electrophysiological changes, the abundance of GluA1-containing AMPARs in biochemically fractionated synaptosomes was 40% higher after wakefulness than after sleep (Vyazovskiy et al., 2008; Hinard et al., 2012).”
BackgroundSleep smart—optimizing sleep for declarative learning and memory
Feld, G. B., & Diekelmann, S. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.00622 · Cited by 87
Removal of Synaptic Ca 2+ -Permeable AMPA Receptors during Sleep
Lanté, F., Toledo-Salas, J.-C., Ondrejcak, T., Rowan, M. J., & Ulrich, D. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3210-10.2011 · Cited by 74
“These sleep–wake cycle-dependent changes at neocortical synapses were mainly attributed to nonrapid eye movement (NREM) sleep activity (Vyazovskiy et al., 2008).”
BackgroundInfluentialMemory processes during sleep: beyond the standard consolidation theory
Axmacher, N., Draguhn, A., Elger, C. E., & Fell, J. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0019-1 · Cited by 80
“[117] observed a net synaptic potentiation during waking state and a depression during sleep.”
Sleep as a Therapeutic Target in the Aging Brain
Bah, T. M., Goodman, J. R., & Iliff, J. J. (2019) · Neurotherapeutics · doi:10.1007/s13311-019-00769-6 · Cited by 76
Human REM sleep recalibrates neural activity in support of memory formation
Lendner, J. D., Niethard, N., Mander, B. A., van Schalkwijk, F. J., Schuh‐Hofer, S., Schmidt, H., Knight, R. T., Jan Born, A., Walker, M. P., Lin, J. J., et al. (2023) · Science Advances · doi:10.1126/sciadv.adj1895 · Cited by 82
Acosta-Peña, E., Camacho‐Abrego, I., Melgarejo-Gutiérrez, M. A., Flores, G., Drucker-Colı́n, R., & García‐García, F. (2014) · Synapse · doi:10.1002/syn.21779 · Cited by 73
“…is not clear; however, it could suggest that sleep may play an active role in synaptic network remodeling (Gilestro et al., 2009; Liu et al., 2010; Vyazovskiy et al., 2008) through erasing unnecessary connections and providing the brain additional storage capability and well functioning as…”
Metadata
- Authors
- Vyazovskiy, V. V., Cirelli, C., Pfister-Genskow, M., Faraguna, U., & Tononi, G.
- Affiliations
- University of Wisconsin–Madison (US)
- Corresponding author
- Cirelli, Chiara
- Tononi, Giulio
- Venue
- Nature Neuroscience
- Published
- 2008-01-20
- Volume
- 11
- Issue
- 2
- Pages
- 200-208
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2109919607
- Cited by
- 837
- References
- 53
- Citations by year
- 2026: 27 · 2025: 48 · 2024: 49 · 2023: 28 · 2022: 44 · 2021: 48 · 2020: 40 · 2019: 60 · 2018: 37 · 2017: 57 · 2016: 36 · 2015: 43 · 2014: 45 · 2013: 62 · 2012: 53
- FWCI
- 26.92
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Surrey Research Insight Open Access (The University of Surrey) (submittedVersion)
- Open Research (University of Surrey) (submittedVersion)
- CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- National Institutes of Health (DP1OD000579)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- synaptic potentiation, synaptic depression, sleep, wakefulness, AMPA receptors, GluR1, receptor phosphorylation, CaMKII, GSK3β, slow-wave activity, sleep pressure, cortical evoked potentials, long-term potentiation, memory consolidation, hippocampus, cortex, synaptic plasticity
- MeSH terms
- Glycogen Synthase Kinase 3 beta, Animals, Behavior, Animal, Cerebral Cortex, Electroencephalography, Electromyography, Gene Expression Regulation, Hippocampus, Male, Neuronal Plasticity, Phosphorylation, Rats, Inbred WKY, Serine, Sleep, Synapses, Temperature, Threonine, Wakefulness, Receptors, AMPA, Glycogen Synthase Kinase 3, Rats, Calcium-Calmodulin-Dependent Protein Kinase Type 2
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