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 has been linked to sleep dysfunction via the proposed role of sleep in synaptic homeostasis.
“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
The Abstract (page unavailable) proposes that sleep restores synaptic homeostasis, supporting the mechanism named in the claim. The cited passages do not link that mechanism or sleep dysfunction to the salience model of psychosis. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe synaptic homeostasis hypothesis is primarily proposed as a theory of the function of slow wave sleep.
“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
The “Synaptic homeostasis and slow wave activity” section links SHY to slow-wave activity and proposes that slow oscillations contribute to synaptic renormalization. But the paper describes SHY as a hypothesis about the fundamental function of sleep broadly, and its “REM sleep” section considers a possible role for REM sleep. Calling it primarily a theory of slow-wave sleep narrows its stated scope. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe beneficial effect of TMR during non-REM sleep on memory performance is well established across a variety of memory domains.
“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]
In “Synaptic renormalization by down-selection and memory” (page unavailable), the review reports experimental benefits of cuing during sleep and discusses selective enhancement in a model of declarative learning. It does not establish that targeted memory reactivation during non-REM sleep benefits performance across the range of memory domains claimed; its discussion of visuomotor learning concerns sleep benefits generally, not cuing. (LLM, conf=0.84)
Experimental — accuracy not yet measuredSlow wave sleep mediates a downscaling of synaptic strength, allowing informational efficiency to be restored for the next day.
“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
According to the synaptic homeostasis hypothesis, the need for sleep (sleep pressure) arises physiologically as a result of synaptic potentiation in wakefulness.
“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
At the level of global network regulation, sleep is considered to primarily serve downregulation (down-selection) of synaptic connectivity.
“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]
The synaptic homeostasis hypothesis (SHY) by Tononi and Cirelli comprehensively elaborates the view that sleep primarily serves downregulation of synaptic connectivity.
“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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“The salience model of psychosis (Kapur, 2003; Kapur, Mizrahi, & Li, 2005) has been linked to sleep dysfunction via the proposed role of sleep in synaptic homeostasis (Tononi & Cirelli, 2014).”
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Shaping the Default Activity Pattern of the Cortical Network
Sanchez-Vives, M. V., Massimini, M., & Mattia, M. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.015 · Cited by 167 · see citing works
Mechanisms of homeostatic plasticity in the excitatory synapse
Fernandes, D., & Carvalho, A. L. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13687 · Cited by 170 · see citing works
The consequences of sleep deprivation on cognitive performance
Khan, M., & Al-Jahdali, H. H. (2023) · Neurosciences · doi:10.17712/nsj.2023.2.20220108 · Cited by 188 · see citing works
- 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 · 2013: 1
- 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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