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Diekelmann and Born offer an elegant and convincing overview of evidence supporting sleep’s role in the consolidation of newly acquired memories1. Increasing awareness of memory stages that move beyond classical consolidation (e.g.2), a process concerned with the veridical preservation of stored information, highlights the internal contradictions of a system which, on the one hand, may seek to preserve memories in their original form, while on the other, allows them to evolve into more generalized representations of the world in which we live.
While there is considerable evidence that slow-wave sleep (SWS) facilitates the consolidation and thus preservation of newly formed episodic memories3, emerging evidence suggests that sleep, and in some cases, rapid eye movement (REM) sleep, can play an important role in the extraction of generalized informational schemas from individual experiences4–6. This is an alternative view to that proposed by Diekelmann and Born 1, which examines systems- followed by synaptic-consolidation across the night.
Here, we focus on the integrative stage of memory processing3, 7, beyond consolidation. Without implying that any of these stages is uniquely linked to a specific brain state, we review evidence for the proposal that sleep, and REM sleep in particular, supports three specific, but not mutually exclusive, forms of memory integration: 1) the unitization of recently acquired related items, 2) the assimilation of recently encoded items into networks of more remote items, and 3) the abstraction of generalizable rules from existing information stores, a process that leads to the construction of novel, higher-level schemas (Fig 1).
The human brain is remarkably efficient at combining temporally and conceptually distinct memories into “unitized” constructs, especially during sleep. For example, overnight unitization has been seen using a sequential finger-tapping motor-skill task8 in which subjects learn to type numerical sequences, such as 4-1-3-2-1-3-2-1-4. During initial learning, subjects appear to break the sequence into “chunks” (e.g., 413-21-3214), separated by brief pauses. But following a night of sleep, the sequence becomes unitized, and is typed without pauses (i.e., 413213214). Similar unitization has been seen with a transitive inference task9, in which subjects are explicitly taught the relationships between pairs of elements from a 5-element set and then, 12 hr later, are asked to infer the relationships between novel pairs of elements. While all subjects show improved performance, those tested after a night of sleep (as opposed to others trained in the morning and tested that evening) showed a disproportionate 25% advantage in correctly inferring the most distant relationships. Such findings emphasize the ability of sleep to link separate yet related items, producing useful and efficient unitized representations and conceptual schemas.
The human brain also integrates new memories into preexisting networks of related information, or schemas, a process referred to as “assimilation”10. Such assimilation may be optimized during the neurophysiological state of REM sleep. Subjects solve 30% more anagram word puzzles following awakenings from REM sleep than after NREM awakenings11. Similarly, following awakenings from REM sleep, and in contrast to waking and NREM, normally weakly related word pairs produce more semantic priming than do strongly related pairs12. A more specific example of assimilation is the incorporation of newly learned spoken words into preexisting lexical networks, measured by interference created between the new words and well-known, phonemically related words. A night of sleep, but not an equivalent time spent awake, supports such assimilation, integrating newly learned spoken words into pre-existing lexical memory stores13.
Of course, assimilation presupposes the existence of conceptual schemas into which new information can be assimilated. The “abstraction” of such schemas from raw information also can benefit from sleep. Infants exposed to an artificial grammar consisting of non-sense three-syllable “words” display awareness of the abstracted grammatical rules embedded in the stimuli following a nap, but not after an equivalent time period awake14. Similarly, a night of sleep more than doubles the likelihood that subjects will discover a hidden rule for solving a class of mathematical problems15. Such building of rule abstraction may also benefit specifically from REM sleep. Several studies, using the “Wff N Proof” logic task16, a probabilistic learning task17, and the remote associates task18, all implicate REM sleep in the abstraction of patterns and rules from large numbers of stimulus trials.
Beyond preserving or strengthening item memories, sleep appears to facilitate the offline assimilation and generalization of these individual memories in a manner that optimizes their potential usefulness in facing the future. Such integrative models of memory processing have been suggested before in various contexts3, 4, 7, 19.
What we hope to add to this discussion is the functional distinction between these stages. We propose that a first post-encoding stage, which may occur preferentially during SWS, consolidates new episodic item memories, while keeping individual memory representations separate and distinct. In contrast, a second, potentially REM-dependent, stage supports the evolution of these and older memories into rich associative networks, mapping our past and predicting our future, a process requiring a cooperative systems-level transformation of memories. It is this second stage of memory integration that extracts, abstracts, and generalizes recently consolidated item memories in a process that may be linked to the production of dreams. Several aspects of REM physiology support its role in such integrative functions. These include reduced levels of noradrenaline and increased levels of acetylcholine5, minimal hippocampal outflow to the cortex20, cortico-cortical processing in association areas without contribution from dorsolateral prefrontal regions21, and dominance of theta wave carrier oscillations, facilitating associative linking throughout disparate cortical areas22.
While the first-stage of item memory consolidation may occur across a single night, or even a single period of SWS, effective integration of these memories likely takes multiple NREM-REM cycles or multiple nights before optimal representations are complete. Indeed, these memory-processing demands may be one evolutionary factor that has shaped the canonical human NREM-REM cycle, and within it, the shift from SWS to REM dominance across the night. In the end, veridical representations of most episodic item memories likely decay (maybe actively during sleep), leaving only the abstracted, generalized meaning of accumulated experiences. Perhaps it is no surprise that we were never told to “stay awake on a problem”.
This work was supported in part by grants from the National Institutes of Health (AG31164 [M.P.W.]); and the University of California, Berkeley [M.P.W.]).