The effect of sleep‐specific brain activity versus reduced stimulus interference on declarative memory consolidation

Studies suggest that the consolidation of newly acquired memories and underlying long‐term synaptic plasticity might represent a major function of sleep. In a combined repeated‐measures and parallel‐group sleep laboratory study (active waking versus sleep, passive waking versus sleep), we provide evidence that brief periods of daytime sleep (42.1 ± 8.9 min of non‐rapid eye movement sleep) in healthy adolescents (16 years old, all female), compared with equal periods of waking, promote the consolidation of declarative memory (word‐pairs) in participants with high power in the electroencephalographic sleep spindle (sigma) frequency range. This observation supports the notion that sleep‐specific brain activity when reaching a critical dose, beyond a mere reduction of interference, promotes synaptic plasticity in a hippocampal‐neocortical network that underlies the consolidation of declarative memory.     

Enhancement of declarative memory performance following a daytime nap is contingent on strength of initial task acquisition

STUDY OBJECTIVES: In this study we examined the benefit of a daytime nap containing only NREM sleep on the performance of three declarative memory tasks: unrelated paired associates, maze learning, and the Rey-Osterrieth complex figure. Additionally, we explored the impact of factors related to task acquisition on sleep-related memory processing. To this end, we examined whether testing of paired associates during training leads to sleep-related enhancement of memory compared to simply learning the word pairs without test. We also examined whether strength of task acquisition modulates sleep-related processing for each of the three tasks. SUBJECTS AND PROCEDURE: Subjects (11 male, 22 female) arrived at 11:30, were trained on each of the declarative memory tasks at 12:15, and at 13:00 either took a nap or remained awake in the sleep lab. After the nap period, all subjects remained in the lab until retest at 16:00. RESULTS: Compared to subjects who stayed awake during the training-retest interval, subjects who took a NREM nap demonstrated enhanced performance for word pairs that were tested during training, but not for untested word pairs. For each of the three declarative memory tasks, we observed a sleep-dependent performance benefit only for subjects that most strongly acquired the tasks during the training session. CONCLUSIONS: NREM sleep obtained during a daytime nap benefits declarative memory performance, with these benefits being intimately tied to how well subjects acquire the tasks and the way in which the information is acquired.     

Is sleep‐related verbal memory consolidation impaired in sleepwalkers?

In order to evaluate verbal memory consolidation during sleep in subjects experiencing sleepwalking or sleep terror, 19 patients experiencing sleepwalking/sleep terror and 19 controls performed two verbal memory tasks (16‐word list from the Free and Cued Selective Reminding Test, and a 220‐ and 263‐word modified story recall test) in the evening, followed by nocturnal video polysomnography (n = 29) and morning recall (night‐time consolidation after 14 h, n = 38). The following morning, they were given a daytime learning task using the modified story recall test in reverse order, followed by an evening recall test after 9 h of wakefulness (daytime consolidation, n = 38). The patients experiencing sleepwalking/sleep terror exhibited more frequent awakenings during slow‐wave sleep and longer wakefulness after sleep onset than the controls. Despite this reduction in sleep quality among sleepwalking/sleep terror patients, they improved their scores on the verbal tests the morning after sleep compared with the previous evening (+16 ± 33%) equally well as the controls (+2 ± 13%). The performance of both groups worsened during the daytime in the absence of sleep (?16 ± 15% for the sleepwalking/sleep terror group and ?14 ± 11% for the control group). There was no significant correlation between the rate of memory consolidation and any of the sleep measures. Seven patients experiencing sleepwalking also sleep‐talked during slow‐wave sleep, but their sentences were unrelated to the tests or the list of words learned during the evening. In conclusion, the alteration of slow‐wave sleep during sleepwalking/sleep terror does not noticeably impact on sleep‐related verbal memory consolidation.     

The impact of sleep duration and subject intelligence on declarative and motor memory performance: how much is enough?

Recent findings clearly demonstrate that daytime naps impart substantial memory benefits compared with equivalent periods of wakefulness. Using a declarative paired associates task and a procedural motor sequence task, this study examined the effect of two lengthier durations of nocturnal sleep [either a half night (3.5 h) or a full night (7.5 h) of sleep] on over-sleep changes in memory performance. We also assessed whether subject intelligence is associated with heightened task acquisition and, more importantly, whether greater intelligence translates to greater over-sleep declarative and procedural memory enhancement. Across both tasks, we demonstrate that postsleep performance gains are nearly equivalent, regardless of whether subjects obtain a half night or a full night of sleep. Remarkably, the over-sleep memory changes observed on both tasks are very similar to findings from studies examining performance following a daytime nap. Consistent with previous research, we also observed a strong positive correlation between amount of Stage 2 sleep and motor skill performance in the full-night sleep group. This finding contrasts with a highly significant correlation between spectral power in the spindle frequency band (12–15 Hz) and motor skill enhancement only in the half-night group, suggesting that sigma power and amount of Stage 2 sleep are both important for optimal motor memory processing. While subject intelligence correlated positively with acquisition and retest performance on both tasks, it did not correlate with over-sleep changes in performance on either task, suggesting that intelligence may not be a powerful modulator of sleep's effect on memory performance.     

Incorporation of presleep stimuli into dream contents: evidence for a consolidation effect on declarative knowledge during REM sleep?

Presleep stimuli to be retained for further recall is often incorporated into dream contents. To establish whether processing for insertion into dream contents may improve consolidation, we compared the retention rate at delayed recall of contents resulting from incorporation of presleep sentence-stimuli with those of other contents of the same dream experiences. We hypothesized that association with a cognitive task of recall facilitates access to recently acquired items of declarative knowledge such as presleep stimuli, and triggers the deep elaboration of their semantic features, which involves rehearsal. Twelve subjects were given a task of delayed recall for three nonsense sentences delivered once a time before each of the sleep (re-)onsets over an experimental night. After each awakening in rapid eye movement sleep, subjects were asked to report dream experience and recall the sentence to be retained. In the morning, after spontaneous awakening, subjects were unexpectedly requested to again report their dream experiences and to recall the stimuli. Two pairs of judges independently identified possible incorporations of the stimuli, and parsed dream reports into propositional content units. The proportion of night reports with at least one incorporation of the stimulus delivered (i.e. valid incorporations) was higher than that of reports with contents similar to a stimulus(-i) not yet delivered (forward pseudo-incorporations) or delivered prior to an earlier sleep period (backward pseudo-incorporations). The proportion of content units common to night and morning reports (considered to be better consolidated) was significantly higher for incorporated contents than for other contents, including pseudo-incorporated contents. Instead, the retention at morning recall of words of sentence-stimuli corresponding to incorporated contents was not significantly higher than that of other words. The better retention of incorporated contents provides a partial confirmation (that is, limited to the output of the processing) that a generation effect, which benefits retention of actively processed information, is operative during sleep as well as in waking.     

Sleep enhances memory consolidation in children

Sleep is an active state that plays an important role in the consolidation of memory. It has been found to enhance explicit memories in both adults and children. However, in contrast to adults, children do not always show a sleep‐related improvement in implicit learning. The majority of research on sleep‐dependent memory consolidation focuses on adults; hence, the current study examined sleep‐related effects on two tasks in children. Thirty‐three typically developing children aged 6–12 years took part in the study. Actigraphy was used to monitor sleep. Sleep‐dependent memory consolidation was assessed using a novel non‐word learning task and the Tower of Hanoi cognitive puzzle, which involves discovering an underlying rule to aid completion. Children were trained on the two tasks and retested following approximately equal retention intervals of both wake and sleep. After sleep, children showed significant improvements in performance of 14% on the non‐word learning task and 25% on the Tower of Hanoi task, but no significant change in score following the wake retention interval. Improved performance on the Tower of Hanoi may have been due to children consolidating explicit aspects of the task, for example rule‐learning or memory of previous sequences; thus, we propose that sleep is necessary for consolidation of explicit memory in children. Sleep quality and duration were not related to children's task performance. If such experimental sleep‐related learning enhancement is generalizable to everyday life, then it is clear that sleep plays a vital role in children's educational attainment.     

Instrumental conditioning of human sensorimotor rhythm (12-15 Hz) and its impact on sleep as well as declarative learning

STUDY OBJECTIVES: To test whether instrumental conditioning of sensorimotor rhythm (SMR; 12-15 Hz) has an impact on sleep parameters as well as declarative memory performance in humans. DESIGN: Randomized, parallel group design SETTING: 10 instrumental conditioning sessions, pre- and posttreatment investigation including sleep evaluations PARTICIPANTS: 27 healthy subjects (13 male) Interventions: SMR-conditioning (experimental group) or randomized-frequency conditioning (control group); declarative memory task before and after a 90-min nap MEASUREMENT AND RESULTS: The experimental group was trained to enhance the amplitude of their SMR-frequency range, whereas the control group participated in a randomized-frequency conditioning program (i.e., every session a different 3-Hz frequency bin between 7 and 20 Hz). During pre- and posttreatment the subjects had to attend the sleep laboratory to take a 90-min nap (2:00-3:30 pm) and to perform a declarative memory task before and after sleep. The experimental design was successful in conditioning an increase in relative 12-15 Hz amplitude within 10 sessions (d = 0.7). Increased SMR activity was also expressed during subsequent sleep by eliciting positive changes in different sleep parameters (sleep spindle number [d = 0.6], sleep onset latency [d = 0.7]); additionally, this increased 12-15 Hz amplitude was associated with enhancement in retrieval score computed at immediate cued recall (d = 0.9). CONCLUSION: Relative SMR amplitude increased over 10 instrumental conditioning sessions (in the experimental group only) and this "shaping of one's own brain activity" improved subsequent declarative learning and facilitated the expression of 12-15 Hz spindle oscillations during sleep. Most interestingly, these electrophysiological changes were accompanied by a shortened sleep onset latency.     

An ultra short episode of sleep is sufficient to promote declarative memory performance

Various studies have demonstrated that a night of sleep has a beneficial effect on the retention of previously acquired declarative material. In two experiments, we addressed the question of whether this effect extends to daytime naps. In the first experiment we assessed free recall of a list of 30 words after a 60 min retention interval that was either filled with daytime napping or waking activity. Memory performance was significantly enhanced after napping as opposed to waking but was not correlated with time spent in slow wave sleep or total sleep time within the napping condition. The second experiment was designed to clarify the role of total sleep time and therefore included an additional third group, which was allowed to nap for no longer than 6 min on average. In comparing word recall after conditions of no napping (waking), short napping, and long napping, we found superior recall for both nap conditions in contrast to waking as well as for long naps in contrast to short naps. These results demonstrate that even an ultra short period of sleep is sufficient to enhance memory processing. We suggest that the mere onset of sleep may initiate active processes of consolidation which - once triggered - remain effective even if sleep is terminated shortly thereafter.     

Modulatory effects of emotion and sleep on recollection and familiarity

Growing evidence suggests that declarative memory benefits from the modulatory effects of emotion and sleep. The primary goal of the present study was to determine whether these two factors interact to enhance memory or they act independently of each other. Twenty-eight volunteers participated in the study. Half of them were sleep deprived the night immediately following the exposure to emotional and non-emotional images, whereas the control group slept at home. Their memory for images was tested 1 week later along the valence and arousal dimension of emotion with the remember–know procedure. As emotional events appear to gain preference during encoding, via the modulatory effect of amygdala on prefrontal and medial temporal lobe regions, conscious retrieval of emotional pictures (relative to neutral ones) was expected to be less disrupted by sleep loss. Results indicated that emotional images were more richly experienced in memory than neutral, particularly those with high arousal and positive valence. Even though sleep deprivation resulted in behavioral impairment at retrieval of both emotional and neutral images, results revealed that remember-based recognition accuracy and its underlying process of recollection for emotional images were less influenced by the lack of sleep (the mean difference between control and sleep-deprived subjects was around 40% higher for neutral images than for emotional images). Familiarity, however, was affected by neither emotion nor sleep. Taken together, these results suggest that emotion and sleep influence differentially the subjective experience of remembering and knowing and the underlying processes of recollection and familiarity through brain mechanisms probably involving amygdala- and hippocampo-neocortical networks respectively.     

EEG sigma and slow‐wave activity during NREM sleep correlate with overnight declarative and procedural memory consolidation

Previous studies suggest that sleep‐specific brain activity patterns such as sleep spindles and electroencephalographic slow‐wave activity contribute to the consolidation of novel memories. The generation of both sleep spindles and slow‐wave activity relies on synchronized oscillations in a thalamo‐cortical network that might be implicated in synaptic strengthening (spindles) and downscaling (slow‐wave activity) during sleep. This study further examined the association between electroencephalographic power during non‐rapid eye movement sleep in the spindle (sigma, 12–16 Hz) and slow‐wave frequency range (0.1–3.5 Hz) and overnight memory consolidation in 20 healthy subjects (10 men, 27.1 ± 4.6 years). We found that both electroencephalographic sigma power and slow‐wave activity were positively correlated with the pre–post‐sleep consolidation of declarative (word list) and procedural (mirror‐tracing) memories. These results, although only correlative in nature, are consistent with the view that processes of synaptic strengthening (sleep spindles) and synaptic downscaling (slow‐wave activity) might act in concert to promote synaptic plasticity and the consolidation of both declarative and procedural memories during sleep.     

Memory sources of dreams: the incorporation of autobiographical rather than episodic experiences

The present study aimed to explore autobiographical memories (long‐lasting memories about the self) and episodic memories (memories about discrete episodes or events) within dream content. We adapted earlier episodic memory study paradigms and reinvestigated the incorporation of episodic memory sources into dreams, operationalizing episodic memory as featuring autonoetic consciousness, which is the feeling of truly re‐experiencing or reliving a past event. Participants (n = 32) recorded daily diaries and dream diaries, and reported on wake–dream relations for 2 weeks. Using a new scale, dreams were rated for their episodic richness, which categorized memory sources of dreams as being truly episodic (featuring autonoetic consciousness), autobiographical (containing segregated features of experiences that pertained to waking life) or otherwise. Only one dream (0.5%) was found to contain an episodic memory. However, the majority of dreams (>80%) were found to contain low to moderate incorporations of autobiographical memory features. These findings demonstrate the inactivity of intact episodic memories, and emphasize the activity of autobiographical memory and processing within dreams. Taken together, this suggests that memories for personal experiences are experienced fragmentarily and selectively during dreaming, perhaps in order to assimilate these memories into the autobiographical memory schema.