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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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“The homeostatic mechanism of synaptic potentiation during wakefulness and depression during sleep requires glutamatergic signaling and follows the circadian change of AMPA receptor levels (Vyazovskiy et al., 2008), and is influenced by Homer 1a function (Diering et al., 2017).”
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ResultSleep and developmental plasticity
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“, 2007; Diekelmann and Born, 2010; Steriade, 1999) and seemingly at odds (Liu et al., 2010; Vyazovskiy et al., 2008) with our results in the visual cortex.”
ResultCortical Up states induce the selective weakening of subthreshold synaptic inputs
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An essential role for MEF2C in the cortical response to loss of sleep in mice
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BackgroundLocal Sleep Oscillations: Implications for Memory Consolidation
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Wake slow waves in focal human epilepsy impact network activity and cognition
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“These data are consistent with our original conclusions drawn from fewer neurons that Type 3 cells have synapse dynamics opposite to SHY’s predictions.”
Astrocyte regulation of sleep circuits: experimental and modeling perspectives
Fellin, T., Ellenbogen, J. M., Pittà, M. D., Ben‐Jacob, E., & Halassa, M. M. (2012) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2012.00065 · Cited by 52
“In vivo recordings of the neocortex in the freely behaving preparation have shown that neural firing rates (Vyazovskiy et al., 2009) and trans-callosal synaptic transmission (Vyazovskiy et al., 2008) exhibit a similar bidirectional modulation by wake and sleep.”
BackgroundMemory, plasticity and sleep - A role for calcium permeable AMPA receptors?
Shepherd, J. D. (2012) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2012.00049 · Cited by 49
Benedetti, F., Dallaspezia, S., Lorenzi, C., Pirovano, A., Radaelli, D., Locatelli, C., Poletti, S., Colombo, C., & Smeraldi, E. (2011) · Journal of Affective Disorders · doi:10.1016/j.jad.2011.10.039 · Cited by 49
Olonode, E. T., Aderibigbe, A. O., Adeoluwa, O. A., Eduviere, A. T., & Ben‐Azu, B. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.12.024 · Cited by 49
Clawson, B. C., Durkin, J., Suresh, A. K., Pickup, E. J., Broussard, C., & Aton, S. J. (2018) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2018.00040 · Cited by 49
A biomarker-authenticated model of schizophrenia implicating NPTX2 loss of function
Xiao, M.-F., Roh, S., Zhou, J., Chien, D. C.-C., Lucey, B. P., Craig, M. T., Hayes, L. N., Coughlin, J. M., Leweke, F. M., Jia, M., et al. (2021) · Science Advances · doi:10.1126/sciadv.abf6935 · Cited by 47
“The notion that diurnal changes in excitatory synapse strength are balanced by inhibitory circuit modulation is supported by the observation that firing rate does not show a prominent diurnal change ( 41 ) despite evidence of diurnal changes in excitatory synapse strength ( 21 , 42 , 43 ).”
BackgroundWeiss, J. T., & Donlea, J. M. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.777799 · Cited by 49
“At the molecular level, synaptoneurosomes from the cortex and hippocampus of adult rats display increased protein levels of GluA1-containing AMPA receptors after spontaneous and forced wake than after sleep (Vyazovskiy et al., 2008).”
BackgroundAntidepressant chronotherapeutics for bipolar depression
Benedetti, F. (2012) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2012.14.4/fbenedetti · Cited by 50
Overnight Changes in the Slope of Sleep Slow Waves during Infancy
Fattinger, S., Jenni, O. G., Schmitt, B., Achermann, P., & Huber, R. (2014) · SLEEP · doi:10.5665/sleep.3390 · Cited by 53
The role of synaptic activity in the regulation of amyloid beta levels in Alzheimer's disease
Cheng, X., Wu, J., Geng, M., & Xiong, J. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.11.021 · Cited by 51
Davies, B., Brown, L. A., Cais, O., Watson, J., Clayton, A. J., Chang, V. T., Biggs, D., Preece, C., Hernandez-Pliego, P., Krohn, J., et al. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx270 · Cited by 48
“In rats, wakefulness and sleep are characterized by changes in extracellular glutamate levels (18,19), as well as changes in the level and phosphorylation state of GluA1-containing alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate (AMPA)-type ionotropic glutamate receptors (AMPARs) (encoded by Gria1) (20), importan…”
BackgroundRantamäki, T., & Kohtala, S. (2020) · Pharmacological Reviews · doi:10.1124/pr.119.018697 · Cited by 45
“In line with SHY, studies have demonstrated that synapse size and the number of AMPARs in synaptic sites decrease during sleep (Vyazovskiy et al., 2008; de Vivo et al., 2017; Diering et al., 2017).”
BackgroundResultKohtala, S., Alitalo, O., Rosenholm, M., Rozov, S. V., & Rantamäki, T. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107741 · Cited by 47
Aged rats are hypo-responsive to acute restraint: implications for psychosocial stress in aging
Buechel, H. M., Popović, J., Staggs, K. E., Anderson, K. L., Thibault, O., & Blalock, E. M. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00013 · Cited by 48
The Neurobiological Basis of Sleep and Sleep Disorders
Joiner, W. J. (2018) · Physiology · doi:10.1152/physiol.00013.2018 · Cited by 61
“In support of this hypothesis, A release is upregulated by synaptic activity (32, 66), which is generally higher during waking than during sleep (127).”
BackgroundWhat is sleep exactly? Global and local modulations of sleep oscillations all around the clock
Andrillon, T., & Oudiette, D. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105465 · Cited by 52
“…of cytoarchitectural (increase in the number and size of dendritic contacts with time spent awake), genetic (expression of genes involved in synaptic plasticity) and molecular (GluA1-containing AMPA receptors, AMPARs) changes (Vyazovskiy et al., 2008; Maret et al., 2011; de Vivo et al., 2017).”
BackgroundAnaplastic Lymphoma Kinase Acts in the Drosophila Mushroom Body to Negatively Regulate Sleep
Bai, L., & Sehgal, A. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005611 · Cited by 44
“Levels of synaptic proteins are associated with sleep/wake states in both flies and mammals [4,5], and sleep deprivation impairs memory formation in a variety of species, including humans [6], mice [7], and Drosophila [8,9].”
BackgroundCircadian Oscillations within the Hippocampus Support Memory Formation and Persistence
Eckel‐Mahan, K. L. (2012) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2012.00046 · Cited by 48
Cirelli, C. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.04.001 · Cited by 50
Procedural learning and sleep hippocampal low frequencies in humans
Moroni, F., Nobili, L., Curcio, G., Carli, F. D., Tempesta, D., Marzano, C., Gennaro, L. D., Mai, R., Francione, S., Russo, G. L., et al. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.05.027 · Cited by 44
“Accordingly, parallel molecular changes have been recently found in both the cerebral cortex and the hippocampus, as shown by molecular correlates of synaptic potentiation (during wakefulness) and depression (during sleep) being similar in these two forebrain areas (Vyazovskiy et al., 2008).”
InfluentialNeurochemical and electrophysiological changes induced by paradoxical sleep deprivation in rats
Mohammed, H. S., Ezz, H. S. A., Khadrawy, Y. A., & Noor, N. A. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.06.018 · Cited by 45
“In addition, the number of GluR1-containing AMPA receptors increases after waking relative to sleep in cortex and hippocampus [18].”
BackgroundDistinct phosphorylation states of mammalian CaMKIIβ control the induction and maintenance of sleep
Tone, D., Ode, K. L., Zhang, Q., Fujishima, H., Yamada, R. G., Nagashima, Y., Matsumoto, K., Wen, Z., Yoshida, S. Y., Mitani, T. T., et al. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001813 · Cited by 42
Vai, B., Poletti, S., Radaelli, D., Dallaspezia, S., Bulgarelli, C., Locatelli, C., Bollettini, I., Falini, A., Colombo, C., Smeraldi, E., et al. (2015) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2015.07.015 · Cited by 42
Recurrent seizures induce a reversible impairment in a spatial hidden goal task
Lin, H., Holmes, G. L., Kubie, J. L., & Muller, R. U. (2009) · Hippocampus · doi:10.1002/hipo.20565 · Cited by 43
“In this regard, it is noteworthy that recent work shows that sleep favors net synaptic depression whereas wakefulness favors net synaptic potentiation (Tononi and Cirelli, 2006; Vyazovskiy et al., 2008).”
NR2A at CA1 Synapses Is Obligatory for the Susceptibility of Hippocampal Plasticity to Sleep Loss
Longordo, F., Kopp, C., Mishina, M., Luján, R., & Lüthi, A. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1215-09.2009 · Cited by 42
“, 2008) and is accompanied by differential expression of genes and proteins involved in synaptic plasticity (Cirelli, 2006; Vyazovskiy et al., 2008).”
BackgroundInfluentialStem Cell Factor (SCF) is a putative biomarker of antidepressant response
Benedetti, F., Poletti, S., Hoogenboezem, T. A., Locatelli, C., Ambrée, O., de Wit, H., Wijkhuijs, A. J. M., Mazza, E. B., Bulgarelli, C., Vai, B., et al. (2016) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-016-9672-y · Cited by 42
“This interpretation is in agreement with previous findings, showing that electrophysiological measures of cortical excitability in frontal cortex (BA6), which in animal models reflect neuroplasticity and synaptic building (Vyazovskiy et al. 2008), are higher at baseline in responders, and are further increased by anti…”
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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