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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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BackgroundMethodResultInfluentialOffline neuronal activity and synaptic plasticity during sleep and memory consolidation
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Homeostatic Plasticity in the Nervous System
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“Animal studies showed that, after a sustained period of wakefulness, most cortical neurons respond to perturbation stronger and more synchronously than in the control condition [56], signs of cortical hyperexcitability associated with synaptic potentiation [57,58].”
BackgroundSpontaneous neural activity during human non-rapid eye movement sleep
Mascetti, L., Foret, A., Bourdiec, A. S.-L., Muto, V., Kussé, C., Jaspar, M., Matarazzo, L., Dang‐Vu, T. T., Schabus, M., & Maquet, P. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53839-0.00008-9 · Cited by 16
“Moreover, slowwavesaredeemedfaithfully reflecting the dissipation of local sleep pressure accrued during wakefulness (Borbely, 1982) potentially througha recalibrationof glutamatergic neurotransmission (Tononi and Cirelli, 2003; Vyazovskiy et al., 2008, 2009).”
BackgroundRen, J., Zhang, M., Li, T., Zhang, J.-E., Lin, R., Chen, S., Luo, M., & Dong, M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0163500 · Cited by 15
A Hypnic Hypothesis of Alzheimer's Disease
Clark, C. N., & Warren, J. D. (2013) · Neurodegenerative Diseases · doi:10.1159/000350060 · Cited by 14
Liu, B., Seay, M. J., & Buonomano, D. V. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1104-22.2022 · Cited by 18
A role for TMS/EEG in neuropsychiatric disorders
Canali, P. (2014) · Neurology Psychiatry and Brain Research · doi:10.1016/j.npbr.2014.02.001 · Cited by 16
Rapid alterations in cortical protein profiles underlie spontaneous sleep and wake bouts
Vazquez, J., Hall, S. C., Witkowska, H. E., & Greco, M. A. (2008) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21970 · Cited by 18
“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., 2007, 2008].”
ResultThe role of calcium and CaMKII in sleep
Wang, Y., Minami, Y., Ode, K. L., & Ueda, H. R. (2022) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2022.1059421 · Cited by 16
“Interestingly, CaMKIIα with phosphorylated T310 is lower in the dark phase (Vyazovskiy et al., 2008; Diering et al., 2017), suggesting that CaMKIIα undergoes different phosphorylation states depending on the time of day and/or sleep-wake states.”
BackgroundResultLevels of Interference in Long and Short-Term Memory Differentially Modulate Non-REM and REM Sleep
Fraize, N., Carponcy, J., Joseph, M. A., Comte, J., Luppi, P., Libourel, P., Salin, P. A., Malleret, G., & Parmentier, R. (2016) · SLEEP · doi:10.5665/sleep.6322 · Cited by 14
Slow wave detection in sleeping mice: Comparison of traditional and machine learning methods
Bukhtiyarova, O., Soltani, S., Chauvette, S., & Timofeev, I. (2018) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2018.08.016 · Cited by 14
Visual Plasticity in Adulthood: Perspectives from Hebbian and Homeostatic Plasticity
Bang, J. W., Hamilton-Fletcher, G., & Chan, K. C. (2021) · The Neuroscientist · doi:10.1177/10738584211037619 · Cited by 17
Polyphasic Wake/Sleep Episodes in the Fire Ant, Solenopsis Invicta
Cassill, D. L., Brown, S., Swick, D., & Yanev, G. P. (2009) · Journal of Insect Behavior · doi:10.1007/s10905-009-9173-4 · Cited by 14
“Converging evidence supports the hypothesis that neurons and neural processes are universal across species—vertebrates and invertebrates alike (Hildebrand and Shepherd 1997; Griffith and Rosbash 2008; Vyazovskiy et al. 2008).”
BackgroundCircadian Modulation off Neuroplasticity in Humans and Potential Therapeutic Implications
Sale, M. V., Ridding, M. C., & Nordstrom, M. A. (2010) · Reviews in the Neurosciences · doi:10.1515/revneuro.2010.21.1.55 · Cited by 14
Halász, P., Hegyi, M., Siegler, Z., & Fogarasi, A. (2014) · Journal of Epileptology · doi:10.1515/joepi-2015-0015 · Cited by 14
“Patients with shunted hydrocephalus, represented approximately 30% of cases of reported by Veggiotti et al. (1999) and by Caraballo et al. (2008).”
BackgroundModelling Sleep and General Anaesthesia
SLEIGH, J. W., Voss, L. J., Steyn‐Ross, M. L., Steyn‐Ross, D. A., & Wilson, M. T. (2011) · Springer eBooks · doi:10.1007/978-1-4614-0173-5_2 · Cited by 15
“The reason for this phenomenon is not known with certainty, but probably involves some synaptic re-organization which is required for more efficient information handling (Tononi 2009; Tononi and Cirelli 2006; Vyazovskiy et al. 2008).”
BackgroundSleep and vigilance linked to melanism in wild barn owls
Scriba, M. F., Rattenborg, N. C., Dreiss, A. N., Vyssotski, A. L., & Roulin, A. (2014) · Journal of Evolutionary Biology · doi:10.1111/jeb.12450 · Cited by 14
“Conversely, the benefits of sleep include memory consolidation (Diekelmann & Born, 2010), brain maintenance (Vyazovskiy et al., 2008; Xie et al., 2013), energy homeostasis (St-Onge, 2013) and immune system regulation (Opp, 2009).”
BackgroundA metabolic–transcriptional network links sleep and cellular energetics in the brain
Wisor, J. P. (2011) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-011-1030-6 · Cited by 13
“The phosphorylation of GSK3β increases in synaptosomes during enforced wakefulness [80].”
BackgroundRuben, M. D., Hogenesch, J. B., & Smith, D. F. (2019) · Neurologic Clinics · doi:10.1016/j.ncl.2019.03.004 · Cited by 15
Reciprocal interactions between MK-801, sleep deprivation and recovery in modulating rat behaviour
Dubiela, F. P., Messias, M. F., Moreira, K. D. M., Zanlorenci, L. H. F., Grassl, C., Frussa‐Filho, R., Nóbrega, J. N., Tufik, S., & Hipólide, D. C. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.07.031 · Cited by 13
Sleep: hitting the reset button
Griffith, L. C., & Rosbash, M. (2008) · Nature Neuroscience · doi:10.1038/nn0208-123 · Cited by 13
Chronic high‐caloric diet modifies sleep homeostasis in mice
Panagiotou, M., Meijer, J. H., & Deboer, T. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13932 · Cited by 13
Torabi, Z., Rezaie, M., Aramvash, A., Nasiri-Khalili, M.-A., Nasehi, M., Abedi, B., & Vaseghi, S. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.113890 · Cited by 14
Siegel, J. M. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4160-6645-3.00010-4 · Cited by 13
Systems memory consolidation during sleep: oscillations, neuromodulators, and synaptic remodeling
Kim, J., & Park, M. (2025) · BMB Reports · doi:10.5483/bmbrep.2025-0033 · Cited by 19
“Many studies have demonstrated that during sleep, the contact area between cortical axon terminals and dendritic spines is globally reduced, while synaptic AMPA receptor levels also decrease to result in a measurable reduction in synaptic strength (74, 75, 78, 79).”
Sleep as a predictor of tDCS and language therapy outcomes
Herrmann, O., Ficek, B., Webster, K. T., Frangakis, C., Spira, A. P., & Tsapkini, K. (2021) · SLEEP · doi:10.1093/sleep/zsab275 · Cited by 13
Sleep Delta power, age, and sex effects in treatment-resistant depression
Hejazi, N. S., Duncan, W. C., Kheirkhah, M., Kowalczyk, A. M., Riedner, B. A., Oppenheimer, M. R., Momenan, R., Yuan, Q., Kerich, M., Goldman, D. A., et al. (2024) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2024.04.028 · Cited by 16
From macro to micro: slow-wave sleep and its pivotal health implications
Ishii, T., Taweesedt, P. T., Chick, C. F., O'Hara, R. M., & Kawai, M. (2024) · Frontiers in Sleep · doi:10.3389/frsle.2024.1322995 · Cited by 15
Blindfolding during wakefulness causes decrease in sleep slow wave activity
Korf, E. M., Mölle, M., Jan Born, A., & Ngo, H.-V. V. (2017) · Physiological Reports · doi:10.14814/phy2.13239 · Cited by 11
“Moreover, increases in SWA after prolonged wake periods coincide with increases in the expression of markers of synaptic potentiation in cortical tissues (Vyazovskiy et al. 2008; Dash et al. 2012).”
Background
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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