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.     

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.     

Sleep restriction can attenuate prioritization benefits on declarative memory consolidation

As chronic sleep restriction is a widespread problem among adolescents, the present study investigated the effects of a 1‐week sleep restriction (SR) versus control period on the consolidation of long‐term memory for prose passages. We also determined whether the benefit of prioritization on memory is modulated by adequate sleep occurring during consolidation. Fifty‐six healthy adolescents (25 male, aged 15–19 years) were instructed to remember a prose passage in which half of the content was highlighted (prioritized), and were told that they would receive an additional bonus for remembering highlighted content. Following an initial free recall test, participants underwent a 7‐night period in which they received either a 5‐h (SR) or 9‐h (control) nightly sleep opportunity, monitored by polysomnography on selected nights. Free recall of the passage was tested at the end of the sleep manipulation period (1 week after encoding), and again 6 weeks after encoding. Recall of highlighted content was superior to that of non‐highlighted content at all three time‐points (initial, 1 week, 6 weeks). This beneficial effect of prioritization on memory was stronger 1 week relative to a few minutes after encoding for the control, but not the SR group. N3 duration was similar in the control and SR groups. Overall, the present study shows that the benefits of prioritization on memory are enhanced over time, requiring time and sleep to unfold fully. Partial sleep deprivation (i.e. 5‐h nocturnal sleep opportunity) may attenuate such benefits, but this may be offset by preservation of N3 sleep duration.     

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.     

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.     

Autobiographical memory impairment in obstructive sleep apnea patients with and without depressive symptoms

Obstructive sleep apnea is associated with memory impairments, and higher rates of depressive symptoms and major depressive disorder compared with community estimates. Autobiographical memory overgenerality, a behaviour characterized by difficulty recalling specific memories from one's own life, is recognized as a marker of depression. Previous studies have demonstrated the predictive quality of specific autobiographical memory recall on the course of depression in patients with obstructive sleep apnea. However, it remains unclear whether impaired autobiographical memory is simply a feature of depression, or whether it is also impaired in patients with obstructive sleep apnea without depression. This study aimed to investigate whether autobiographical memory impairments can be observed in patients with obstructive sleep apnea, independent of the severity of depressive symptoms. Twenty‐one patients with obstructive sleep apnea symptomatic for depressive symptoms (mean age = 43.43 years, SD = 9.97), 17 patients with obstructive sleep apnea asymptomatic for depressive symptoms (mean age = 40.65 years, SD = 9.39), and 20 healthy controls without sleep‐disordered breathing (mean age = 32.80 years, SD = 6.69) completed an Autobiographical Memory Test. Patients with obstructive sleep apnea symptomatic for depressive symptoms recalled significantly fewer specific memories when compared with healthy controls (P = 0.010). No difference in the recall of specific autobiographical memory was observed between symptomatic and asymptomatic patients with obstructive sleep apnea. With regard to valence, symptomatic patients with obstructive sleep apnea recalled significantly fewer negative specific memories when compared with controls (P = 0.010). Impairment in specific autobiographical memory recall can be observed in patients with obstructive sleep apnea, regardless of the severity of depressive symptoms; however, this effect may not be as prominent in younger patients with obstructive sleep apnea.     

Sleep-dependent prospective memory consolidation is impaired with aging

Study ObjectivesExisting literature suggests that sleep-dependent memory consolidation is impaired in older adults but may be preserved for personally relevant information. Prospective memory (PM) involves remembering to execute future intentions in a timely manner and has behavioral importance. As previous work suggests that N3 sleep is important for PM in young adults, we investigated if the role of N3 sleep in PM consolidation would be maintained in older adults.MethodsForty-nine young adults (mean age ± SD: 21.8 ± 1.61 years) and 49 healthy older adults (mean age ± SD: 65.7 ± 6.30 years) were randomized into sleep and wake groups. After a semantic categorization task, participants encoded intentions comprising four related and four unrelated cue-action pairs. They were instructed to remember to perform these actions in response to cue words presented during a second semantic categorization task 12 h later that encompassed either daytime wake (09:00 am–21:00 pm) or overnight sleep with polysomnography (21:00 pm–09:00 am).ResultsThe significant condition × age group × relatedness interaction suggested that the sleep benefit on PM intentions varied according to age group and relatedness (p = 0.01). For related intentions, sleep relative to wake benefitted young adults’ performance (p < 0.001) but not older adults (p = 0.30). For unrelated intentions, sleep did not improve PM for either age group. While post-encoding N3 was significantly associated with related intentions’ execution in young adults (r = 0.43, p = 0.02), this relationship was not found for older adults (r = −0.07, p = 0.763).ConclusionsThe age-related impairment of sleep-dependent memory consolidation extends to PM. Our findings add to an existing body of work suggesting that the link between sleep and memory is functionally weakened in older adulthood.     

Rapid eye movement fragmentation,not slow‐wave sleep,predicts neutral declarative memory consolidation in posttraumatic stress disorder

Individuals diagnosed with posttraumatic stress disorder (PTSD) experience disruption at both slow‐wave sleep (SWS) and rapid‐eye movement (REM) sleep stages and demonstrate marked memory impairment. A small group of studies suggests that, within the disorder, there is a mechanistic relation between these sleep and memory impairments. This study sought to extend that literature by examining whether, in PTSD‐diagnosed individuals, memory‐retention deficits are present after a sleep‐filled (but not after a wake‐filled) delay (i.e., whether memory deficits can be traced to interruptions of sleep‐dependent memory consolidation). Moreover, we investigated whether SWS‐ or REM‐based disturbances, or both, contribute to retention deficits. We recruited participants into three groups: PTSD (n = 21), trauma‐exposed non‐PTSD (TE; n = 19) and healthy control (HC; n = 20). Using a crossover design, we assessed memory recall before and after an 8‐hr period of polysomnography‐monitored sleep and an 8‐hr period of regular waking activity. PTSD‐diagnosed participants retained less information than controls over the sleep‐filled (but not wake‐filled) delay. Furthermore, increased REM fragmentation predicted postsleep memory retention in PTSD‐diagnosed individuals only. No SWS parameter was associated with or predictive of the amount of information retained postsleep. We conclude that specific REM‐related changes in PTSD‐diagnosed individuals affected sleep‐dependent neutral declarative memory consolidation. Generally, these findings extend the literature suggesting that the co‐occurrence of sleep and memory difficulties in PTSD is not accidental, but that these two symptom clusters are meaningfully related. Specifically, the study illustrates that subtle REM‐related disruptions contribute most strongly to memory impairment in PTSD.     

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.     

Impaired memory consolidation during sleep in patients with functional memory disorder

Functional memory disorder (FMD) is characterized by mnestic and attentional deficits without symptoms of mild cognitive impairment or dementia. FMD usually develops in subjects with high psychosocial stress level and is classified to the somatoform disorders. We assessed memory performance (procedural mirror tracing task, declarative visual and verbal memory task) and other cognitive functions before and after one night of sleep in 12 FMD patients (mean age: 51.7 yrs, 7 females) and 12 healthy subjects matched for age, gender and IQ. Memory performance and other neurocognitive tasks did not differ between the groups at baseline. After one night of sleep, FMD patients showed an impairment of declarative memory consolidation compared to healthy subjects (visual task: p = 0.004; verbal task: p = 0.039). Spectral analysis of sleep-EEG indicated an increased cortical excitation in FMD. We hypothesize that a hyperarousal state in FMD might contribute to sleep disturbance implicating negative effects on declarative memory consolidation.     

Does paradoxical sleep deprivation disturb memory trace consolidation?

The effect of water tank PSD on memory in the passive avoidance test as well as on open field behavior was studied in rats. The effect of combining water tank PSD with a period of normal sleep-wakefulness cycle or with PSD by non-emotional awakening was investigated in a special series of experiments. It is concluded that PSD, even by the water tank procedure, does not disturb trace consolidation and formation of long-term memory in the passive avoidance test. However, a change in the correlation of motor-exploratory activity and fear reaction, due to the stressful situation intrinsic in the water tank PSD procedure, does not allow the animals to reach comparatively long temporal criteria in the passive avoidance test.     

Sleep‐deprivation and autobiographical memory: evidence from sleep‐deprived nurses

Negative effects of sleep deprivation on different types of memory are well documented, but the specific effects on autobiographical memory performance are not well studied. In this study, we investigated performance on the autobiographical memory test in a group of sleep‐deprived and well‐rested nurses. One‐hundred participants divided into sleep‐deprived (N = 50, 25 females) and well‐rested (N = 50, 25 females) groups took part in the study. The sleep‐deprived group included night‐shift nurses with 8–12 hr sleep deprivation, while the well‐rested group had the usual night sleep before performance assessment. All participants were matched for gender, age, education and employment status. They completed depression and anxiety inventories, and underwent the autobiographical memory test, which included 18 cue words with positive, negative and neutral valence. The sleep‐deprived group scored significantly higher in depression scores. Analysis of covariance (ANCOVA) results showed that sleep‐deprived participants had a significantly poorer autobiographical memory compared with the well‐rested group. Additionally, specific memories were significantly declined in the sleep‐deprived group. This group remembered significantly less positive and more negative memories. Findings implicate that sleep deprivation has detrimental effects on autobiographical memory specificity and valence, and is associated with mood dysregulation.     

The relationships between memory systems and sleep stages

Sleep function remains elusive despite our rapidly increasing comprehension of the processes generating and maintaining the different sleep stages. Several lines of evidence support the hypothesis that sleep is involved in the off-line reprocessing of recently-acquired memories. In this review, we summarize the main results obtained in the field of sleep and memory consolidation in both animals and humans, and try to connect sleep stages with the different memory systems. To this end, we have collated data obtained using several methodological approaches, including electrophysiological recordings of neuronal ensembles, post-training modifications of sleep architecture, sleep deprivation and functional neuroimaging studies. Broadly speaking, all the various studies emphasize the fact that the four long-term memory systems (procedural memory, perceptual representation system, semantic and episodic memory, according to Tulving's SPI model; Tulving, 1995) benefit either from non-rapid eye movement (NREM) (not just SWS) or rapid eye movement (REM) sleep, or from both sleep stages. Tulving's classification of memory systems appears more pertinent than the declarative/non-declarative dichotomy when it comes to understanding the role of sleep in memory. Indeed, this model allows us to resolve several contradictions, notably the fact that episodic and semantic memory (the two memory systems encompassed in declarative memory) appear to rely on different sleep stages. Likewise, this model provides an explanation for why the acquisition of various types of skills (perceptual-motor, sensory-perceptual and cognitive skills) and priming effects, subserved by different brain structures but all designated by the generic term of implicit or non-declarative memory, may not benefit from the same sleep stages.     

Sleep and memory consolidation: The role of electrophysiological neuroimaging

Summary Memory consolidation involves a complex series of molecular, cellular and network-level processes that take place on time scales from millisecond to months. Evidence from a wide range of experimental observations supports the hypothesis that parts of these processes occur during sleep when the brain is not engaged in processing and encoding incoming information. Indeed, sleep seems to be favorable for brain plasticity. Experience-dependent cortical plasticity observed during sleep has been hypothesized to be part of the global process of memory consolidation. Thus, studying task-dependent, regionally specific reactivation of neuronal assemblies during posttraining sleep may make important contributions to elucidating the role of sleep in memory trace processing. A new methodology – low-resolution brain electromagnetic tomography (LORETA) – offers the possibility of localizing electrical activity produced by cortical neuronal generators under normal (undisturbed) sleeping conditions. The high time resolution of brain electrical data can be exploited to produce neuroimages for specific EEG spectral frequency bands (e.g. delta, theta, or spindle bands). This makes it possible to investigate, dependent on the type of memory, when – in which sleep stages (S2 sleep, SWS, REM sleep) – and where – in which cortical brain regions (primary sensory cortex, higher association cortex) – experience-dependent reactivation occurs.     

Human slow-wave sleep and the cerebral cortex

SUMMARY  Recent hypotheses about the roles of human slow-wave sleep (hSWS—delta EEG activity) are appraised. The possible linkage between hSWS and the functions of the prefrontal cortex (PFC) are explored with respect to normal subjects and to disorders involving PFC deficits.     

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.     

Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep

STUDY OBJECTIVES: To investigate polysomnographic (PSG) sleep and NREM sleep characteristics, including sleep spindles and spectral activity involved in offline consolidation of a motor sequence learning task. DESIGN: Counterbalanced within-subject design. SETTING: Three weekly visits to the sleep laboratory. PARTICIPANTS: Fourteen healthy participants aged between 20 and 30 years (8 women). INTERVENTIONS: Motor sequence learning (MSL) task or motor control (CTRL) task before sleep. MEASUREMENTS AND RESULTS: Subjects were trained on either the MSL or CTRL task in the evening and retested 12 hours later the following morning on the same task after a night of PSG sleep recording. Total number and duration of sleep spindles and spectral power between 0.5 and 24 Hz were quantified during NREM sleep. After performing the MSL task, subjects exhibited a large increase in number and duration of sleep spindles compared to after the CTRL task. Higher sigma (sigma; 13 Hz) and beta (beta; 18-20 Hz) spectral power during the post-training night's sleep were also observed after the MSL task. CONCLUSIONS: These results provide evidence that sleep spindles are involved in the offline consolidation of a new sequence of finger movements known to be sleep dependent. Moreover, they expand on prior findings by showing that changes in NREM sleep following motor learning are specific to consolidation (and learning), and not to nonspecific motor activity. Finally, these data demonstrate, for the first time, higher fast rhythms (beta frequencies) during sleep after motor learning.     

Phase‐amplitude coupling of sleep slow oscillatory and spindle activity correlates with overnight memory consolidation

Initially independent lines of research suggest that sleep‐specific brain activity patterns, observed as electroencephalographic slow oscillatory and sleep spindle activity, promote memory consolidation and underlying synaptic refinements. Here, we further tested the emerging concept that specifically the coordinated interplay of slow oscillations and spindle activity (phase‐amplitude coupling) support memory consolidation. Particularly, we associated indices of the interplay between slow oscillatory (0.16–1.25 Hz) and spindle activity (12–16 Hz) during non‐rapid eye movement sleep (strength [modulation index] and phase degree of coupling) in 20 healthy adults with parameters of overnight declarative (word‐list task) and procedural (mirror‐tracing task) memory consolidation. The pattern of results supports the notion that the interplay between oscillations facilitates memory consolidation. The coincidence of the spindle amplitude maximum with the up‐state of the slow oscillation (phase degree) was significantly associated with declarative memory consolidation (r = .65, p = .013), whereas the overall strength of coupling (modulation index) correlated with procedural memory consolidation (r = .45, p = .04). Future studies are needed to test for potential causal effects of the observed association between neural oscillations during sleep and memory consolidation, and to elucidate ways of modulating these processes, for instance through non‐invasive brain‐stimulation techniques.     

Effects of early and late nocturnal sleep on priming and spatial memory.

A wordstem priming task (nondeclarative memory), and a mental spatial rotation task (declarative memory) were presented to subjects of an experimental "sleep" group (n = 11) and of a "wake" control group (n = 10). Repetition priming effects and recall of spatial memory were tested after 3-hr retention intervals, which followed learning and were placed either in the early or in the late half of the night. Sleep group subjects slept during the retention intervals while subjects of the wake group stayed awake. As expected, early retention sleep was dominated by slow wave sleep (SWS), whereas rapid eye movement (REM) sleep prevailed during late retention sleep. After early retention sleep, recall of spatial memory was superior to that after late retention sleep (p < 0.01), and also to that after retention intervals of wakefulness (p < 0.05). In contrast, priming was more effective after late than early retention sleep (p < 0.05). It appears that early sleep dominated by SWS facilitates consolidation of declarative memory whereas late sleep dominated by REM sleep facilitates consolidation of nondeclarative memory.