Neuroscience: a memory boost while you sleep.
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Biomedical subjects
Publications and source records attributed to Robert Stickgold.
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Those inclined to relish in scientific controversy will not be disappointed by the literature on the effects of sleep on memory. Opinions abound. Yet refinements in the experimental study of these complex processes of sleep and memory are bringing this fascinating relationship into sharper focus. A longstanding position contends that sleep passively protects memories by temporarily sheltering them from interference, thus providing precious little benefit for memory. But recent evidence is unmasking a more substantial and long-lasting benefit of sleep for declarative memories. Although the precise causal mechanisms within sleep that result in memory consolidation remain elusive, recent evidence leads us to conclude that unique neurobiological processes within sleep actively enhance declarative memories.
Mounting behavioral evidence in humans supports the claim that sleep leads to improvements in recently acquired, nondeclarative memories. Examples include motor-sequence learning; visual-discrimination learning; and perceptual learning of a synthetic language. In contrast, there are limited human data supporting a benefit of sleep for declarative (hippocampus-mediated) memory in humans (for review, see). This is particularly surprising given that animal models (e.g.,) and neuroimaging studies (e.g.,) predict that sleep facilitates hippocampus-based memory consolidation. We hypothesized that we could unmask the benefits of sleep by challenging the declarative memory system with competing information (interference). This is the first study to demonstrate that sleep protects declarative memories from subsequent associative interference, and it has important implications for understanding the neurobiology of memory consolidation.
Although the functions of sleep remain largely unknown, one of the most exciting hypotheses is that sleep contributes importantly to processes of memory and brain plasticity. Over the past decade, a large body of work, spanning most of the neurosciences, has provided a substantive body of evidence supporting this role of sleep in what is becoming known as sleep-dependent memory processing. We review these findings, focusing specifically on the role of sleep in (a) memory encoding, (b) memory consolidation, (c) brain plasticity, and (d) memory reconsolidation; we finish with a summary of the field and its potential future directions.
Sleep disturbance has been implicated in cocaine use; however, the nature of the disturbance and its potential effects on cognition and learning are largely unknown. Twelve chronic cocaine users completed a 23-day inpatient study that included randomized, placebo-controlled, cocaine self-administration sessions. Six subjects received cocaine on each of days 4-6 and placebo on days 18-20, the other six received cocaine on each of days 18-20 and placebo on days 4-6. Sleep was measured by polysomnography, the Nightcap sleep monitor, and self-reported measures. Simple and vigilance reaction times were measured daily; a motor-sequence test of procedural learning was administered four times. Electrophysiological measures of sleep showed a different pattern than self-reported sleep across cocaine administration and abstinence: total sleep time and sleep latency were at their worst by 14-17 days of abstinence while self-reported sleep was at its best. Vigilance correlated positively with electrophysiologically measured sleep and negatively with self-reported measures. Similarly, sleep-dependent procedural learning correlated with total sleep time and was impaired at 17 days abstinence relative to 2- and 3-days abstinence. Slow-wave activity was lowest at days 4-9 of abstinence and highest during use and days 10-17 of abstinence. With sustained abstinence, chronic cocaine users exhibit decreased sleep, impaired vigilance and sleep-dependent procedural learning, and spectral activity suggestive of chronic insomnia. However, they report subjectively improving sleep, indicating they are unaware of this "occult" insomnia. These results suggest the possibility of homeostatic sleep drive dysregulation in chronic cocaine users.
The concept of 'sleeping on a problem' is familiar to most of us. But with myriad stages of sleep, forms of memory and processes of memory encoding and consolidation, sorting out how sleep contributes to memory has been anything but straightforward. Nevertheless, converging evidence, from the molecular to the phenomenological, leaves little doubt that offline memory reprocessing during sleep is an important component of how our memories are formed and ultimately shaped.
Learning of procedural skills develops gradually, with performance improving significantly with practice. But improvement on some tasks, including a visual texture discrimination task, continues in the absence of further practice, expressly during periods of sleep and not across equivalent waking episodes. Here we report that the brain activation revealed significantly different patterns of performance-related functional activity following a night of sleep relative to 1 h post-training without intervening sleep. When task activation patterns after a night of sleep were compared with activation patterns without intervening sleep (1 h post-training), significant regions of increased signal intensity were observed in the primary visual cortex, the occipital temporal junction, the medial temporal lobe and the inferior parietal lobe. In contrast, a region of decreased signal intensity was found in the right temporal pole. Corroborating these condition differences, correlations between behavioural performance and brain activation revealed significantly different patterns of performance-related functional activity following a night of sleep relative to those without intervening sleep. Together, these data provide evidence of overnight bi-directional changes in functional anatomy, differences that may form the neural basis of sleep-dependent learning expressed on this task.
RATIONALE: In cocaine dependent individuals, changes in subjective and objective sleep quality accompany their characteristic binge-abstinence cycle. Preliminary studies suggest that sleep quality may decline with prolonged abstinence. Reported here are results of the most extensive study to date on sleep abnormalities during cocaine binge and confirmed abstinence under controlled conditions. OBJECTIVES: The purpose of the current study was to use an experimental, inpatient model of the cocaine binge and abstinence cycle to examine the course and magnitude of sleep disturbances during cocaine use and abstinence. METHODS: Five inpatient non-treatment seeking cocaine users completed 3 baseline days of drug abstinence followed by 3 days of medically monitored "binge" cocaine use, and then 15 days of drug abstinence. Physiological sleep was recorded with polysomnography and the Nightcap ambulatory monitor, while subjective sleep was assessed by questionnaire. RESULTS: Across 3 days of binge cocaine use and 15 subsequent days of confirmed drug abstinence, mean sleep duration, efficiency and latency changed in the direction of poorer sleep quality. In contrast, subjective reports of sleep quality remained unchanged across the same period. CONCLUSIONS: Physiological sleep quality deteriorated from days when cocaine was used across the first 2 weeks of confirmed drug abstinence. In contrast, subjective reports of sleep quality remained unchanged across the same period. We postulate that this dissociation between objective and subjective sleep quality results from a cocaine-use related disruption of the sleep homeostat. Worsening sleep quality during cocaine abstinence may contribute to the risk of relapse and its treatment may offer novel therapeutic strategies for cocaine dependence.
Although there is no consensus regarding the functions of sleep, one exciting hypothesis is that sleep contributes importantly to learning and memory. Over the last decade, several studies have provided substantive evidence supporting the role of sleep in memory processing. This article focuses on sleep-dependent learning and brain plasticity in humans, specifically in the development of skill performance that is the foundation of many sports actions. The different forms and stages of human memory are discussed, then evidence of sleep-dependent skill learning and associated sleep-dependent brain plasticity is described. In conclusion, a consideration of the fundamental importance of sleep in real-life skill learning is provided.
Memory consolidation and reconsolidation reflect molecular, cellular and systems-level processes that convert labile memory representations into more permanent ones, available for continued reactivation and recall over extended periods of time. Here, we discuss the complexities of consolidation and reconsolidation, and suggest they should be viewed not as all-or-none phenomena, but as a continuing series of biological adjustments that enhance both the efficiency and the utility of stored memories over time and in response to changing needs of the organism. As such, consolidation and reconsolidation might be better thought of as memory organization and reorganization. A rapidly growing body of evidence suggests that many of these processes are optimally engaged during sleep.
Five cocaine-dependent individuals completed a 22-day inpatient study of sleep and cognition. Following 3 days of drug-free baseline, participants underwent 3 days of twice-daily smoked cocaine base self-administration (6 50-mg doses, 14 minutes apart), followed by 15 days of abstinence. Each morning and afternoon, the CDR repeatable, multiple-version, computerized cognitive battery (whose stability following practice has been documented) was administered. During abstinence, performance deteriorated on vigilance tasks (especially reaction time) as well as on immediate and delayed verbal recognition tasks but not on working memory tasks. Declines were most evident in the afternoon. Data suggest that abstinence can unmask cognitive deficits induced by chronic cocaine use and circadian factors may mediate their severity.
The last 10 years have produced a wealth of scientific studies reporting a role for sleep in offline memory processing. Despite this evidence, debate continues to rage over the very existence of sleep-dependent learning and memory processing. We briefly review here the evidence in support of sleep's role in memory consolidation.
We hypothesized that representations of social interactions in REM and non-REM (NREM) dreams would reflect differing regional brain activation patterns associated with the two sleep states, and that levels of aggressive interactions would be higher in REM than in NREM dreams. One hundred REM, 100 NREM, and 100 wake reports were collected in the home from 8 men and 7 women using the Nightcap sleep-wake mentation-monitoring system and scored for number and variety of social interactions. We found that (a) social interactions were more likely to be depicted in dream than in wake reports, (b) aggressive social interactions were more characteristic of REM than NREM or wake reports, and (c) dreamer-initiated friendliness was more characteristic of NREM than REM reports. We conclude that processing of, or simulations about, selected social interactions is preferentially performed while "off-line" during the dream state, with the REM state specializing in simulation of aggressive interactions and the NREM state specializing in simulation of friendly interactions.
BACKGROUND: Schizophrenia patients have difficulty mastering even rote procedural tasks in rehabilitation settings. Although most studies demonstrate intact procedural learning in schizophrenia, recent findings demonstrate that a critical component of procedural learning is dependent on sleep. This study tested the hypothesis that patients with schizophrenia have a deficit in sleep-dependent procedural learning. METHODS: Using a simple, well-characterized test of motor skill learning, the finger tapping motor sequence task (MST), 26 patients with chronic, medicated schizophrenia and 14 demographically matched healthy control subjects were tested on two occasions, 24 hours apart. The main outcome measures were learning of the MST on day 1 (practice-dependent learning) and overnight, sleep-dependent improvement in performance. RESULTS: Although schizophrenia patients and control subjects did not differ in practice-dependent learning, patients failed to show overnight improvement (4% deterioration) and differed significantly from control subjects who showed a significant 11% improvement. CONCLUSIONS: We present here the first demonstration of a failure of sleep-dependent consolidation of procedural learning in chronic, medicated schizophrenia. This deficit occurred in the context of normal practice-dependent learning within a training session. This behavioral dissociation is consistent with evidence that practice- and sleep-dependent motor learning reflect independent processes and suggests that they are differentially affected in schizophrenia.
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While the functions of sleep remain largely unknown, one of the most exciting and contentious hypotheses is that sleep contributes importantly to memory. A large number of studies offer a substantive body of evidence supporting this role of sleep in what is becoming known as sleep-dependent memory processing. This review will provide evidence of sleep-dependent memory consolidation and sleep-dependent brain plasticity and is divided into five sections: (1) an overview of sleep stages, memory categories, and the distinct stages of memory development; (2) a review of the specific relationships between sleep and memory, both in humans and animals; (3) a survey of evidence describing sleep-dependent brain plasticity, including human brain imaging studies as well as animal studies of cellular neurophysiology and molecular biology. We close (4) with a consideration of unanswered questions as well as existing arguments against the role of sleep in learning and memory and (5) a concluding summary.
BACKGROUND: Chronic sleep-onset insomnia is a prevalent health complaint in adults. Although behavioral and pharmacological therapies have been shown to be effective for insomnia, no placebo-controlled trials have evaluated their separate and combined effects for sleep-onset insomnia. The objective of this study was to evaluate the clinical efficacy of behavioral and pharmacological therapy, singly and in combination, for chronic sleep-onset insomnia. METHODS: This was a randomized, placebo-controlled clinical trial that involved 63 young and middle-aged adults with chronic sleep-onset insomnia. Interventions included cognitive behavior therapy (CBT), pharmacotherapy, or combination therapy compared with placebo. The main outcome measures were sleep-onset latency as measured by sleep diaries; secondary measures included sleep diary measures of sleep efficiency and total sleep time, objective measures of sleep variables (Nightcap sleep monitor recorder), and measures of daytime functioning. RESULTS: In most measures, CBT was the most sleep effective intervention; it produced the greatest changes in sleep-onset latency and sleep efficiency, yielded the largest number of normal sleepers after treatment, and maintained therapeutic gains at long-term follow-up. The combined treatment provided no advantage over CBT alone, whereas pharmacotherapy produced only moderate improvements during drug administration and returned measures toward baseline after drug use discontinuation. CONCLUSIONS: These findings suggest that young and middle-age patients with sleep-onset insomnia can derive significantly greater benefit from CBT than pharmacotherapy and that CBT should be considered a first-line intervention for chronic insomnia. Increased recognition of the efficacy of CBT and more widespread recommendations for its use could improve the quality of life of a large numbers of patients with insomnia.
Little is known about the neurophysiological mechanisms underlying the human sleep-wake cycle. Using intracranial electrodes in humans, we investigated changes in topographic distribution of gamma power and local- and long-range gamma EEG coherence in neocortex and hippocampus during different cerebral states. We report significantly greater variability in gamma power across cortical regions during wakefulness than during either slow wave or rapid eye movement (REM) sleep. In addition, local (within cortical regions) and long-range (between cortical regions) gamma coherence was significantly higher during wakefulness than during sleep, and functional gamma-range coupling between the neocortex and hippocampus was seen during wakefulness, but not during sleep. These findings demonstrate a functional link between different stages of conscious awareness and the level of coupling of gamma-band oscillations in the human brain.