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Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration
Open accessAbstract
Summary Sleep is universal, tightly regulated, and its loss impairs cognition. But why does the brain need to disconnect from the environment for hours every day? The synaptic homeostasis hypothesis (SHY) proposes that sleep is the price the brain pays for plasticity. During a waking episode, learning statistical regularities about the current environment requires strengthening connections throughout the brain. This increases cellular needs for energy and supplies, decreases signal-to-noise ratios, and saturates learning. During sleep, spontaneous activity renormalizes net synaptic strength and restores cellular homeostasis. Activity-dependent down-selection of synapses can also explain the benefits of sleep on memory acquisition, consolidation, and integration. This happens through the off-line, comprehensive sampling of statistical regularities incorporated in neuronal circuits over a lifetime. This review considers the rationale and evidence for SHY and points to open issues related to sleep and plasticity.
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“The salience model of psychosis (Kapur, 2003, Kapur et al., 2005) has been linked to sleep dysfunction via the proposed role of sleep in synaptic homeostasis (Tononi & Cirelli, 2014).”
From The role of sleep dysfunction in the occurrence of delusions and hallucinations: A systematic review (2015) · cites this paper as Tononi & Cirelli, 2014
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“On the other hand, the synaptic homeostasis hypothesis is primarily proposed as a theory of the function slow wave sleep, whereas the primary sleep architecture changes directly related to psychosis in the research literature to date involve REM sleep.”
From The role of sleep dysfunction in the occurrence of delusions and hallucinations: A systematic review (2015) · cites this paper as Tononi & Cirelli, 2014
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“The beneficial effect of TMR during non-REM sleep on memory performance is well established across a variety of memory domains, 115 including visuospatial 116-119 and verbal 120,121 declarative memory as well as motor learning.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [121]
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“Slow wave sleep, in this theory, mediates a downscaling of synaptic strength, allowing informational efficiency to be restored for the next day.”
From The role of sleep dysfunction in the occurrence of delusions and hallucinations: A systematic review (2015) · cites this paper as Tononi & Cirelli, 2014
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“According to the synaptic homeostasis hypothesis, the need for sleep (or sleep pressure) arises physiologically as a result of synaptic potentiation in wakefulness (new connections are constantly made in response to the environment while awake, but there is no corresponding downscaling or removing of associations).”
From The role of sleep dysfunction in the occurrence of delusions and hallucinations: A systematic review (2015) · cites this paper as Tononi & Cirelli, 2014
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“At the level of global network regulation, sleep is considered to primarily serve the downregulation, i.e., in a strict sense a down-selection of synaptic connectivity.223”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [223]
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“This view has been comprehensively elaborated in the ''synaptic homeostasis hypothesis'' (SHY) by Tononi and Cirelli [223][224][225] (Figure 2B).”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [223]
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Metadata
- Authors
- Tononi, G., & Cirelli, C.
- Affiliations
- University of Wisconsin System (US)
- University of Wisconsin–Madison (US)
- Corresponding author
- Tononi, Giulio
- Cirelli, Chiara
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2014-01
- Volume
- 81
- Issue
- 1
- Pages
- 12-34
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3921176
- OpenAlex
- W1977647750
- Semantic Scholar
- 61972f1694fafd898abf59be6068327214e9f48a
- Cited by
- 2,356
- References
- 254
- Citations by year
- 2026: 211 · 2025: 247 · 2024: 194 · 2023: 265 · 2022: 196 · 2021: 185 · 2020: 225 · 2019: 228 · 2018: 149 · 2017: 142 · 2016: 127 · 2015: 126 · 2014: 57
- FWCI
- 14.54
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH099231, R01MH091326)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- sleep, synaptic homeostasis hypothesis, synaptic plasticity, cellular homeostasis, memory consolidation, memory integration, signal-to-noise ratio, learning, spontaneous neuronal activity
- MeSH terms
- Animals, Brain, Homeostasis, Humans, Learning, Neuronal Plasticity, Sleep, Synapses
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