Synaptic Mechanisms of Memory Consolidation during Sleep Slow Oscillations
Open accessAbstract
Sleep is critical for regulation of synaptic efficacy, memories, and learning. However, the underlying mechanisms of how sleep rhythms contribute to consolidating memories acquired during wakefulness remain unclear. Here we studied the role of slow oscillations, 0.2–1 Hz rhythmic transitions between Up and Down states during stage 3/4 sleep, on dynamics of synaptic connectivity in the thalamocortical network model implementing spike-timing-dependent synaptic plasticity. We found that the spatiotemporal pattern of Up-state propagation determines the changes of synaptic strengths between neurons. Furthermore, an external input, mimicking hippocampal ripples, delivered to the cortical network results in input-specific changes of synaptic weights, which persisted after stimulation was removed. These synaptic changes promoted replay of specific firing sequences of the cortical neurons. Our study proposes a neuronal mechanism on how an interaction between hippocampal input, such as mediated by sharp wave-ripple events, cortical slow oscillations, and synaptic plasticity, may lead to consolidation of memories through preferential replay of cortical cell spike sequences during slow-wave sleep. SIGNIFICANCE STATEMENT Sleep is critical for memory and learning. Replay during sleep of temporally ordered spike sequences related to a recent experience was proposed to be a neuronal substrate of memory consolidation. However, specific mechanisms of replay or how spike sequence replay leads to synaptic changes that underlie memory consolidation are still poorly understood. Here we used a detailed computational model of the thalamocortical system to report that interaction between slow cortical oscillations and synaptic plasticity during deep sleep can underlie mapping hippocampal memory traces to persistent cortical representation. This study provided, for the first time, a mechanistic explanation of how slow-wave sleep may promote consolidation of recent memory events.
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Many selective synaptic pruning and refinement processes occur during sleep, and sleep is crucial for proper circuit maturation and long-term memory formation in humans and animals.
“Many of these selective synaptic pruning and refinement processes occur during sleep, and sleep is crucial for proper circuit maturation and long-term memory formation in humans and animals201–204.”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [201]
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Effects of PER3 clock gene polymorphisms on aging-related changes of the cerebral cortex
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Neural Circuits Underlying Social Fear in Rodents: An Integrative Computational Model
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Differential thalamocortical interactions in slow and fast spindle generation: A computational model
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Self-citationLearning-Induced Sequence Reactivation During Sharp-Wave Ripples: A Computational Study
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AISleep: Automated and interpretable sleep staging from single-channel EEG data
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On the theory of mental representation block. a novel perspective on learning and behavior
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(2023) · Oxford University Press eBooks · doi:10.1093/oso/9780198864998.002.0009
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Alain Destexhe, A., & B, T. J. S. A. (2023) · Oxford University Press eBooks · doi:10.1093/oso/9780198864998.003.0006
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A physiological role for sleep oscillations
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Biophysical models of the membrane potential and ionic currents
Alain Destexhe, A., & B, T. J. S. A. (2023) · Oxford University Press eBooks · doi:10.1093/oso/9780198864998.003.0002
Spindle oscillations in the thalamocortical system
Alain Destexhe, A., & B, T. J. S. A. (2023) · Oxford University Press eBooks · doi:10.1093/oso/9780198864998.003.0007
Data available on the Internet
Alain Destexhe, A., & B, T. J. S. A. (2023) · Oxford University Press eBooks · doi:10.1093/oso/9780198864998.005.0003
(2023) · Oxford University Press eBooks · doi:10.1093/oso/9780198864998.002.0006
Electrophysiological properties of thalamic reticular neurons
Alain Destexhe, A., & B, T. J. S. A. (2023) · Oxford University Press eBooks · doi:10.1093/oso/9780198864998.003.0004
(2023) · Oxford University Press eBooks · doi:10.1093/oso/9780198864998.002.0005
(2023) · Oxford University Press eBooks · doi:10.1093/oso/9780198864998.002.0004
Alain Destexhe, A., & B, T. J. S. A. (2023) · Oxford University Press eBooks · doi:10.1093/oso/9780198864998.003.0001
(2023) · Oxford University Press eBooks · doi:10.1093/oso/9780198864998.002.0003
(2023) · Oxford University Press eBooks · doi:10.1093/oso/9780198864998.002.0007
- Authors
- Wei, Y., Krishnan, G. P., & Bazhenov, M.
- Affiliations
- University of California, Riverside (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2016-04-13
- Volume
- 36
- Issue
- 15
- Pages
- 4231-4247
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4829648
- OpenAlex
- W2340922036
- Cited by
- 116
- References
- 67
- Citations by year
- 2026: 8 · 2025: 7 · 2024: 8 · 2023: 28 · 2022: 15 · 2021: 9 · 2020: 13 · 2019: 8 · 2018: 9 · 2017: 8 · 2016: 3
- FWCI
- 5.94
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (MH099645)
- Multidisciplinary University Research Initiative
- Office of Naval Research (N00014-13-1-0672, R01 EB009282, R01 MH099645)
- National Institute of Mental Health (R01MH099645)
- National Institute of Biomedical Imaging and Bioengineering (R01EB009282)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- memory consolidation, slow oscillations, slow-wave sleep, synaptic plasticity, spike-timing-dependent plasticity, thalamocortical network, hippocampal ripples, sharp-wave ripples, computational model
- MeSH terms
- Algorithms, Cerebral Cortex, Computer Simulation, Electroencephalography, Humans, Memory, Models, Neurological, Neuronal Plasticity, Neurons, Sleep, Synapses, Thalamus, Calcium Channels, Sodium Channels, Neural Networks, Computer
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