Review
The contribution of sleep to hippocampus-dependent memory consolidation

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There is now compelling evidence that sleep promotes the long-term consolidation of declarative and procedural memories. Behavioral studies suggest that sleep preferentially consolidates explicit aspects of these memories, which during encoding are possibly associated with activation in prefrontal–hippocampal circuitry. Hippocampus-dependent declarative memory benefits particularly from slow-wave sleep (SWS), whereas rapid-eye-movement (REM) sleep seems to benefit procedural aspects of memory. Consolidation of hippocampus-dependent memories relies on a dialog between the neocortex and hippocampus. Crucial features of this dialog are the neuronal reactivation of new memories in the hippocampus during SWS, which stimulates the redistribution of memory representations to neocortical networks; and the neocortical slow (<1 Hz) oscillation that synchronizes hippocampal-to-neocortical information transfer to activity in other brain structures.

Section snippets

Sleep and consolidation of memory

Sleep in mammals is characterized primarily by behavioral inactivity together with distinct electrophysiological changes in brain activity. Despite some ongoing fundamental controversy about the function of sleep in general and the specific link of sleep to memory function, the last two decades have seen an upsurge in literature supporting the importance of sleep for memory consolidation and brain plasticity 1, 2, 3, 4. Eventually memory consolidation could turn out to be the essential function

Memory systems and explicitness in memory

In recent years there has accumulated strong evidence that sleep supports consolidation of both procedural and declarative memories (reviewed elsewhere, e.g. refs 1, 2, 4, 6, 7, 8, 9; see also Box 1). The consolidating effect of sleep was demonstrated principally in two ways. On the one hand, it was shown that compared with wakefulness, sleep after learning stabilizes newly encoded representations by increasing their resistance to interfering inputs. Thus, sleep after acquisition of declarative

What is the role of specific sleep stages?

Sleep is a complex phenomenon hallmarked by the cyclic occurrence of non-REM (non-rapid eye movement) and REM sleep stages (Box 2). Essentially the significance of sleep states for memory consolidation has been investigated through two general approaches: by investigating (i) the impact of partial or selective post-learning sleep deprivation on delayed retrieval, and (ii) modifications in sleep architecture and sleep stage-associated electrophysiological phenomena immediately following

Reactivation of memories

A leading concept assumes that consolidation during sleep evolves from repeated covert reactivation of the neuronal networks that were previously used to encode the information, although alternative views have been proposed (Box 2). Reactivations are covert in the sense that they are not consciously experienced as during wake retrieval. Reactivation is supposed to support both synaptic consolidation and systems consolidation, the latter involving transfer of memory representations to other

A dialog between neocortex and hippocampus to consolidate memory

Modeling of memory has shown that two complementing stages are required in a memory system to enable it to store information for the long term and to incorporate new material within long-term memory without compromising pre-existing memories 5, 56. It is assumed that, to prevent interference with pre-existing long-term memories during incorporation of new memories, information is encoded temporarily into an intermediate buffer from where in an offline process it is gradually transferred to the

Questions for future research

An intriguing puzzle that remains is to dissociate more clearly those aspects of memory and underlying neuronal systems that do and do not access the sleep-dependent consolidating process. Explicit aspects of a memory seem to be crucial here. It is presently unclear how explicitness influences the consolidation of concurrent implicit aspects. Also the link between awareness and involvement of prefrontal–hippocampal circuitry during encoding and subsequent consolidation needs elaboration.

Acknowledgements

We are grateful to Susanne Diekelmann, Ines Wilhelm and Björn Rasch for critically reading earlier versions of the manuscript. This work was supported by the DFG, SFB 654.

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