Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration

By Giulio Tononi, Chiara Cirelli. 2014

2,069 citations recorded by the source corpus.

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.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

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Citations in the corpus

Replay in Deep Learning: Current Approaches and Missing Biological Elements (2021, neutral): “In biological networks, normalization and synaptic changes co-occur with replay (Chauvette, Seigneur, & Timofeev, 2012; Tononi & Cirelli, 2014).”
Alleviating catastrophic forgetting using context-dependent gating and synaptic stabilization (2018, background): “Consistent with this notion, neuroscience studies have proposed that diverse mechanisms operating at the systems (10, 11), morphological (2, 4), and transcriptional (12) levels all act to stabilize learned information, raising the question as to whether several complementary algorithms are required ”
Memory consolidation. (2015, background): “The other suggested mechanism for consolidation during sleep is “downscaling”— “with sleep homeostatically but nonspecifically regulating synaptic weights to improve the signal-to-noise ratio of memory traces” (Tononi and Cirelli 2006, 2014).”
Plasticity during Sleep Is Linked to Specific Regulation of Cortical Circuit Activity (2017, background): “On the other hand, sleep was shown to support the global homeostatic regulation of synaptic turnover in the brain (Tononi and Cirelli, 2014).”
Cellular and Systems Consolidation of Declarative Memory (2017, background): “" Scaling " refers to " …sleep homeostatically but nonspecifically regulating synaptic weights to improve the signal-to-noise ratio of memory traces " (Tononi and Cirelli 2006; Tononi and Cirelli 2014).”
Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning (2015, background): “A recent modification of the sleep homeostasis framework acknowledges that the “downsize all” framework is oversimplified and entertains, although does not demonstrate, the possibility that previously used and unused synapses are differentially affected during sleep (Tononi and Cirelli, 2014).”
Sleep for cognitive enhancement (2014, background): “…hypothesis, on the other hand, assumes that synaptic connections become widely depotentiated during sleep, whereby selected memory representations are depotentiated less or are spared from depotentiation so that these memories come out relatively stronger (Tononi and Cirelli, 2006, 2014).”
The two‐process model of sleep regulation: a reappraisal (2016, background): “Tononi and Cirelli have proposed the synaptic homeostasis hypothesis of sleep regulation (Tononi and Cirelli, 2006, 2014).”