Sleep and Memory

Abstract

Current behavioural evidence indicates that sleep plays a central role in memory consolidation. Neural events during post‐learning sleep share key features with both early and late stages of memory consolidation. For example, recent studies have shown neuronal changes during post‐learning sleep which reflect early synaptic changes associated with consolidation, including activation of shared intracellular pathways and modifications of synaptic strength. Sleep may also play a role in later stages of consolidation involving propagation of memory traces throughout the brain. However, to date the precise molecular and physiological aspects of sleep required for this process remain unknown. The behavioural effects of sleep may be mediated by the large‐scale, global changes in neuronal activity, synchrony and intracellular communication that accompany sleep, or by synapse‐specific ‘replay’ of activity patterns associated with prior learning.

Key Concepts:

  • Memory consolidation involves plastic changes at the synaptic and brain‐systems levels; these changes occur over timescales of minutes (synaptic consolidation) to days or months (systems consolidation).

  • Cellular changes occurring during early post‐learning sleep suggest that synaptic consolidation may occur preferentially during sleep.

  • Brain‐imaging and gene expression studies have provided limited evidence that sleep may facilitate the gradual redistribution of memory traces throughout the brain.

  • Sleep may facilitate consolidation through large‐scale changes in neural activity, neurotransmission or gene expression associated with REM and NREM sleep.

  • It remains unclear whether sleep‐dependent consolidation is mediated by permissive (global) or instructive (synapse‐specific) mechanisms.

Keywords: sleep; memory; synaptic plasticity; consolidation; long‐term potentiation; long‐term depression

Figure 1.

Synaptic and systems levels of memory consolidation. In the first hours following acquisition, a memory trace is represented in specific neural circuits (in this example, within the hippocampus, highlighted in grey, a). The memory trace is then gradually integrated into a broader neuronal network, including areas not involved in acquisition (in this example, in the neocortex, b), and distributed over time throughout the neocortex (c). Synaptic consolidation (schematised in d) involves activation of NMDA receptor (NMDA‐R)‐ and kinase‐dependent signalling cascades which promote de novo mRNA and protein synthesis. NMDA‐R activation increases calcium (Ca2+) influx, whereas neurotransmitter‐mediated activation of G‐protein coupled receptors stimulate cyclic adenosine monophosphate (cAMP) production. These intracellular signals in turn promote the phosphorylation‐dependent activation of kinases (e.g. PKA, CaMKII and extracellular signal‐regulated kinase (ERK)) (Wang et al., ). These kinases activate cAMP response‐element binding protein (CREB)‐dependent immediate‐early gene (IEG) expression (e.g. zif268, arc/arg3.1 and c‐fos) (Abel and Lattal, ). Products of these transcripts are then translated, together with additional effectors of synaptic potentiation or depression (e.g. glutamate receptor subunits, BDNF and CaMKII). Systems consolidation (schematised in e) requires subsequent activation of CaMKII and synthetic pathways over a period of days to months (Wang et al., ), as memory traces expand through more broadly distributed brain areas.

Figure 2.

Potential roles of sleep in synaptic and systems consolidation. (a) Representative changes in release of acetylcholine (ACh) and noradrenaline (NA) in the cortex (relative to waking) during REM and NREM sleep. Representative EEG traces for the two sleep states show cortical activity similar to that of waking during REM sleep, and high‐amplitude EEG oscillations – including sleep spindles and slow‐wave activity (SWA) – during NREM sleep. (b) Sequence of events showing the transfer over time of the memory trace from hippocampus to neocortical distributed network (see Figure a–c for detailed description). (c–e) Potential cellular mechanisms underlying sleep facilitation of consolidation. Functions demonstrated to occur specifically during sleep are shown in colour; mechanisms that might be activated in sleep, but not yet proven are indicated with a question mark. Mechanisms that have not been studied with respect to sleep are shown in grey. (c) Mechanisms implicated in sleep facilitation of synaptic consolidation are schematised in a neuron within the circuits activated by prior learning (in this example, a neuron in the hippocampus). NMDA‐R activation during sleep may be necessary for some early forms of consolidation (Gais et al., ), whereas PKA, CaMKII and CREB activation and protein synthesis are correlated with the time‐dependent requirement for sleep in other forms of learning (Bourtchouladze et al., ; Horn, ; Saha and Datta, ). Increased expression of the IEGzif268 occurs during REM sleep following some forms of learning (Ribeiro et al., ), while arc/arg3.1 and c‐fos expression are correlated in time with the requirement for sleep following other learning paradigms (Horn, ; Bock et al., ). (d) The same signalling pathways may be activated in additional neural circuits during subsequent systems consolidation (schematised as a neuron in the neocortex which is synaptically connected with the original hippocampal neuron). Changes in neurotransmission or activity during sleep (e.g. synchronised bursting activity produce by SWA and spindles) could promote intercellular communication between these brain areas (represented by red arrows). During subsequent stages of systems consolidation (e), these same sleep‐dependent mechanisms may promote further expansion of memory traces throughout the neocortex (indicated by red arrows).

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Further Reading

Maquet P, Smith C and Stickgold R (eds) (2003) Sleep and Brain Plasticity. Oxford: Oxford University Press.

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Aton, Sara J, Seibt, Julie, and Frank, Marcos G(Aug 2014) Sleep and Memory. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021395.pub2]