Sleep-associated Consolidation Research Articles

Episodic memory and sleep are involved in the maintenance of context-specific lexical information.

Familiar words come with a wealth of associated knowledge about their variety of usage, accumulated over a lifetime. How do we track and adjust this knowledge as new instances of a word are encountered? A recent study (Cognition) found that, for homonyms (e.g., bank), sleep-associated consolidation facilitates the updating of meaning dominance. Here, we tested the generality of this finding by exposing participants to (Experiment 1; N = 125) nonhomonyms (e.g., bathtub) in sentences that biased their meanings toward a specific interpretation (e.g., bathtub-slip vs. bathtub-relax), and (Experiment 2; N = 128) word-class ambiguous words (e.g., loan) in sentences where the words were used in their dispreferred word class (e.g., "He will loan me money"). Both experiments showed that such sentential experience influenced later interpretation and usage of the words more after a night's sleep than a day awake. We interpret these results as evidence for a general role of episodic memory in language comprehension such that new episodic memories are formed every time a sentence is comprehended, and these memories contribute to lexical processing next time the word is encountered, as well as potentially to the fine-tuning of long-term lexical knowledge. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Future-relevant memories are not selectively strengthened during sleep.

Overnight consolidation processes are thought to operate in a selective manner, such that important (i.e. future-relevant) memories are strengthened ahead of irrelevant information. Using an online protocol, we sought to replicate the seminal finding that the memory benefits of sleep are enhanced when people expect a future test [Wilhelm et al., 2011]. Participants memorised verbal paired associates to a criterion of 60 percent (Experiment 1) or 40 percent correct (Experiment 2) before a 12-hour delay containing overnight sleep (sleep group) or daytime wakefulness (wake group). Critically, half of the participants were informed that they would be tested again the following day, whereas the other half were told that they would carry out a different set of tasks. We observed a robust memory benefit of overnight consolidation, with the sleep group outperforming the wake group in both experiments. However, knowledge of an upcoming test had no impact on sleep-associated consolidation in either experiment, suggesting that overnight memory processes were not enhanced for future-relevant information. These findings, together with other failed replication attempts, show that sleep does not provide selective support to memories that are deemed relevant for the future.

Electrophysiological indicators of sleep-associated memory consolidation in 5- to 6-year-old children.

In adults, the synchronized interplay of sleep spindles (SP) and slow oscillations (SO) supports memory consolidation. Given tremendous developmental changes in SP and SO morphology, it remains elusive whether across childhood the same mechanisms as identified in adults are functional. Based on topography and frequency, we characterize slow and fast SPs and their temporal coupling to SOs in 24 pre-school children. Further, we ask whether slow and fast SPs and their modulation during SOs are associated with behavioral indicators of declarative memory consolidation as suggested by the literature on adults. Employing an individually tailored approach, we reliably identify an inherent, development-specific fast centro-parietal SP type, nested in the adult-like slow SP frequency range, along with a dominant slow frontal SP type. Further, we provide evidence that the modulation of fast centro-parietal SPs during SOs is already present in pre-school children. However, the temporal coordination between fast centro-parietal SPs and SOs is weaker and less precise than expected from research on adults. While we do not find evidence for a critical contribution of SP-SO coupling for memory consolidation, crucially, slow frontal and fast centro-parietal SPs are each differentially related to sleep-associated consolidation of items of varying quality. Whereas a higher number of slow frontal SPs is associated with stronger maintenance of medium-quality memories, a higher number of fast centro-parietal SPs is linked to a greater gain of low-quality items. Our results demonstrate two functionally relevant inherent SP types in pre-school children although SP-SO coupling is not yet fully mature.

5.30 THE EFFECT OF CLOSED-LOOPED ACOUSTIC STIMULATION DURING SLEEP IN CHILDREN WITH AND WITHOUT ADHD: ENHANCING THE CONSOLIDATION OF REWARDED MEMORIES BY INCREASING SLOW-WAVE ACTIVITY?

Slow oscillations (SO) during slow-wave sleep foster the consolidation of declarative memory. Children with ADHD display deficits in the sleep-associated consolidation of declarative memory, possibly due to an altered function of SO. A recent study showed that the external induction of SO by transcranial direct current stimulation (tDCS) can normalize the sleep-dependent consolidation of declarative memory in children with ADHD. The present study aimed at enhancing SO activity using closed-looped acoustic stimulation during slow-wave sleep in children with ADHD. This method was proven to enhance endogenous SO activity during sleep and to foster sleep-dependent consolidation of declarative memory.

Consolidation of Reward Memory during Sleep Does Not Require Dopaminergic Activation.

Sleep enhances memories, especially if they are related to future rewards. Although dopamine has been shown to be a key determinant during reward learning, the role of dopaminergic neurotransmission for amplifying reward-related memories during sleep remains unclear. In this study, we scrutinize the idea that dopamine is needed for the preferential consolidation of rewarded information. We impaired dopaminergic neurotransmission, thereby aiming to wipe out preferential sleep-dependent consolidation of high- over low-rewarded memories during sleep. Following a double-blind, balanced, crossover design, 17 young healthy men received the dopamine d2-like receptor blocker sulpiride (800 mg) or placebo, after learning a motivated learning task. The task required participants to memorize 80 highly and 80 lowly rewarded pictures. Half of them were presented for a short (750 msec) and a long (1500 msec) duration, respectively, which permitted dissociation of the effects of reward on sleep-associated consolidation from those of mere encoding depth. Retrieval was tested after a retention interval of approximately 22 hr that included 8 hr of nocturnal sleep. As expected, at retrieval, highly rewarded memories were remembered better than lowly rewarded memories, under placebo. However, there was no evidence for an effect of reducing dopaminergic neurotransmission with sulpiride during sleep on this differential retention of rewarded information. This result indicates that dopaminergic activation likely is not required for the preferential consolidation of reward-associated memory. Rather, it appears that dopaminergic activation only tags such memories at encoding for intensified reprocessing during sleep.

0102 The Relationship Between Overnight Consolidation and Next-Day Learning

Abstract Introduction Contemporary models of sleep-associated consolidation posit that overnight memory processing paves the way for next-day learning in hippocampus. However, the extent to which new hippocampal learning is dependent on overnight consolidation has yet to be investigated. In this study, we compared the impacts of sleep and sleep deprivation on the consolidation and encoding of hippocampus-dependent memories and, importantly, examined whether individual differences in consolidation were associated with individual differences in encoding. Methods Thirty healthy adults (17 females, mean age 20.1±1.65) were trained on a spatial memory task in the evening before a night of sleep or total sleep deprivation (repeated measures). Participants completed a spatial memory test the following morning, and then encoded a novel set of word-image pairs. Two days later (after recovery sleep), memory for the word-image pairs was tested. We predicted that participants’ spatial memory recall would predict performance on the word-image test, suggesting that overnight consolidation lays the groundwork for new encoding in hippocampus. Results Sleep (vs. sleep deprivation) improved spatial memory accuracy the following morning (t(29)=3.93, p<.001, d=0.72) and word-image recall two days later (t(29)=12.19, p<.001, d=2.23), suggesting that sleep facilitated the consolidation and encoding of hippocampus-dependent memories, respectively. However, the benefit of sleep for spatial memory recall was not significantly correlated with the benefit of sleep for word-image encoding (r(28)= 0.01, p=0.971), suggesting that hippocampal encoding was not contingent on foregoing overnight consolidation processes. Conclusion In support of previous findings, overnight sleep improved consolidation and next-day encoding, as compared to an equivalent period of sleep deprivation. However, the present results did not reveal any relationship between an individual’s sleep-associated consolidation and their next-day learning. Support Department of Psychology, University of York scholarship to A.áV.G. Medical Research Council Career Development Award (MR/P020208/1) to S.A.C.

Sleep-dependent consolidation in children with comprehension and vocabulary weaknesses: it'll be alright on the night?

Vocabulary is crucial for an array of life outcomes and is frequently impaired in developmental disorders. Notably, 'poor comprehenders' (children with reading comprehension deficits but intact word reading) often have vocabulary deficits, but underlying mechanisms remain unclear. Prior research suggests intact encoding but difficulties consolidating new word knowledge. We test the hypothesis that poor comprehenders' sleep-associated vocabulary consolidation is compromised by their impoverished lexical-semantic knowledge. Memory for new words was tracked across wake and sleep to assess encoding and consolidation in 8-to-12-year-old good and poor comprehenders. Each child participated in two sets of sessions, one beginning in the morning (AM-encoding) and the other in the evening (PM-encoding). In each case, they were taught 12 words and were trained on a spatial memory task. Memory was assessed immediately, 12- and 24-hr later via stem-completion, picture-naming, and definition tasks to probe different aspects of word knowledge. Long-term retention was assessed 1-2months later. Recall of word-forms improved over sleep and postsleep wake, as measured in both stem-completion and picture-naming tasks. Counter to hypotheses, deficits for poor comprehenders were not observed in consolidation but instead were seen across measures and throughout testing, suggesting a deficit from encoding. Variability in vocabulary knowledge across the whole sample predicted sleep-associated consolidation, but only when words were learned early in the day and not when sleep followed soon after learning. Poor comprehenders showed weaker memory for new words than good comprehenders, but sleep-associated consolidation benefits were comparable between groups. Sleeping soon after learning had long-lasting benefits for memory and may be especially beneficial for children with weaker vocabulary. These results provide new insights into the breadth of poor comprehenders' vocabulary weaknesses, and ways in which learning might be better timed to remediate vocabulary difficulties.

Acoustic closed-loop stimulation during sleep improves consolidation of reward-related memory information in healthy children but not in children with attention-deficit hyperactivity disorder.

Slow oscillations (SO) during slow-wave sleep foster the consolidation of declarative memory. Children with attention-deficit hyperactivity disorder (ADHD) display deficits in the sleep-associated consolidation of declarative memory, possibly due to an altered function of SO. The present study aimed at enhancing SO activity using closed-looped acoustic stimulation during slow-wave sleep in children with ADHD. A total of 29 male children (14 with ADHD; aged 8-12 years) participated in a double-blind, placebo-controlled study trial. Children spent two experimental nights in a sleep lab, one stimulation night and one sham night. A declarative learning task (word-pair learning) with a reward condition was used as a primary outcome. Secondary outcome variables were a procedural memory (serial reaction time) and working memory (WM; n-back) task. Encoding of declarative and procedural memory took place in the evening before sleep. After sleep, the retrieval took place followed by the n-back task. The stimulation successfully induced SO activity during sleep in children with and without ADHD. After stimulation, only healthy children performed better on high-rewarded memory items (primary outcome). In contrast, there were indications that only children with ADHD benefitted from the stimulation with respect to procedural as well as WM performance (secondary outcome). We were able to show that the acoustic closed-loop stimulation can be applied to enhance SO activity in children with and without ADHD. Our data indicate that SO activity during sleep interacts with subsequent memory performance (primary outcome: rewarded declarative memory; secondary outcome: procedural and WM) in children with and without ADHD.

Sleep’s role in the reconsolidation of declarative memories

Sleep is known to support the consolidation of newly encoded and initially labile memories. Once consolidated, remote memories can return to a labile state upon reactivation and need to become reconsolidated in order to persist. Here we asked whether sleep also benefits the reconsolidation of remote memories after their reactivation and how reconsolidation during sleep compares to sleep-dependent consolidation processes. In three groups, participants were trained on a visuo-spatial learning task in the presence of a contextual odor. Participants in the ‘reconsolidation’ group learned the task on day 1. On day 2, they were subjected to a reactivation procedure by presenting the odor cue and a mock recall test in the learning context before a 40-min sleep or wake period. Participants in the ‘remote consolidation’ group followed the same procedure but did not receive reactivation on day 2. Participants in the ‘recent consolidation’ group skipped the procedure on day 1 and learned the task immediately before the sleep or wake period. After the sleep or wake interval, memory stability was tested in all subjects. The results show that this short 40-min sleep period significantly facilitated the reconsolidation of reactivated memories, whereas the consolidation of non-reactivated remote memories was less affected and recently encoded memories did not benefit at all. These findings tentatively suggest that sleep has a beneficial effect on the reconsolidation of remote memories, acting at a faster rate than sleep-associated consolidation.

Markers of automaticity in sleep-associated consolidation of novel words

Two experiments investigated effects of sleep on consolidation and integration of novel form-meaning mappings using size congruity and semantic distance paradigms. Both paradigms have been used in previous studies to measure automatic access to word meanings. When participants compare semantic or physical font size of written word-pairs (e.g. BEE–COW), judgments are typically faster if relative sizes are congruent across both dimensions. Semantic distance effects are also found for wellestablished words, with semantic size judgements faster for pairs that differ substantially on this dimension. English-speaking participants learned novel form-meaning mappings with Mandarin (Experiment 1) or Malay (Experiment 2) words and were tested following overnight sleep or a similar duration awake. Judgements on English words controlled for circadian effects. The sleep group demonstrated selective stronger size congruity and semantic distance effects for novel word-pairs. This benefit occurred in Experiment 1 for semantic size comparisons of novel words, and in Experiment 2 on comparisons where novel pairs had large distances and font differences (for congruity effects) or in congruent trials (for semantic distance effects). Conversely, these effects were equivalent across sleep and wake for English words. Experiment 2 included polysomnography data and revealed that changes in the strength of semantic distance and congruity effects were positively correlated with slow-wave sleep and sleep spindles respectively. These findings support systems consolidation accounts of declarative learning and suggest that sleep plays an active role in integrating new words with existing knowledge, resulting in increased automatic access of the acquired knowledge.

The role of sleep and sleep deprivation in consolidating fear memories

Sleep, in particular REM sleep, has been shown to improve the consolidation of emotional memories. Here, we investigated the role of sleep and sleep deprivation on the consolidation of fear memories and underlying neuronal mechanisms. We employed a Pavlovian fear conditioning paradigm either followed by a night of polysomnographically monitored sleep, or wakefulness in forty healthy participants. Recall of learned fear was better after sleep, as indicated by stronger explicitly perceived anxiety and autonomous nervous responses. These effects were positively correlated with the preceding time spent in REM sleep and paralleled by activation of the basolateral amygdala. These findings suggest REM sleep-associated consolidation of fear memory in the human amygdala. In view of the critical participation of fear learning mechanisms in the etiology of anxiety and post-traumatic stress disorder, deprivation of REM sleep after exposure to distressing events is an interesting target for further investigation.

Consolidation of vocabulary is associated with sleep in children

Although the acquisition of a novel word is apparently rapid, adult research suggests that integration of novel and existing knowledge (measured by engagement in lexical competition) requires sleep-associated consolidation. We present the first investigation of whether a similar time-course dissociation characterizes word learning across development. Consistent with previous research but counter to adults, 7-12-year-olds showed sleep-associated consolidation effects in declarative but not procedural memory. Nevertheless, the relationship between sleep and word learning in children was remarkably similar to the pattern for adults. Following exposure to nonword competitors (e.g. biscal) in the a.m. or p.m., children's ability to recognize and recall the nonwords improved only after sleep (after approximately 12-hrs for the p.m. group and 24-hrs for the a.m. group), with performance stable 1 week later. Novel nonwords only induced lexical competition effects after sleep. These findings suggest that children utilize a dual memory system when acquiring and integrating new vocabulary and highlight sleep as integral to this process. A video abstract of this article can be viewed at http://www.youtube.com/watch?feature=youtube_gdata&v=2UNuKCAakOk&gl=GB.

Reduced sleep-associated consolidation of declarative memory in attention-deficit/hyperactivity disorder

Sleep supports the consolidation of declarative memory. Patients with attention-deficit/hyperactivity disorder (ADHD) are not only characterized by sleep problems but also by declarative memory deficits. Given that the consolidation of declarative memory during sleep is supported by slow oscillations, which are predominantly generated by the prefrontal cortex, and that ADHD patients display low prefrontal brain activity, we assumed that ADHD patients show reduced sleep-associated consolidation of declarative memory. The impact of sleep on the consolidation of declarative memory was examined with a picture recognition task. Twelve ADHD patients (10-16 years) and 12 healthy controls participated in two experimental conditions: in the sleep condition, learning was performed in the evening and picture recognition was tested after nocturnal sleep; in the wake condition, learning was conducted in the morning while retrieval took place after a day of wakefulness. Analyses of recognition accuracy revealed reduced sleep-associated enhancement of recognition accuracy in ADHD. While sleep-associated enhancement of recognition accuracy was correlated with slow oscillation power during non-REM sleep in healthy controls, no such correlations were observed in ADHD. These data indicate a deficit in sleep-associated consolidation of declarative memory in ADHD. Moreover, our results suggest reduced functionality of slow oscillations in sleep-associated consolidation of declarative memory in ADHD.

Sleep Selectively Enhances Memory Expected to Be of Future Relevance

The brain encodes huge amounts of information, but only a small fraction is stored for a longer time. There is now compelling evidence that the long-term storage of memories preferentially occurs during sleep. However, the factors mediating the selectivity of sleep-associated memory consolidation are poorly understood. Here, we show that the mere expectancy that a memory will be used in a future test determines whether or not sleep significantly benefits consolidation of this memory. Human subjects learned declarative memories (word paired associates) before retention periods of sleep or wakefulness. Postlearning sleep compared with wakefulness produced a strong improvement at delayed retrieval only if the subjects had been informed about the retrieval test after the learning period. If they had not been informed, retrieval after retention sleep did not differ from that after the wake retention interval. Retention during the wake intervals was not affected by retrieval expectancy. Retrieval expectancy also enhanced sleep-associated consolidation of visuospatial (two-dimensional object location task) and procedural motor memories (finger sequence tapping). Subjects expecting the retrieval displayed a robust increase in slow oscillation activity and sleep spindle count during postlearning slow-wave sleep (SWS). Sleep-associated consolidation of declarative memory was strongly correlated to slow oscillation activity and spindle count, but only if the subjects expected the retrieval test. In conclusion, our work shows that sleep preferentially benefits consolidation of memories that are relevant for future behavior, presumably through a SWS-dependent reprocessing of these memories.

The whats and whens of sleep-dependent memory consolidation

Sleep benefits memory consolidation. The reviewed studies indicate that this consolidating effect is not revealed under all circumstances but is linked to specific psychological conditions. Specifically, we discuss to what extent memory consolidation during sleep depends on the type of learning materials, type of learning and retrieval test, different features of sleep and the subject population. Post-learning sleep enhances consolidation of declarative, procedural and emotional memories. The enhancement is greater for weakly than strongly encoded associations and more consistent for explicitly than implicitly encoded memories. Memories associated with expected reward gain preferentially access to sleep-dependent consolidation. For declarative memories, sleep benefits are more consistently revealed with recall than recognition procedures at retrieval testing. Slow wave sleep (SWS) particularly enhances declarative memories whereas rapid eye movement (REM) sleep preferentially supports procedural and emotional memory aspects. Declarative memory profits already from rather short sleep periods (1-2 h). Procedural memory profits seem more dose-dependent on the amount of sleep following the day after learning. Children's sleep with high amounts of SWS distinctly enhances declarative memories whereas elderly and psychiatric patients with disturbed sleep show impaired sleep-associated consolidation often of declarative memories. Based on the constellation of psychological conditions identified we hypothesize that access to sleep-dependent consolidation requires memories to be encoded under control of prefrontal-hippocampal circuitry, with the same circuitry controlling subsequent consolidation during sleep.

Hypoglycemia During Sleep Impairs Consolidation of Declarative Memory in Type 1 Diabetic and Healthy Humans

Early nocturnal sleep enhances the consolidation of declarative memories acquired during prior wakefulness. Patients with type 1 diabetes frequently experience hypoglycemic episodes during sleep. We investigated whether short-lasting hypoglycemia during early nocturnal sleep affects the sleep-associated consolidation of declarative memories. Sixteen type 1 diabetic patients and 16 healthy subjects matched for age and BMI were tested. On one condition, a linear fall of plasma glucose to 2.2 mmol/l was induced within 60 min by infusing insulin during early sleep. On the control condition, euglycemia (>3.86 mmol/l) was maintained throughout the night. In the morning, subjects recalled word pairs learned in the preceding evening. To assess mood and attention, a symptom questionnaire, an adjective check list, and the Stroop test were applied. Also, auditory event-related brain potentials were recorded. After euglycemia, subjects recalled 1.5 +/- 0.5 more word pairs than after hypoglycemia (P < 0.01), remembering 2.0 +/- 0.6 more word pairs than at immediate recall before sleep (P = 0.002). Across the hypoglycemic night, no such gain occurred (+0.5 +/- 0.6 words; P = 0.41). Hypoglycemia during sleep also impaired mood (P < 0.05) but did not affect attention. Effects compared well between type 1 diabetic patients and healthy control subjects. Our findings indicate specific sensitivity of declarative memory consolidation during sleep to rather short episodes of mild hypoglycemia. This effect may disable memory processing in type 1 diabetic patients prone to nocturnal hypoglycemic episodes and underlines the importance of considering sleep as a critical period in the treatment of these patients.

Boosting slow oscillations during sleep potentiates memory

There is compelling evidence that sleep contributes to the long-term consolidation of new memories. This function of sleep has been linked to slow (<1 Hz) potential oscillations, which predominantly arise from the prefrontal neocortex and characterize slow wave sleep. However, oscillations in brain potentials are commonly considered to be mere epiphenomena that reflect synchronized activity arising from neuronal networks, which links the membrane and synaptic processes of these neurons in time. Whether brain potentials and their extracellular equivalent have any physiological meaning per se is unclear, but can easily be investigated by inducing the extracellular oscillating potential fields of interest. Here we show that inducing slow oscillation-like potential fields by transcranial application of oscillating potentials (0.75 Hz) during early nocturnal non-rapid-eye-movement sleep, that is, a period of emerging slow wave sleep, enhances the retention of hippocampus-dependent declarative memories in healthy humans. The slowly oscillating potential stimulation induced an immediate increase in slow wave sleep, endogenous cortical slow oscillations and slow spindle activity in the frontal cortex. Brain stimulation with oscillations at 5 Hz--another frequency band that normally predominates during rapid-eye-movement sleep--decreased slow oscillations and left declarative memory unchanged. Our findings indicate that endogenous slow potential oscillations have a causal role in the sleep-associated consolidation of memory, and that this role is enhanced by field effects in cortical extracellular space.

Impaired Sleep-Related Memory Consolidation in Primary Insomnia—A Pilot Study

To compare sleep-related consolidation of procedural memory in patients with primary insomnia and healthy controls. Controlled comparison pilot study. Sleep Laboratory of the Department of Psychiatry and Psychotherapy, University of Freiburg, Germany. Seven patients with primary insomnia and 7 sex-, age-, and IQ-matched healthy controls. Subjects spent 1 night in the sleep laboratory with polysomnographic monitoring. Performance on a mirror tracing task was measured before and after sleep. Polysomnography revealed a trend toward disturbed sleep in the patients, compared with the control group, without reaching significance. Performance in the mirror tracing task before sleep did not differ between the groups. Both groups performed significantly better in the retest condition after sleep. Healthy controls showed an improvement of 42.8% +/- 5.8% in the mirror tracing draw time, whereas patients with insomnia showed an improvement of 20.4% +/- 14.8% (multivariate analyses of variance test session x group interaction: F(3,10) = 10.9, p = .002). These preliminary findings support the view that sleep-associated consolidation of procedural memories may be impaired in patients with primary insomnia.

Effects of Cortisol Suppression on Sleep-Associated Consolidation of Neutral and Emotional Memory

Previous research indicates that hippocampus-dependent declarative memory benefits from early nocturnal sleep, when slow-wave sleep (SWS) prevails and cortisol release is minimal, whereas amygdala-dependent emotional memory is enhanced through late sleep, when rapid eye movement (REM) sleep predominates. The role of the strong cortisol rise accompanying late sleep for emotional memory consolidation has not yet been investigated. Effects of the cortisol synthesis inhibitor metyrapone on sleep-associated consolidation of memory for neutral and emotional texts were investigated in a randomized, double-blind, placebo-controlled study in 14 healthy men. Learning took place immediately before treatment, which was followed by 8 hours of sleep. Retrieval was tested at 11 am the next morning. Metyrapone suppressed cortisol during sleep and blocked particularly the late-night rise in cortisol. It reduced SWS and concomitantly impaired the consolidation of neutral texts. Emotional texts were spared from this impairing influence, however. Metyrapone even amplified emotional enhancement in text recall indicating amygdala-dependent memory. Cortisol blockade during sleep impairs hippocampus-dependent declarative memory formation but enhances amygdala-dependent emotional memory formation. The natural cortisol rise during late sleep may thus protect from overshooting emotional memory formation, a mechanism possibly pertinent to the development of posttraumatic stress disorder.