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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Muscimol and zolpidem impair sleep-dependent plastic changes in visual cortex in cats, suggesting GABA plays critical role for plastic processes during sleep.
“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]
The Results section (‘Sleep enhances ODP’; page unavailable) confirms sleep-dependent visual-cortex plasticity in cats. But this paper tests the NMDA-receptor antagonist APV and the PKA inhibitor Rp-8-Cl-cAMPS, not muscimol or zolpidem. Its References list a separate zolpidem study; our copy does not establish the claimed GABA mechanism. (LLM, conf=0.82)
Experimental — accuracy not yet measuredOf zaleplon, eszopiclone, zolpidem, and triazolam, only zolpidem impaired sleep-dependent ODP, although all reduced REM sleep and increased non-REM sleep.
“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]
The Results (Experiment 1; page unavailable) say that hypnotic drugs profoundly inhibited post-deprivation REM sleep without impairing ODP. The References list a study titled “The non-benzodiazepine hypnotic Zolpidem impairs sleep-dependent cortical plasticity.” Our copy does not establish the four-drug comparison or that all four increased non-REM sleep. (LLM, conf=0.79)
Experimental — accuracy not yet measuredThese sleep-dependent changes are prevented by blocking NMDA receptors or PKA during sleep after monocular experience.
“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]
Sleep-dependent ODP is prevented by blocking glutamatergic NMDA receptors or cAMP-dependent protein kinase (PKA) during sleep after monocular deprivation.
“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]
The beneficial effect of sleep on consolidation of ODP mainly strengthens cortical responses to stimulation of the nondeprived eye.
“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]
ODP was impaired following trazodone, probably via blocking 5-HT2c receptors during sleep.
“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]
The Results section reports that APV and Rp-8-Cl-cAMPS blocked sleep-dependent ODP consolidation, and mentions a prior finding that hypnotic drugs did not impair ODP. Searches for trazodone and 5-HT2C receptors found no passage addressing whether trazodone impaired ODP or acted through that receptor. (LLM, conf=0.73)
Experimental — accuracy not yet measuredSleep affects memory consolidation in the visual cortex.
“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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- 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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