Enhancement of memory by auditory stimulation during postlearning REM sleep in humans

Guerrién, Alain; Dujardin, Kathy; Mandai, Osamu; Sockeel, Pascal; Leconte, Pierre

doi:10.1016/0031-9384(89)90219-9

Cited by 61 publications

(44 citation statements)

References 10 publications

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“…2D). Unexpectedly, however, overnight improvement was not significant (3.2 6 2.0%, P = 0.14), perhaps due to the unfamiliar conditions of the sleep laboratory.This correlation between REM sleep and performance is consistent with past animal and human studies showing that an increased amount of post-training REM sleep occurs when a sufficient level of learning has occurred during prior training (Guerrien et al 1989;Hennevin et al 1995;Smith 1995). Studies in rats have demonstrated specific reactivation patterns of hippocampal neuronal activity during REM sleep in the same temporal sequence as they had during prior wakefulness, suggesting that circuits may be restructured during REM sleep by selectively strengthening some recently acquired memories (Guerrien et al 1989;Hennevin et al 1995;Smith 1995;Poe et al 2000;Louie and Wilson 2001).…”

supporting

confidence: 87%

“…Studies in rats have demonstrated specific reactivation patterns of hippocampal neuronal activity during REM sleep in the same temporal sequence as they had during prior wakefulness, suggesting that circuits may be restructured during REM sleep by selectively strengthening some recently acquired memories (Guerrien et al 1989;Hennevin et al 1995;Smith 1995;Poe et al 2000;Louie and Wilson 2001).…”

mentioning

confidence: 93%

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Sleep enhances category learning

Djonlagic¹,

Rosenfeld²,

Shohamy³

et al. 2009

Learn. Mem.

107

100

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The ability to categorize objects and events in the world around us is a fundamental and critical aspect of human learning. We trained healthy adults on a probabilistic category-learning task in two different training modes. The aim of this study was to see whether either form of probabilistic category learning (feedback or observational) undergoes subsequent enhancement during sleep. Our results suggest that after training, a good night of sleep can lead to improved performance the following day on such tasks.[Supplemental material is available online at http://www.learnmem.org.]From infancy, humans categorize objects and events they encounter. In our daily lives, this category learning enables us to extract rules and patterns from our varied experiences, and to formulate new responses and inferences to familiar objects and events, thereby facilitating decision-making and problem-solving processes .While there is now considerable understanding of the early stages of category learning, relatively little is known about how such learning evolves over time. A growing literature shows that post-training sleep plays an important role in long-term memory consolidation and enhancement (Stickgold 2005;Diekelmann et al. 2009). The most compelling evidence thus far comes from simple perceptual and motor procedural learning, such as fingertapping sequences and visual discrimination tasks (Karni et al. 1994;Gais et al. 2000;Stickgold et al. 2000;Walker et al. 2002;Huber et al. 2004). Much less is understood about the role of sleep in the learning of explicit episodic memory tasks, and even less for more complex memory tasks, such as probabilistic category learning (Smith and Smith 2003;Wagner et al. 2004;Ellenbogen et al. 2007).There are two basic patterns by which categorizations can be learned: We can simply observe stimuli and their outcomes (observational learning), or we can be shown stimuli and then asked to predict outcomes, only then receiving feedback on the accuracy of our response (feedback learning). The Weather Prediction Task (WPT) was initially described by Knowlton et al. (1994) and has been extensively studied as a paradigm for such category learning (Knowlton et al. 1994;Gluck et al. 2002;Meeter et al. 2008).Studies have shown that the WPT activates different memory systems depending on how the task is learned and on the extent of training. Neuroimaging studies have shown that subjects who simply observe stimuli and their outcomes activate learning and memory systems that are supported by the medial temporal lobe (MTL) and prefrontal cortex (observational learning, Fig. 1, top). On the other hand, subjects who must predict outcomes for each stimulus and only then receive feedback on their accuracy (feedback learning, Fig. 1, bottom), initially activate the MTL, but as training continues shift this activation to the striatum, which is known to be involved with habit and skill-learning behaviors (Poldrack et al. 2001).Evidence from studies with patient populations supports this conclusion. Patients in whom b...

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supporting

confidence: 87%

mentioning

confidence: 93%

Sleep enhances category learning

Djonlagic¹,

Rosenfeld²,

Shohamy³

et al. 2009

Learn. Mem.

107

100

View full text Add to dashboard Cite

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“…The relationships of sleep to learning and memory (67, 68), emotional processing (69, 70), and adaptation to stress (71–73) in animals and humans have long been recognized. These have provided further support to the hypothesis that sleep disturbances may contribute to the pathophysiology of PTSD.…”

Section: Sleep-dependent Emotion and Memory Processes: Animal And Hummentioning

confidence: 99%

Sleep Disturbances as the Hallmark of PTSD: Where Are We Now?

Germain

2013

AJP

508

379

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The hypothesis that rapid eye movement (REM) sleep disturbances are the hallmark of posttraumatic stress disorder (PTSD), proposed by Ross and colleagues in 1989, has stimulated a wealth of clinical, preclinical, and animal studies on the role of sleep in the pathophysiology of PTSD. The present review revisits this influential hypothesis in light of clinical and experimental findings that have since accumulated. Polysomnographic studies conducted in adults with PTSD have yielded mixed findings regarding REM sleep disturbances, and they generally suggest modest and nonspecific sleep disruptions. Prospective and treatment studies have provided more robust evidence for the relationship between sleep disturbances and psychiatric outcomes and symptoms. Experimental animal and human studies that have probed the relationship between REM sleep and fear responses, as well as studies focused more broadly on sleep-dependent affective and memory processes, also provide strong support for the hypothesis that sleep plays an important role in PTSD-relevant processes. Overall, the literature suggests that disturbed REM or non-REM sleep can contribute to maladaptive stress and trauma responses and may constitute a modifiable risk factor for poor psychiatric outcomes. Clinicians need to consider that the chronic sleep disruption associated with nightmares may affect the efficacy of first-line PTSD treatments, but targeted sleep treatments may accelerate recovery from PTSD. The field is ripe for prospective and longitudinal studies in high-risk groups to clarify how changes in sleep physiology and neurobiology contribute to increased risk of poor psychiatric outcomes.

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“…REM sleep increases in humans just after intensive learning trials as well (De Koninck et al, 1989; Mandai et al, 1989; Smith and Lapp, 1991; Smith, 1995). Learning can either prolong and/or intensify REM sleep (Smith et al, 1980; Dujardin et al, 1990; Guerrien et al, 1989; Mandai et al, 1989). While it is not the case that smarter animals have more REM sleep (Siegel, 2001), studies of increased REM sleep during times of learning have never been made across species.…”

Section: Spontaneous Physiological Processes During Natural Sleep To mentioning

confidence: 99%

Cognitive neuroscience of sleep

Poe

Walsh

Bjorness³

2010

Progress in Brain Research

146

103

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Mechanism is at the heart of understanding, and this chapter addresses underlying brain mechanisms and pathways of cognition and the impact of sleep on these processes, especially those serving learning and memory. This chapter reviews the current understanding of the relationship between sleep/waking states and cognition from the perspective afforded by basic neurophysiological investigations. The extensive overlap between sleep mechanisms and the neurophysiology of learning and memory processes provide a foundation for theories of a functional link between the sleep and learning systems. Each of the sleep states, with its attendant alterations in neurophysiology, is associated with facilitation of important functional learning and memory processes. For rapid eye movement (REM) sleep, salient features such as PGO waves, theta synchrony, increased acetylcholine, reduced levels of monoamines and, within the neuron, increased transcription of plasticity-related genes, cumulatively allow for freely occurring bidirectional plasticity (long-term potentiation (LTP) and its reversal, depotentiation). Thus, REM sleep provides a novel neural environment in which the synaptic remodeling essential to learning and cognition can occur, at least within the hippocampal complex. During nonREM sleep Stage 2 spindles, the cessation and subsequent strong bursting of noradrenergic cells and coincident reactivation of hippocampal and cortical targets would also increase synaptic plasticity, allowing targeted bidirectional plasticity in the neocortex as well. In delta nonREM sleep, orderly neuronal reactivation events in phase with slow wave delta activity, together with high protein synthesis levels, would facilitate the events that convert early LTP to long lasting LTP. Conversely, delta sleep does not activate immediate early genes associated with de novo LTP. This nonREM sleep-unique genetic environment combined with low acetylcholine levels may serve to reduce the strength of cortical circuits that activate in the ~50% of delta-coincident reactivation events that do not appear in their waking firing sequence. The chapter reviews the results of manipulation studies, typically total sleep or REM sleep deprivation, that serve to underscore the functional significance of the phenomenological associations. Finally, the implications of sleep neurophysiology for learning and memory will be considered from a larger perspective in which the association of specific sleep states with both potentiation or depotentiation is integrated into mechanistic models of cognition.

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Enhancement of memory by auditory stimulation during postlearning REM sleep in humans

Cited by 61 publications

References 10 publications

Sleep enhances category learning

Sleep enhances category learning

Sleep Disturbances as the Hallmark of PTSD: Where Are We Now?

Cognitive neuroscience of sleep

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