A daytime nap containing solely non-REM sleep enhances declarative but not procedural memory

The specialized role that sleep-specific brain physiology plays in memory processing is being rapidly clarified with a greater understanding of the dynamic, complex, and exquisitely orchestrated brain state that emerges during sleep. Behaviorally, the facilitative role of non-REM (NREM) sleep (primarily slow wave sleep) for declarative but not procedural memory performance in humans has been demonstrated in a number of nocturnal sleep studies. However, subjects in these studies were tested after periods of sleep that contained REM sleep in addition to NREM sleep, and comparison wake groups were subjected to mild sleep deprivation. To add some clarity to the findings of these nocturnal studies, we assessed performance on declarative and procedural memory tasks following a daytime training-retest interval containing either a short nap that included NREM without REM sleep, or wakefulness. Consistent with previous findings we show that, after a comparatively brief sleep episode, subjects that take a nap improve more on a declarative memory task than subjects that stay awake, but that improvement on a procedural memory task is the same regardless of whether subjects take a nap or remain awake. Slow wave sleep was the only sleep parameter to correlate positively with declarative memory improvement. These findings are discussed with reference to the general benefits of napping and within the broader context of a growing literature suggesting a role for NREM-specific physiology for the processing of declarative memory.     

Declarative memory consolidation: mechanisms acting during human sleep

Of late, an increasing number of studies have shown a strong relationship between sleep and memory. Here we summarize a series of our own studies in humans supporting a beneficial influence of slow-wave sleep (SWS) on declarative memory formation, and try to identify some mechanisms that might underlie this influence. Specifically, these experiments show that declarative memory benefits mainly from sleep periods dominated by SWS, whereas there is no consistent benefit of this memory from periods rich in rapid eye movement (REM) sleep. A main mechanism of declarative memory formation is believed to be the reactivation of newly acquired memory representations in hippocampal networks that stimulates a transfer and integration of these representations into neocortical neuronal networks. Consistent with this model, spindle activity and slow oscillation-related EEG coherence increase during early sleep after intense declarative learning in humans, signs that together point toward a neocortical reprocessing of the learned material. In addition, sleep seems to provide an optimal milieu for declarative memory reprocessing and consolidation by reducing cholinergic activation and the cortisol feedback to the hippocampus during SWS.     

Sleep in children enhances preferentially emotional declarative but not procedural memories

Although the consolidation of several memory systems is enhanced by sleep in adults, recent studies suggest that sleep supports declarative memory but not procedural memory in children. In the current study, the influence of sleep on emotional declarative memory (recognition task) and procedural memory (mirror tracing task) in 20 healthy children (10-13 years of age) was examined. After sleep, children showed an improvement in declarative memory. Separate analysis with respect to the emotional stimulus content revealed that sleep enhances the recognition of emotional stimuli (p > .001) rather than neutral stimuli (p = .084). In the procedural task, however, no sleep-enhanced memory improvement was observed. The results indicate that sleep in children, comparable to adults, enhances predominantly emotional declarative memory; however, in contrast to adults, it has no effect on the consolidation of procedural memory.     

Reactivation and Consolidation of Memory During Sleep

ABSTRACT— Recent research has shown compellingly that sleep supports the consolidation of declarative memories for events and facts. During consolidation, memories are stabilized against future interference and undergo qualitative changes with regard to their "explicitness" and underlying neural representation. In this article, we argue that declarative memory consolidation during sleep is based on covert reactivations of newly encoded memory traces in the hippocampus. During slow-wave sleep (SWS), the prominent slow oscillations act to synchronize the repeated reactivation of the newly encoded representations in hippocampal networks with the generation of spindle activity in the thalamus, supporting changes in neocortical networks that contribute to long-term memory storage. In this view, sleep plays an active role in the consolidation of memories, in which the neuronal reactivation of newly acquired memories is critical for the redistribution and integration of these memories into the network of pre-existing long-term memories.     

Memory for reward location is enhanced even though acetylcholine efflux within the amygdala is impaired in rats with damage to the diencephalon produced by thiamine deficiency

Sleep facilitates declarative memory processing. However, we know little about whether sleep plays a role in the processing of a fundamental feature of declarative memory, relational memory – the flexible representation of items not directly learned prior to sleep. Thirty-one healthy participants first learned at 12 pm two sets of face–object photograph pairs (direct associative memory), in which the objects in each pair were common to both lists, but paired with two different faces. Participants either were given approximately 90 min to have a NREM-only daytime nap (n = 14) or an equivalent waking period (n = 17). At 4:30 pm, participants who napped demonstrated significantly better retention of direct associative memory, as well as better performance on a surprise task assessing their relational memory, in which participants had to associate the two faces previously paired with the same object during learning. Particularly noteworthy, relational memory performance was correlated with the amount of NREM sleep during the nap, with only slow-wave sleep predicting relational memory performance. Sleep stage data did not correlate with direct associative memory retention. These results suggest an active role for sleep in facilitating multiple processes that are not limited to the mere strengthening of rote memories, but also the binding of items that were not directly learned together, reorganizing them for flexible use at a later time.     

System consolidation of memory during sleep

Over the past two decades, research has accumulated compelling evidence that sleep supports the formation of long-term memory. The standard two-stage memory model that has been originally elaborated for declarative memory assumes that new memories are transiently encoded into a temporary store (represented by the hippocampus in the declarative memory system) before they are gradually transferred into a long-term store (mainly represented by the neocortex), or are forgotten. Based on this model, we propose that sleep, as an offline mode of brain processing, serves the ‘active system consolidation’ of memory, i.e. the process in which newly encoded memory representations become redistributed to other neuron networks serving as long-term store. System consolidation takes place during slow-wave sleep (SWS) rather than rapid eye movement (REM) sleep. The concept of active system consolidation during sleep implicates that (a) memories are reactivated during sleep to be consolidated, (b) the consolidation process during sleep is selective inasmuch as it does not enhance every memory, and (c) memories, when transferred to the long-term store undergo qualitative changes. Experimental evidence for these three central implications is provided: It has been shown that reactivation of memories during SWS plays a causal role for consolidation, that sleep and specifically SWS consolidates preferentially memories with relevance for future plans, and that sleep produces qualitative changes in memory representations such that the extraction of explicit and conscious knowledge from implicitly learned materials is facilitated.     

The contribution of sleep to hippocampus-dependent memory consolidation

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 (<1Hz) oscillation that synchronizes hippocampal-to-neocortical information transfer to activity in other brain structures.     

Immediate as well as delayed post learning sleep but not wakefulness enhances declarative memory consolidation in children

While there is mounting evidence for the importance of sleep for declarative memory consolidation in adults, so far this issue has not been investigated in children despite considerable differences in sleep duration and sleep architecture between children and adults. Here, 27 children (aged between 9 and 12yr) were examined on two conditions: on the Sleep-Wake condition, subjects learned word pairs in the evening and delayed recall was tested first in the next morning after sleep and then again in the following evening after daytime wakefulness. On the Wake-Sleep condition, learning took place in the morning and delayed recall was tested in the evening of the same day and again in the next morning after sleep. In both conditions retention of declarative memory was significantly increased only after an interval of sleep that either followed immediately after learning (as in the Sleep-Wake condition) or that followed after daytime wakefulness (as in the Wake-Sleep condition), respectively. The results support the hypothesis that sleep plays an active role in declarative memory consolidation even if delayed and further show for the first time the importance of sleep for declarative memory consolidation during childhood.     

Relationship between the number of life events and memory capacity in children

Stressful life events can result into declined memory performance at later age. One hypothesis suggests that stress affects the hippocampus, a brain area important for memory functioning. This study explored a potential relationship between the number of negative stressful life events and hippocampus-dependent declarative but not hippocampus-independent procedural memory performance in a community sample of 255 children, aged 6–12 years. The findings revealed that negative stressful life events were negatively related to verbal declarative memory, but not to nonverbal declarative and procedural memory. The memory impairments could not be accounted for by attention and sleep disturbances, and parenting characteristics as perceived by the child did not influence the vulnerability for the stress-related memory impairments. These findings provide further insight into the deleterious effects of negative stressful life events on learning in school-aged children.     

原发性失眠对睡眠依赖性记忆巩固的影响及机制

现代社会的失眠问题异常突出,其对睡眠依赖性记忆巩固（SDC）的影响日益引起重视。目前,原发性失眠（PI）对陈述性及程序性记忆SDC的影响存在分歧。梳理以往研究发现,系统巩固假说和突触稳态假说支持睡眠结构紊乱及脑结构异常可能是PI患者SDC损伤的潜在脑机制。未来研究可考虑同步采集行为、脑电和脑成像数据,深入探究PI影响SDC的脑机制,并验证上述假说;还可尝试通过经颅电/磁刺激和目标记忆重激活等无创性干预措施改善PI患者的SDC效应。     

Neurocognitive dysfunction in children with sleep disorders

It is well known that adults with sleep disturbances frequently exhibit a wide range of neurocognitive decrements, and that these deficits are potentially reversible with effective treatment. However, the consequences of respiratory sleep disturbances on neurocognitive function in children have only recently been evaluated, and suggest a strong causal association between the episodic hypoxia and sleep fragmentation that characterize the disease and the emergence of reduced memory, attention and intelligence as well as a link to problematic and hyperactive behaviours and mood disturbances. This article takes a critical look at the current literature on these issues, reviews the major findings and discusses such findings in conjunction with those derived from pertinent animal models.     

Sleep in children improves memory performance on declarative but not procedural tasks

Sleep supports the consolidation of memory in adults. Childhood is a period hallmarked by huge demands of brain plasticity as well as great amounts of efficient sleep. Whether sleep supports memory consolidation in children as in adults is unclear. We compared effects of nocturnal sleep (versus daytime wakefulness) on consolidation of declarative (word-pair associates, two-dimensional [2D] object location), and procedural memories (finger sequence tapping) in 15 children (6-8 yr) and 15 adults. Beneficial effects of sleep on retention of declarative memories were comparable in children and adults. However, opposite to adults, children showed smaller improvement in finger-tapping skill across retention sleep than wakefulness, indicating that sleep-dependent procedural memory consolidation depends on developmental stage.     

Language in benign childhood epilepsy with centro-temporal spikes abbreviated form: rolandic epilepsy and language

Although Benign Childhood Epilepsy with Centrotemporal Spikes (BECTS) has a good prognosis, a few studies have suggested the existence of language disorders relating to the interictal dysfunction of perisylvian language areas. In this study, we focused on language assessment in 16 children aged 6-15 currently affected by BECTS or in remission. An important proportion of children showed moderate or more severe language impairment. The most affected domains were expressive grammar and literacy skills. We found linguistic deficits during the course of epilepsy but also persistent deficits in children in remission, suggesting possible long-term effects. Our results support the hypothesis that BECTS may be associated with impairment to language and suggest the possibility of a direct link between epileptic activity and language development, and the existence of long-term consequences.     

Atypicalities in sleep and semantic consolidation in autism

Sleep is known to support the neocortical consolidation of declarative memory, including the acquisition of new language. Autism spectrum disorder (ASD) is often characterized by both sleep and language learning difficulties, but few studies have explored a potential connection between the two. Here, 54 children with and without ASD (matched on age, nonverbal ability and vocabulary) were taught nine rare animal names (e.g., pipa). Memory was assessed via definitions, naming and speeded semantic decision tasks immediately after learning (pre‐sleep), the next day (post‐sleep, with a night of polysomnography between pre‐ and post‐sleep tests) and roughly 1 month later (follow‐up). Both groups showed comparable performance at pre‐test and similar levels of overnight change on all tasks; but at follow‐up children with ASD showed significantly greater forgetting of the unique features of the new animals (e.g., pipa is a flat frog). Children with ASD had significantly lower central non‐rapid eye movement (NREM) sigma power. Associations between spindle properties and overnight changes in speeded semantic decisions differed by group. For the TD group, spindle duration predicted overnight changes in responses to novel animals but not familiar animals, reinforcing a role for sleep in the stabilization of new semantic knowledge. For the ASD group, sigma power and spindle duration were associated with improvements in responses to novel and particularly familiar animals, perhaps reflecting more general sleep‐associated improvements in task performance. Plausibly, microstructural sleep atypicalities in children with ASD and differences in how information is prioritized for consolidation may lead to cumulative consolidation difficulties, compromising the quality of newly formed semantic representations in long‐term memory.     

Midlife decline in declarative memory consolidation is correlated with a decline in slow wave sleep

Sleep architecture as well as memory function are strongly age dependent. Slow wave sleep (SWS), in particular, decreases dramatically with increasing age, starting already beyond the age of 30. SWS normally predominates during early nocturnal sleep and is implicated in declarative memory consolidation. However, the consequences of changes in sleep across the life span for sleep-associated memory consolidation have not been evaluated so far. Here, we compared declarative memory consolidation (for word-pair associates) during sleep in young and middle-aged healthy humans. The age groups (18–25 vs. 48–55 yr) did not differ with regard to learning performance before retention periods that covered, respectively, the first and second half of nocturnal sleep. However, after early retention sleep, where the younger subjects showed distinctly more SWS than the middle-aged (62.3 ± 3.7 min vs. 18.4 ± 7.2 min, P < 0.001), retrieval of the word pairs in the middle-aged was clearly worse than in the young (P < 0.001). In contrast, declarative memory retention did not differ between groups after late sleep, where retention was generally worse than after early sleep (P = 0.005). Retention of declarative memories was the same in both age groups when sleep periods containing equal amounts of SWS were compared, i.e., across late sleep in the young and across early sleep in the middle-aged. Our results indicate a decline in sleep-associated declarative memory consolidation that develops already during midlife and is associated with a decrease in early nocturnal SWS.     

Slow wave sleep during a daytime nap is necessary for protection from subsequent interference and long-term retention

While it is now generally accepted that sleep facilitates the processing of newly acquired declarative information, questions still remain as to the type and length of sleep necessary to best benefit declarative memories. A better understanding could lend support in one direction or another as to the much-debated role of sleep, be it passive, permissive, or active, in memory processing. The present study employed a napping paradigm and compared performance on a bimodal paired-associates task of those who obtained a 10-min nap, containing only Stages 1 and 2 sleep, to those whose nap contained slow-wave sleep (SWS) and rapid eye movement (REM) sleep (60-min nap), as well as to subjects who remained awake. Measurements were obtained for baseline performance at training, after a sleep/no sleep interval for short-term retention, after a subsequent stimulus-related interference task, and again after a weeklong retention period. While all groups learned the information similarly, both nap groups performed better than the Wake group when examining short-term retention, approximately 1.5h after training (10-min p=.052, 60-min p=.002). However, performance benefits seen in the 10-min nap group proved to be temporary. Performance after a stimulus-related interference task revealed significantly better memory retention in the 60-min nap group, with interference disrupting the memory trace far less than both the Wake and 10-min nap groups (p<.001, p=.006, respectively). After a weeklong retention period, sleep's benefit to memory persisted in the 60-min nap group, with performance significantly greater than both the Wake and 10-min nap groups (p<.001, p=.004, respectively). It is our conclusion that SWS, obtained only by those in the 60-min nap group, served to actively facilitate the consolidation of learned bimodal paired-associates, supported by theories such as the Standard Theory of Consolidation as well as the Synaptic Homeostasis Hypothesis.     

Memory consolidation during sleep: interactive effects of sleep stages and HPA regulation

Sleep is critically involved in the consolidation of previously acquired memory traces. However, nocturnal sleep is not uniform but is subject to distinct changes in electrophysiological and neuroendocrine activity. Specifically, the first half of the night is dominated by slow wave sleep (SWS), whereas rapid eye movement (REM) sleep prevails in the second half. Concomitantly, hypothalamo-pituitary-adrenal (HPA) activity as indicated by cortisol release is suppressed to a minimum during early sleep, while drastically increasing during late sleep. We have shown that the different sleep stages and the concomitant glucocorticoid release are interactively involved in the consolidation of different types of memories. SWS-rich early sleep has been demonstrated to benefit mainly the consolidation of hippocampus-dependent declarative memories (i.e. facts and episodes). In contrast, REM sleep-rich late sleep was shown to improve in particular emotional memories involving amygdalar function, as well as procedural memories (for skills) not depending on hippocampal or amygdalar function. Enhancing plasma glucocorticoid concentrations during SWS-rich early sleep counteracted hippocampus-dependent declarative memory consolidation, but did not affect hippocampus-independent procedural memory. Preventing the increase in cortisol during late REM sleep-rich sleep by administration of metyrapone impaired hippocampus-dependent declarative memory but enhanced amygdala-dependent emotional aspects of memory. The data underscore the importance of pituitary-adrenal inhibition during early SWS-rich sleep for efficient consolidation of declarative memory. The increase in cortisol release during late REM sleep-rich sleep may counteract an overshooting consolidation of emotional memories.     

Sleep after learning aids memory recall

In recent years, the effect of sleep on memory consolidation has received considerable attention. In humans, these studies concentrated mainly on procedural types of memory, which are considered to be hippocampus-independent. Here, we show that sleep also has a persisting effect on hippocampus-dependent declarative memory. In two experiments, we examined high school students' ability to remember vocabulary. We show that declarative memory is enhanced when sleep follows within a few hours of learning, independent of time of day, and with equal amounts of interference during retention intervals. Sleep deprivation has a detrimental effect on memory, which was significant after a night of recovery sleep. Thus, fatigue accumulating during wake intervals could be ruled out as a confound.     

Memory reactivation and consolidation during sleep

Do our memories remain static during sleep, or do they change? We argue here that memory change is not only a natural result of sleep cognition, but further, that such change constitutes a fundamental characteristic of declarative memories. In general, declarative memories change due to retrieval events at various times after initial learning and due to the formation and elaboration of associations with other memories, including memories formed after the initial learning episode. We propose that declarative memories change both during waking and during sleep, and that such change contributes to enhancing binding of the distinct representational components of some memories, and thus to a gradual process of cross-cortical consolidation. As a result of this special form of consolidation, declarative memories can become more cohesive and also more thoroughly integrated with other stored information. Further benefits of this memory reprocessing can include developing complex networks of interrelated memories, aligning memories with long-term strategies and goals, and generating insights based on novel combinations of memory fragments. A variety of research findings are consistent with the hypothesis that cross-cortical consolidation can progress during sleep, although further support is needed, and we suggest some potentially fruitful research directions. Determining how processing during sleep can facilitate memory storage will be an exciting focus of research in the coming years.The idea that memory storage is supported by events that take place in the brain while a person is sleeping is an idea that is only rarely acknowledged in the neuroscience community. At present, most memory research proceeds with no mention of any influence of sleep on memory. Nonetheless, this hypothesis is gaining empirical support. Research into connections between memory and sleep represents a burgeoning enterprise at the crossroads of traditional memory research and sleep research, an enterprise poised to provide novel insights into the human experience.This article presents some speculations about connections between memory and sleep. We entertain the notion that declarative memories are subject to modification during sleep, and that enduring storage of such memories is systematically influenced by neural events taking place during sleep. Although other types of memory may also be subject to change during sleep (see Maquet et al. 2003), we emphasize declarative memory here.This article also functions as an introduction to the set of papers selected for this special issue of Learning & Memory. These papers together outline portions of the current empirical basis for memory-sleep connections, including research in humans and in nonhuman animals. The findings are tantalizing, and yet there are undoubtedly major gaps in our knowledge about the functions of sleep and about how sleep may be related to memory storage. Future research on this topic is bound to grow in exciting and unpredictable ways. Here, we explore questions about declarative memory and sleep that may serve as a useful guide for such research.     

The relationship between sleep and working memory in children with neurological conditions

The objective of this study is to investigate whether sleep problems might account for the increased working memory deficits observed in school-aged children with neurological conditions. A novel, transdiagnostic approach to the investigation was chosen, and sleep is treated as a process that can potentially account for working memory difficulties across a range of neurological conditions. Prevalence estimates of sleep problems are also examined. Archival data of 237 children aged 6 to 11 years were collected from a Western Australian statewide neuropsychological service for the period 26 July 2011 to 14 January 2014. Measures of parent-reported sleep quality, snoring, and daytime sleepiness were obtained, in addition to objective measures of verbal and spatial working memory, storage capacity, and processing speed. The results of the data analysis reveal that over one third of participants reported having clinically-significant levels of sleep problems and that poor sleep quality is significantly associated with verbal working memory difficulties. This association remains after partialling out the variance contributed to performance by storage capacity and processing speed, suggesting that sleep is impacting upon an executive component of working memory. No other significant associations are observed. The results suggest that poor sleep quality is associated with an executive component of verbal (rather than spatial) working memory in children with neurological conditions. This has implications for the biological mechanisms thought to underlie the relationship between sleep and cognition in children. The results also demonstrate the clinical utility of a transdiagnostic approach when investigating sleep and cognition in children with neurological conditions.