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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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Homer1a drives homeostatic scaling-down of excitatory synapses during sleep
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“For instance, whereas one study performed Western blot analysis specifically on synaptoneurosomal fractions (Vyazovskiy et al., 2008), others used membrane fractions or whole homogenates (e.”
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Cortisol Inhibits Neuroplasticity Induction in Human Motor Cortex
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BackgroundSleep-wake cycles drive daily dynamics of synaptic phosphorylation
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Hippocampal ripples down-regulate synapses
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Effects of Sleep and Wake on Oligodendrocytes and Their Precursors
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BackgroundResultLaminar analysis of slow wave activity in humans
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BackgroundInfluentialGenetics of circadian rhythms and sleep in human health and disease
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“…slices are consistent with the report that the slope and amplitude of field potentials increase in wake and decrease in sleep in freely moving rats (Vyazovskiy et al., 2008), and with similar observations in humans using transcranial magnetic stimulation and high-density EEG (Bellina et al., 2008).”
BackgroundMethodResultInfluentialLocal Experience-Dependent Changes in the Wake EEG after Prolonged Wakefulness
Hung, C., Sarasso, S., Ferrarelli, F., Riedner, B. A., Ghilardi, M. F., Cirelli, C., & Tononi, G. (2012) · SLEEP · doi:10.5665/sleep.2302 · Cited by 233
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“Of note, in adult rats, levels of phosphorylated GSK- 3ß are higher in wake than in sleep (Vyazovskiy et al., 2008).”
InfluentialInvolvement of Ca2+-Dependent Hyperpolarization in Sleep Duration in Mammals
Tatsuki, F., Sunagawa, G. A., Shi, S., Susaki, E. A., Yukinaga, H., Perrin, D., Sumiyama, K., Ukai‐Tadenuma, M., Fujishima, H., Ohno, R.-I., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.032 · Cited by 200
“Although some experimental results support the synaptic homeostasis hypothesis (Vyazovskiy et al., 2008), others challenge it (Yang et al., 2014).”
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“…far, the evidence is based on glucose metabolism or gene expression related to metabolism of lipids and proteins (Kennedy et al., 1982; Everson et al., 1994; Cirelli and Tononi, 2000b; Netchiporouk et al., 2001; Franken et al., 2003; Brown, 2004; Mackiewicz et al., 2007; Vyazovskiy et al., 2008a).”
BackgroundCarvalho, D. Z., Louis, E. K. S., Knopman, D. S., Boeve, B. F., Lowe, V. J., Roberts, R. O., Mielke, M. M., Przybelski, S. A., Machulda, M. M., Petersen, R. C., et al. (2018) · JAMA Neurology · doi:10.1001/jamaneurol.2018.0049 · Cited by 216
“However,Aβ42generation isalso influencedbysynapticactivity,(24,25,63)which ismaximumduringwakefulnessanddecreasedafter sleep, correlating with slowwave activity.(64) Slowwave activity reduces cerebral cortexmetabolism(65)andalsoappears topromotedownscaling of synaptic connections.”
Control and Function of the Homeostatic Sleep Response by Adenosine A1Receptors
Bjorness, T. E., Kelly, C., Gao, T., Poffenberger, V., & Greene, R. W. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2942-08.2009 · Cited by 201
“It has been suggested that sleep function is involved in the consolidation of learning (Walker and Stickgold, 2004; Stickgold and Walker, 2005) or in the global homeostasis of synaptic plasticity of learning and memory (Vyazovskiy et al., 2008), based on observations of performance with or without intervening episodes…”
BackgroundSleep-Dependent Improvement in Visuomotor Learning: A Causal Role for Slow Waves
Crupi, D., Hulse, B. K., Peterson, M. J., Huber, R., Ansari, H., Coen, M., Cirelli, C., Benca, R. M., Ghilardi, M. F., & Tononi, G. (2009) · Sleep · doi:10.1093/sleep/32.10.1273 · Cited by 228
The role of metaplasticity mechanisms in regulating memory destabilization and reconsolidation
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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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