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Mechanisms of Sleep-Dependent Consolidation of Cortical Plasticity
Open accessAbstract
Sleep is thought to consolidate changes in synaptic strength, but the underlying mechanisms are unknown. We investigated the cellular events involved in this process during ocular dominance plasticity (ODP)-a canonical form of in vivo cortical plasticity triggered by monocular deprivation (MD) and consolidated by sleep via undetermined, activity-dependent mechanisms. We find that sleep consolidates ODP primarily by strengthening cortical responses to nondeprived eye stimulation. Consolidation is inhibited by reversible, intracortical antagonism of NMDA receptors (NMDARs) or cAMP-dependent protein kinase (PKA) during post-MD sleep. Consolidation is also associated with sleep-dependent increases in the activity of remodeling neurons and in the phosphorylation of proteins required for potentiation of glutamatergic synapses. These findings demonstrate that synaptic strengthening via NMDAR and PKA activity is a key step in sleep-dependent consolidation of ODP.
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“Conversely, the GABA A agonist muscimol and also zolpidem impaired sleep-dependent plastic changes in the visual cortex in a developmental model of synaptic plasticity in cats [i.e., ocular dominance plasticity (ODP); see sect.VIIA3 for details] (48,411,1059), suggesting that GABA plays a critical role for plastic processes occurring during sleep.”
From About Sleep's Role in Memory (2013) · cites this paper as [48]
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“Of the GABA A agonistic substances zaleplon, eszopiclone, zolpidem, and triazolam, only zolpidem impaired sleep-dependent ODP, although all substances distinctly reduced REM sleep and increased non-REM sleep (48,1059).”
From About Sleep's Role in Memory (2013) · cites this paper as [48]
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“These sleep-dependent changes are prevented by blocking NMDA receptors or cAMP-dependent protein kinase (PKA) during sleep after monocular experience (48)”
From About Sleep's Role in Memory (2013) · cites this paper as [48]
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“Sleep-dependent ODP is prevented by blocking glutamatergic NMDA receptors or cAMP-dependent protein kinase (PKA) during sleep after monocular deprivation (48).”
From About Sleep's Role in Memory (2013) · cites this paper as [48]
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“The beneficial effect of sleep on consolidation of ODP mainly leads to a strengthening of the cortical responses to stimulation of the nondeprived eye (48).”
From About Sleep's Role in Memory (2013) · cites this paper as [48]
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“ODP was impaired following application of the atypical hypnotic trazodone, probably acting via blocking 5-HT 2c receptors during sleep (48).”
From About Sleep's Role in Memory (2013) · cites this paper as [48]
Experimental — accuracy not yet measuredIn the citing paper
“Work in the visual cortex also shows that sleep affects memory consolidation,80–82”
From Sleep Deprivation and Circadian Disruption (2015) · cites this paper as [80]
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Citations
Cites
Memory - A century of consolidation
McGaugh, J. L. (2000) · Science · doi:10.1126/science.287.5451.248 · Cited by 4,250
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Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity
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Sleep-Dependent Learning and Memory Consolidation
Walker, M. P., & Stickgold, R. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.031 · Cited by 1,113 · cited 1×
“, 2006) and that consolidation can occur during sleep (Frank and Benington, 2006; Walker and Stickgold, 2004).”
BackgroundReplay and Time Compression of Recurring Spike Sequences in the Hippocampus
Nádasdy, Z., Hirase, H., Czurkó, A., Csicsvari, J., & Buzsáki, G. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-21-09497.1999 · Cited by 932 · cited 2×
“, 2000; Pavlides and Winson, 1989; Wilson and McNaughton, 1994), which may provide sufficient neuronal depolarization to activate NMDARs (Nadasky et al., 1999).”
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Diekelmann, S., & Born, J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2762 · Cited by 3,760
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783
“The beneficial effect of sleep on consolidation of ODP mainly leads to a strengthening of the cortical responses to stimulation of the nondeprived eye (48).”
BackgroundInfluentialTononi, G., & Cirelli, C. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.025 · Cited by 2,356
Control of sleep and wakefulness
Brown, R. E., Basheer, R., McKenna, J. T., Strecker, R. E., & McCarley, R. W. (2012) · Physiological Reviews · doi:10.1152/physrev.00032.2011 · Cited by 1,477
Cortical firing and sleep homeostasis
Vyazovskiy, V. V., Olcese, U., Lazimy, Y. M., Faraguna, U., Esser, S. K., Williams, J. C., Cirelli, C., & Tononi, G. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.024 · Cited by 740
Metadata
- Authors
- Aton, S. J., Seibt, J., Dumoulin, M., Jha, S. K., Steinmetz, N., Coleman, T., Naidoo, N., & Frank, M. G.
- Affiliations
- University of Pennsylvania (US)
- Jawaharlal Nehru University (IN)
- Corresponding author
- Frank, Marcos G.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2009-02
- Volume
- 61
- Issue
- 3
- Pages
- 454-466
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC2665998
- OpenAlex
- W2161849272
- Cited by
- 244
- References
- 58
- Citations by year
- 2026: 5 · 2025: 12 · 2024: 12 · 2023: 9 · 2022: 17 · 2021: 11 · 2020: 14 · 2019: 16 · 2018: 16 · 2017: 20 · 2016: 13 · 2015: 12 · 2014: 18 · 2013: 21 · 2012: 15
- FWCI
- 7.58
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Surrey Research Insight Open Access (The University of Surrey) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- National Eye Institute (F32EY006831, R01EY019022, F32EY017766)
- 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
- ocular dominance plasticity, monocular deprivation, NMDA receptor, protein kinase A, synaptic plasticity, glutamatergic synapses, synaptic potentiation, cortical plasticity, protein phosphorylation
- MeSH terms
- Animals, Cats, Cerebral Cortex, Enzyme Inhibitors, Learning, Synaptic Transmission, Neuronal Plasticity, Phosphorylation, Photic Stimulation, Sensory Deprivation, Sleep, Synapses, Receptors, N-Methyl-D-Aspartate, Cyclic AMP-Dependent Protein Kinases, Excitatory Amino Acid Antagonists, Glutamic Acid
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