Elsevier

Sleep Medicine Reviews

Volume 18, Issue 6, December 2014, Pages 531-541
Sleep Medicine Reviews

Physiological review
The reorganisation of memory during sleep

https://doi.org/10.1016/j.smrv.2014.03.005Get rights and content

Summary

Sleep after learning promotes the quantitative strengthening of new memories. Less is known about the impact of sleep on the qualitative reorganisation of memory, which is the focus of this review. Studies have shown that, in the declarative system, sleep facilitates the abstraction of rules (schema formation), the integration of knowledge into existing schemas (schema integration) and creativity that requires the disbandment of existing patterns (schema disintegration). Schema formation and integration might primarily benefit from slow wave sleep, whereas the disintegration of a schema might be facilitated by rapid eye movement sleep. In the procedural system, sleep fosters the reorganisation of motor memory. The neural mechanisms of these processes remain to be determined. Notably, emotions have been shown to modulate the sleep-related reorganisation of memories. In the final section of this review, we propose that the sleep-related reorganisation of memories might be particularly relevant for mental disorders. Thus, sleep disruptions might contribute to disturbed memory reorganisation and to the development of mental disorders. Therefore, sleep-related interventions might modulate the reorganisation of memories and provide new inroads into treatment.

Introduction

Learning, memory and the neural plasticity underlying these processes are fundamental characteristics of animals and humans that allow for adaptation in changing environments. Research over the past years has shown that sleep after learning facilitates the quantitative strengthening of newly encoded and initially instable memory traces (for review, please refer to [1]). Quantitative strengthening refers to the veridical preservation of stored information and stabilises memories against disruptive interference and decay [2].

More recently, it has been proposed that sleep might also promote the qualitative reorganisation of memories; i.e., the emergence of new memory content that has not been directly learned. This reorganisation of memories during sleep will be the focus of the current review.

A comprehensive model of sleep and memory was recently proposed [3]. This model overarches the entire fate of a novel memory trace from selectivity in initial processing to its subsequent strengthening and further memory evolution; these processes may, at least partially, be interlinked and complementary. The present review elaborates on memory evolution in the form of qualitative changes in memory content rather than the earlier steps of initial processing or strengthening.

Specifically, we review and integrate the current literature related to the two major memory systems, the declarative and the procedural motor systems, from a behavioural perspective. Subsequently, we review the potential neural mechanisms underlying these systems and the modulation of memory reorganisation by emotions. In the final translational section, the potential implications of sleep-related memory reorganisation for the aetiology and treatment of mental disorders are discussed.

Section snippets

Memory reorganisation – the concept

Human memory is an adaptive system. We do not only consolidate experiences as literal records of the past, but we also transform those experiences into new representations that might substantially differ from what was originally encoded [4]. To the best of our knowledge, Sir Frederic Bartlett was the first to systematically show that memory is constructive in nature [5]. In his famous experiments on repeated reproduction, participants were asked to learn and reproduce a North American folk tale

The reorganisation of declarative memory during sleep

Declarative memory refers to the memory of events and facts. Declarative memory is believed to emerge from synaptic long-term plasticity in a hippocampal–neocortical network [9]. Based on our integration of the literature, we propose a multi-process model comprising schema formation, schema integration and schema disintegration (Fig. 1). More specifically, schema formation arises from the extraction of rules. These rules can then be generalised to novel situations. Schema integration pertains

The reorganisation of motor memory during sleep

The motor memory system entails a heterogeneous collection of implicit abilities and skills [58]. In contrast to the declarative system, the motor memory system is largely independent of the hippocampus and is primarily mediated by the basal ganglia, cerebellum and other brain structures [59]. Motor memory is commonly thought to comprise a process of stabilisation [60] and a gain in performance [61]. According to a widely accepted concept, in addition to mere strengthening, motor memory also

Proposed neural mechanisms of memory reorganisation

Three major hypotheses related to the reorganisation of memories on the neural level have been proposed: the complementary learning systems model [89], the synaptic homeostasis hypothesis [90], and the spreading activation theory [50]. In the following, we briefly summarise these hypotheses and then provide some thoughts about their potential integration into the current framework of memory reorganisation.

Modulation of memory reorganisation by emotions

Emotions critically modulate memories. To date, the majority of sleep studies have shown selective strengthening of emotional memories [108], ∗[109], [110] and a bias toward information with a negative valence [111], [112]. For example, Payne and colleagues [113] varied foreground and background objects in emotional pictures and found that the negative emotional objects in the foreground were strengthened relative to the background after sleep but not after an equal period of wakefulness.

Implications for psychiatry and psychotherapy

Mental disorders are among the major personal, societal and economic problems worldwide. In the current context, mental disorders can be conceptualised as both 1) a dysfunction of brain networks that results from an individual neurobiological disposition and 2) functional (health-promoting) and dysfunctional (disorder-promoting) memory traces that are acquired across the lifespan. The basic assumptions here are that sleep critically modifies memory and mental health and that sleep-related

Conclusion and future directions

The current review provides a critical overview of memory reorganisation during sleep. The studies reviewed suggest that sleep modulates the processes responsible for qualitative changes in memory. The most robust evidence is related to declarative memories, and fewer studies have dealt with qualitative changes in motor memory. Most studies have investigated memory changes on the behavioural level in humans. Due to difficulties in measuring the transformation of memory contents in animals, few

Disclosure of interest

Dieter Riemann has received speaker honoraria from AbbVie. Christoph Nissen has received speaker honoraria from Servier. None of the other authors has any conflict of interest to declare.

Practice points

  • Sleep does not only strengthen memories but also reorganises them and results in qualitative changes in memory content on the behavioural level.

  • Sleep-related memory reorganisation has been observed in the declarative and motor memory system.

  • The formation of novel schemas and schema integration

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