The role of sleep in declarative memory consolidation: passive, permissive, active or none?

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Those inclined to relish in scientific controversy will not be disappointed by the literature on the effects of sleep on memory. Opinions abound. Yet refinements in the experimental study of these complex processes of sleep and memory are bringing this fascinating relationship into sharper focus. A longstanding position contends that sleep passively protects memories by temporarily sheltering them from interference, thus providing precious little benefit for memory. But recent evidence is unmasking a more substantial and long-lasting benefit of sleep for declarative memories. Although the precise causal mechanisms within sleep that result in memory consolidation remain elusive, recent evidence leads us to conclude that unique neurobiological processes within sleep actively enhance declarative memories.

Introduction

There is near consensus that periods of sleep, compared with those of wakefulness, actively improve human performance of recently acquired nondeclarative skills [1, 2, 3, 4]. Examples include the learning of motor sequences [5, 6, 7], of visual texture discriminations [8], of the serial-reaction-time task [9, 10, 11, 12, 13], and of auditory discrimination of a synthetic language [14]. In contrast to nondeclarative learning, relatively few studies (e.g. [15•, 16]) clearly demonstrate beneficial effects of sleep on declarative memories. The limited evidence that sleep benefits declarative memory has led some researchers to contend that sleep provides no benefit for such memories [17].

Distinct views are embedded within the complex and controversial literature addressing the role of sleep in declarative memory consolidation: a framework is needed in order to clarify the discussion.

In this review, we divide the debate regarding sleep and declarative memory into four, readily distinguishable, competing hypotheses: first, that sleep offers nothing for memory; second, that sleep temporarily shields memory from the negative effects of interference, a passive and transient benefit; third, that, as in the second hypothesis, sleep leads to passive protection from interference, but that this protection enables consolidation to take place more efficiently than in wakefulness; and fourth, that unique biological properties of sleep lead to the active consolidation of declarative memories. Below, we discuss distinctions between, assumptions within, and strengths and weaknesses of each of these four perspectives (Table 1). (And although there are many uses of the term ‘consolidation’, in this paper we restrict ourselves to the definition provided by Dudai: the “progressive post-acquisition stabilization of memory” [18]).

Section snippets

Sleep contributes nothing to memory

Several lines of reasoning support the view that sleep plays no role in declarative memory consolidation. First, some have pointed out that those with diminished amounts of rapid eye movement sleep (REM; from either REM-suppressing agents, such as certain types of antidepressants, or rare cases of patients sustaining brainstem damage) have continued to lead normal productive lives [17, 19, 20, 21]. Certainly, if sleep were crucial for memory, then those with such impairments in REM sleep would

Sleep transiently shelters memories from interference

According to the second hypothesis, sleep only transiently sustains memories, by protecting them from interference during sleep, but does not consolidate them. Thus, recall is better in the morning immediately after sleep, compared with that after a day awake, but only until exposure to interference in the subsequent day. Because sleep does not consolidate memories, they will be, once again, rendered vulnerable to interference in the waking day to come — as vulnerable as they would be had the

Sleep creates conditions conducive to memory consolidation, but plays no other unique role in the consolidation process

This hypothesis states that sleep can indirectly contribute to consolidation. Similar to hypothesis two, it incorporates the notion that sleep leads to reduced interference. But extending further, the third hypothesis states that reduced interference during sleep facilitates consolidation. Despite this acknowledgement to sleep-dependent consolidation, the essence of this hypothesis is that there is nothing special about the biological state of sleep that enhances consolidation. Rather, sleep

Unique properties of sleep are directly involved in the memory consolidation process

The search for mechanisms underlying sleep-dependent consolidation of declarative memories in humans must rely on examination of specific properties of sleep physiology. By showing that a specific form of memory consolidation crucially depends on a brain property unique to sleep, one can conclusively validate this hypothesis; the boldest of the four.

Recent attempts have been made to address the biological plausibility of sleep physiology leading to memory consolidation. For example, two recent

Conclusions

A review of the literature concerning the putative role of sleep in declarative memory consolidation reveals divisions among researchers. Embedded within the layers of controversy and multitudes of opinion are four distinct positions regarding how sleep affects declarative memory: no benefit, passive protection, permissive consolidation and active consolidation. Experimental evidence argues strongly for the rejection of the first two hypotheses. The latter two hypotheses both state that

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank M Bedny for her thoughtful comments and constructive feedback in preparing this manuscript. This work was supported by grants from the National Institutes of Health: MH48832 and MH65292 (R Stickgold); HL04095 and HL007901 (JM Ellenbogen).

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