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.
Sleep is essential for both cognition and maintenance of healthy brain function. Slow waves in neural activity contribute to memory consolidation, whereas cerebrospinal fluid (CSF) clears metabolic waste products from the brain. Whether these two processes are related is not known. We used accelerated neuroimaging to measure physiological and neural dynamics in the human brain. We discovered a coherent pattern of oscillating electrophysiological, hemodynamic, and CSF dynamics that appears during non–rapid eye movement sleep. Neural slow waves are followed by hemodynamic oscillations, which in turn are coupled to CSF flow. These results demonstrate that the sleeping brain exhibits waves of CSF flow on a macroscopic scale, and these CSF dynamics are interlinked with neural and hemodynamic rhythms.
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.
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.
The brain does not retain all the information it encodes in a day. Much is forgotten, and of those memories retained, their subsequent “evolution” can follow any of a number of pathways. Emerging data makes clear that sleep is a compelling candidate for performing many of these operations. But how does the sleeping brain know which information to preserve and which to forget? What should sleep do with that information it chooses to keep? For information that is retained, sleep can integrate it into existing memory networks, look for common patterns and distill overarching rules, or simply stabilize and strengthen the memory exactly as it was learned. We suggest such “memory triage” lies at the heart of a sleep-dependent memory processing system that selects new information, in a discriminatory manner, and assimilates it into the brain’s vast armamentarium of evolving knowledge, helping guide each organism through its own, unique life.
Performance on a visual discrimination task showed maximal improvement 48-96 hours after initial training, even without intervening practice. When subjects were deprived of sleep for 30 hours after training and then tested after two full nights of recovery sleep, they showed no significant improvement, despite normal levels of alertness. Together with previous findings 11 that subjects show no improvement when retested the same day as training, this demonstrates that sleep within 30 hours of training is absolutely required for improved performance.Skill learning represents one of several classes of procedural memory, and is defined as experience-dependent improvement in performance on perceptual, perceptuomotor or motor tasks 1 . Such learning is one example of memory consolidation 2 . Once a behavioral training session ends, consolidation of learning continues for some time, and manipulations such as drug treatments can either enhance or reverse this consolidation if administered shortly after training 3 .Sleep deprivation hours after training can interfere with consolidation, which suggests involvement of sleep in consolidation 4 , with rapid-eye-movement (REM) sleep 5 and deeper, slow-wave sleep (SWS) 6 subserving distinct functions 7 . In one such procedure 8 , improvement on a visual discrimination task was only observed after several hours 9 ; overnight improvement was blocked by REM deprivation, although REM sleep was concluded to be a permissive rather than obligatory condition for consolidation of this learning 10 . We subsequently showed that improvement on this task only occurs when subjects are tested following a night of sleep, and that this overnight improvement is proportional to the amount of SWS in the first quarter of the night and of REM sleep in the last quarter, with these two sleep parameters explaining 80% of the intersubject variance in improvement 11 . These results suggest that it is the occurrence of sleep, rather than the simple passage of time, that leads to consolidation and improvement on this task. However, these studies were correlative in nature, and did not demonstrate a clear causal link between sleep and improvement. We now report that performance following a single training session improves beyond the first 24 hours, and improves more after a second night of sleep. We show that this improvement is absolutely dependent on the first night of sleep, and that subsequent sleep cannot replace the first night requirement. These findings add to related data from the last three decades, which suggest that sleep after training can be important in consolidation, integration and maintenance of memories 5-7,12 .Subjects (n = 133) were 18 to 25 years old and gave informed consent before participating in the study, which was approved by the Human Studies Committee of the Massachusetts Mental Health Center. Each subject was trained in a single session lasting 60-90 minutes, and was subsequently tested in a second, identical session, 3 hours to 7 days after training. One group (n = 11) was de...
Central aspects of emotional experiences are often well remembered at the expense of background details. Previous studies have focused on memory after brief delays, but little is known about how these components of emotional memories change over time. Here we investigated the evolution of negative scene memories across 30 minutes, 12 daytime hours spent awake, or 12 nighttime hours including sleep. Negative objects were well remembered at the expense of their backgrounds after 30min. Time spent awake led to forgetting of the entire negative scene, with both objects and their backgrounds decaying at similar rates. Sleep, on the other hand, led to a preservation of negative objects, but not their backgrounds, suggesting that the two components undergo differential processing during sleep. Negative scene memories develop differentially across time delays containing sleep and wake, with sleep selectively consolidating those aspects of a memory that are of greatest value to the organism.
Sleep spindles are characteristic electroencephalogram (EEG) signatures of stage 2 non-rapid eye movement sleep. Implicated in sleep regulation and cognitive functioning, spindles may represent heritable biomarkers of neuropsychiatric disease. Here we characterize spindles in 11,630 individuals aged 4 to 97 years, as a prelude to future genetic studies. Spindle properties are highly reliable but exhibit distinct developmental trajectories. Across the night, we observe complex patterns of age- and frequency-dependent dynamics, including signatures of circadian modulation. We identify previously unappreciated correlates of spindle activity, including confounding by body mass index mediated by cardiac interference in the EEG. After taking account of these confounds, genetic factors significantly contribute to spindle and spectral sleep traits. Finally, we consider topographical differences and critical measurement issues. Taken together, our findings will lead to an increased understanding of the genetic architecture of sleep spindles and their relation to behavioural and health outcomes, including neuropsychiatric disorders.
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