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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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“Another study detected a decrease in GluR1-containing α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) levels during sleep, as well as a decrease in AMPAR, CamKII, and GSK3 beta phosphorylation [56].”
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Memristor-based model of neuronal excitability and synaptic potentiation
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Sleep-Wake and Cortical Synaptic Plasticity
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“The neural mechanisms of the sleep-dependent downscaling are not yet worked out, but a number of molecular and neurophysiological markers related to synaptic potentiation (glutamate receptor type 1 [GluR1]containing a-amino-3-hydroxy-5-methylisoazol-4-propionate [AMPA] receptor; phosphorylation states of AMPARs, Ca2 c…”
BackgroundGorgoni, M., & D’Atri, A. (2015) · ARCHIVES ITALIENNES DE BIOLOGIE · doi:10.12871/000398292015236 · Cited by 6
Sleep/wake movement velocities, trajectories and micro-arousals during maturation in rats
Gradwohl, G., Olini, N., & Huber, R. (2017) · BMC Neuroscience · doi:10.1186/s12868-017-0343-6 · Cited by 7
“GluR1-containing AMPA receptor) of synaptic strength in the rat follow a similar time course: they are increased after periods of wakefulness and decrease in the course of sleep [6].”
Optical imaging and manipulation of sleeping-brain dynamics in memory processing
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Human sleep and its regulation
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Targeting the circadian modulation: novel therapeutic approaches in the management of ASD
Zhang, Y., Chen, Y. J., Li, W., Tang, L., Li, J., & Feng, X. (2024) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2024.1451242 · Cited by 7
“The occurrence of OSRP is speci fi cally observed during the entrained circadian sleep phase and further consolidated during post-stimulus sleep (78, 79).”
BackgroundMethodInfluentialMolecular and cellular rhythms in excitatory and inhibitory neurons in the mouse prefrontal cortex
Burns, J. N., Jenkins, A. K., Yin, R., Zong, W., DePoy, L. M., Petersen, K. A., Kaminsky, M., Vadnie, C. A., Scott, M. R., Tseng, G. C., et al. (2025) · Cerebral Cortex · doi:10.1093/cercor/bhaf188 · Cited by 4
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“In the SCN, GluR2/3-containing AMPARs decrease during the subjective night under DD conditions [111], while in the cortex and hippocampus, GluR1-containing AMPARs increase during wakefulness [112].”
Daily oscillation of the excitation/inhibition ratio is disrupted in two mouse models of autism
Bridi, M., Luo, N., Kim, G., Menarchek, B. J., Lee, R. A., Rodríguez, B. A., Severín, D., Moreno, C., Contreras, A., Wesselborg, C., et al. (2024) · iScience · doi:10.1016/j.isci.2024.111494 · Cited by 6
“22,28,40,50 The ways in which these mechanisms operate in WT mice remain poorly understood, limiting our ability to interpret the exact mechanisms of dysregulation in Fmr1 KO and BTBR mice.”
Citalopram and its use in sleep-deprivation-induced depression
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Synapse-Specific Modulation of Synaptic Responses by Brain States in Hippocampal Pathways
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“Synaptic downscaling has been suggested in the cortex, particularly in the callosal connections of the frontal cortex with electrophysiological methods and in the hippocampus (Hpc) by biochemical methods that do not allow to identify the connections (Vyazovskiy et al., 2008).”
InfluentialNeuroimaging of sleep disorders
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Sleep, Synaptic Plasticity, and Memory
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Five Hours Total Sleep Deprivation Does Not Affect CA1 Dendritic Length or Spine Density
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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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