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The memory function of sleep

Key Points

  • Sleep promotes the consolidation of declarative as well as procedural and emotional memories in a wide variety of tasks. Sleep improves preferentially the consolidation of memories that were encoded explicitly and are behaviourally relevant to the individual.

  • Consolidation during sleep not only strengthens memory traces quantitatively but can also produce qualitative changes in memory representations. An active process of re-organization enables the formation of new associations and the extraction of generalized features. This can ease novel inferences and insights.

  • Spatio-temporal patterns of neuronal activity during encoding in the awake state become re-activated during subsequent sleep, specifically during slow-wave sleep (SWS) which is a state of minimum cholinergic activity. Such re-activations might promote the gradual redistribution of hippocampus-dependent memories from the hippocampus to neocortical sites for long-term storage (system consolidation) and might also trigger enduring synaptic changes to stabilize memories (synaptic consolidation).

  • Neocortical (<1 Hz) slow oscillations, thalamo-cortical spindles and hippocampal sharp-wave ripples are implicated in memory consolidation during SWS. The depolarizing up-states of the slow oscillations synchronously drive the generation of spindles and ripples accompanying hippocampal memory re-activations, thus providing a temporal frame for a fine-tuned hippocampus-to-neocortex transfer of memories.

  • Neocortical slow oscillations concurrently support a global synaptic downscaling that precludes saturation of synaptic networks and improves the capacity to encode new information.

  • Rapid eye movement (REM) sleep is characterized by a local upregulation of plasticity-related immediate early genes in the presence of high cholinergic activity and reduced electroencephalographic coherence between brain regions. These conditions might effectively support local synaptic consolidation.

  • The temporal sequence of SWS and REM sleep in the normal sleep cycle suggests that these sleep stages have complementary roles in memory consolidation: during SWS, system consolidation promotes the re-activation and redistribution of select memory traces for long-term storage, whereas ensuing REM sleep might act to stabilize the transformed memories by enabling undisturbed synaptic consolidation.

Abstract

Sleep has been identified as a state that optimizes the consolidation of newly acquired information in memory, depending on the specific conditions of learning and the timing of sleep. Consolidation during sleep promotes both quantitative and qualitative changes of memory representations. Through specific patterns of neuromodulatory activity and electric field potential oscillations, slow-wave sleep (SWS) and rapid eye movement (REM) sleep support system consolidation and synaptic consolidation, respectively. During SWS, slow oscillations, spindles and ripples — at minimum cholinergic activity — coordinate the re-activation and redistribution of hippocampus-dependent memories to neocortical sites, whereas during REM sleep, local increases in plasticity-related immediate-early gene activity — at high cholinergic and theta activity — might favour the subsequent synaptic consolidation of memories in the cortex.

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Figure 1: Memory re-activation during slow wave sleep (SWS).
Figure 2: Synaptic homeostasis versus active system consolidation.
Figure 3: Sequential contributions of SWS and REM sleep to memory consolidation in a two-stage memory system.

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Acknowledgements

We apologize to those whose work was not cited because of space constraints. We thank Drs. B. Rasch, L. Marshall, I. Wilhelm, M. Hallschmid, E. Robertson and S. Ribeiro for helpful discussions and comments on earlier drafts. This work was supported by a grant from the Deutsche Forschungsgemeinschaft (SFB 654 'Plasticity and Sleep').

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Glossary

Declarative memory

Memories that are accessible to conscious recollection including memories for facts and episodes, for example, learning vocabulary or remembering events. Declarative memories rely on the hippocampus and associated medial temporal lobe structures, together with neocortical regions for long-term storage.

Procedural memory

Memories for skills that result from repeated practice and are not necessarily available for conscious recollection, for example, riding a bike or playing the piano. Procedural memories rely on the striatum and cerebellum, although recent studies indicate that the hippocampus can also be implicated in procedural learning.

Serial reaction time task

A task in which subjects are required to rapidly respond to different spatial cues by pressing corresponding buttons. This task can be performed implicitly (that is, without knowledge that there is a regularity underlying the sequence of cue positions) or explicitly (by informing the subject about this underlying regularity).

Implicit learning

Learning without being aware that something is being learned.

Explicit learning

Learning while being aware that something is being learned.

Memory systems

Different types of memory, such as declarative and non-declarative memory, are thought to be mediated by distinct neural systems, the organization of which is still a topic of debate.

Transitory sleep

Short transitory periods of sleep in rats that, based on EEG criteria, can neither be classified as REM sleep or SWS.

Immediate early genes

Genes that encode transcription factors that are induced within minutes of raised neuronal activity without requiring a protein signal. Immediate-early gene activation is, therefore, used as an indirect marker of neuronal activation. The immediate early genes Arc and Egr1 (zif268) are associated with synaptic plasticity.

Hebbian plasticity

Refers to the functional changes at synapses that increase the efficacy of synaptic transmission and occurs when the presynaptic neuron repeatedly and persistently stimulates the postsynaptic neuron.

Spike-time dependent plasticity

Refers to the functional changes at synapses that alter the efficacy of synaptic transmission depending on the relative timing of pre- and postsynaptic firing ('spiking'). The synaptic connection is strengthened if the presynaptic neuron fires shortly before the postsynaptic neuron, but is weakened if the sequence of firing is reversed.

Up- and down-states

The slow oscillations that predominate EEG activity during SWS are characterized by alternating states of neuronal silence with an absence of spiking activity and membrane hyperpolarization in all cortical neurons ('down-state') and strongly increased wake-like firing of large neuronal populations and membrane depolarization ('up-state').

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Diekelmann, S., Born, J. The memory function of sleep. Nat Rev Neurosci 11, 114–126 (2010). https://doi.org/10.1038/nrn2762

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