Posttraining increases in REM sleep intensity implicate REM sleep in memory processing and provide a biological marker of learning potential

Smith, Carlyle; Nixon, Margaret R.; Nader, Rebecca S.

doi:10.1101/lm.74904

Cited by 146 publications

(108 citation statements)

References 30 publications

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“…For example, experiments using a complex motor task (mirror-tracing) have reported an increase in subsequent REM sleep and a vulnerability to REM deprivation. 9,53 This is in contrast to studies of simple motor tasks (e.g., rotary pursuit, finger tapping), which have shown such tasks to correlate with the amount of stage 2 sleep and to be adversely affected by stage 2 sleep disruptions and not REMD. 2,18,47 Recently, further correlations have been found between the overnight enhancement of simple motor tasks and stage 2 spindle density, as well as an increase of stage 2 spindle density after motor learning.…”

Section: Remd/swsd and Motor Taskscontrasting

confidence: 43%

“…In particular, sleep spindles have been linked to general cognitive and learning abilities, 34,53,65,66 and spindle activity is generally elevated in highly gifted students. 35 These results could indicated that the correlations we found do not reflect a connection between sleep dependent memory enhancement and sleep spindle activity, but rather that the subjects with high spindle activity are generally better learners.…”

Section: Caveatsmentioning

confidence: 99%

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Slow wave sleep and REM sleep awakenings do not affect sleep dependent memory consolidation

Genzel¹,

Dresler²,

Wehrle³

et al. 2007

Pharmacopsychiatry

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study objectives: The effects of REM sleep and slow wave sleep (SWS) deprivation on sleep-dependent motor and declarative memory consolidation. design: Randomized, within-subject, cross-over study setting: Weekly (women: monthly) sleep laboratory visits, with retest 60 hours later Participants: Twelve healthy subjects (6 men) aged between 20 and 30 years interventions: REM sleep deprivation, SWS deprivation, or undisturbed sleep Measurements and results: We deprived subjects once each of REM sleep and SWS, and once let them sleep undisturbed through the night.After each night, we tested declarative and procedural memory consolidation. We tested memory performance by a verbal paired associate task and a sequential finger-tapping task at 21:00 on the study night and again 60 hours later. Although REM sleep and SWS awakenings led to a significant reduction of the respective sleep stages, memory consolidation remained unaffected. We also found a significant correlation between the declarative task and sleep spindles in the undisturbed condition, especially the sleep spindles in the first third of the night. Conclusion: We suggest that word-pair learning relies on stage 2 sleep spindles and requires little SWS. Their sleep dependent consolidation is not affected by SWS deprivation. Simple motor tasks may either be consolidated in stage 2 sleep or depend on only small amounts of REM sleep. Their sleep dependent consolidation is not influenced by REM sleep deprivation.

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Section: Remd/swsd and Motor Taskscontrasting

confidence: 43%

Section: Caveatsmentioning

confidence: 99%

Slow wave sleep and REM sleep awakenings do not affect sleep dependent memory consolidation

Genzel¹,

Dresler²,

Wehrle³

et al. 2007

Pharmacopsychiatry

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“…Perhaps the difficulty in controlling stimuli and environment in humans frequently precludes the ability to detect changes in sleep after learning. Human studies have found that changes in REM sleep after learning are dependent on the type of task (Smith, 2001) and that these changes may also be reflected in REM sleep density or eye movements rather than in the amount of REM sleep (Smith, Nixon, & Nader, 2004). In our study, we controlled exposure to stressful stimuli and included two control groups to define precisely the effects of associative learning on sleep.…”

Section: Discussionmentioning

confidence: 99%

Fear conditioning increases NREM sleep.

Hellman

Abel

2007

Behavioral Neuroscience

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To understand the role that sleep may play in memory storage, the authors investigated how fear conditioning affects sleep-wake states by performing electroencephalographic (EEG) and electromyographic recordings of C57BL/6J mice receiving fear conditioning, exposure to conditioning stimuli, or immediate shock treatment. This experimental design allowed us to examine the effects of associative learning, presentation of the conditioning stimuli, and presentation of the unconditioned stimuli on sleep-wake states. During the 24 hr after training, fear-conditioned mice had approximately 1 hr more of nonrapid-eye-movement (NREM) sleep and less wakefulness than mice receiving exposure to conditioning stimuli or immediate shock treatment. Mice receiving conditioning stimuli had more delta power during NREM sleep, whereas mice receiving fear conditioning had less theta power during rapid-eye-movement sleep. These results demonstrate that a single trial of fear conditioning alters sleep-wake states and EEG oscillations over a 24-hr period, supporting the idea that sleep is modified by experience and that such changes in sleep-wake states and EEG oscillations may play a role in memory consolidation.Keywords fear conditioning; EEG; sleep; mouse; memory Memory consists of several stages including acquisition, consolidation, and retrieval Morris et al., 2003). With a single-trial learning task such as fear conditioning, it is possible to dissect these individual stages. Through the use of pharmacology, lesions, and genetics, researchers have begun to define the molecular and neural systems underlying memory consolidation for fear conditioning (Maren & Quirk, 2004). There have been many reports of sleep enhancing memory consolidation and of sleep deprivation impairing memory consolidation (Graves, Pack, & Abel, 2001;Smith, 1995;Stickgold, Hobson, Fosse, & Fosse, 2001), including recent studies showing that sleep deprivation impairs fear conditioning (Graves, Heller, Pack, & Abel, 2003;McDermott et al., 2003;Ruskin, Liu, Dunn, Bazan, & LaHoste, 2004;Silvestri, 2005). Deprivation of sleep during the first 5 hr after training selectively impairs hippocampus-dependent long-term memory for contextual fear conditioning, without altering memory for cued conditioning (a hippocampus-independent task), suggesting that sleep is important for memory consolidation of tasks mediated by the hippocampal system (Graves, Heller, et al. 2003).Correspondence concerning this article should be addressed to Ted Abel, Department of Biology, 204G Lynch Laboratories, University of Pennsylvania, Philadelphia, PA 19104-6084. abele@sas.upenn NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptTwo stages of sleep potentially contribute to long-term memory consolidation Walker & Stickgold, 2004). One stage is rapid-eye-movement (REM) sleep, when theta oscillations are predominant (Vanderwolf, 1969) and when "replay" of hippocampal neural firing patterns that occur during wakefulness might consolidate memory (Louie & Wilson, 200...

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“…Previous reports about a correlation between baseline amounts of REM sleep and learning potentials, however, have been inconsistent. Some studies have shown a positive association with REM sleep and intelligence (Petre-Quadens and De Lee 1970; Pagel et al 1973); others have shown the opposite (Busby and Pivik 1983), and Smith et al (2004) proposed a model suggesting that the posttraining REM response following task acquisition is partly genetically determined and partly a response to the task itself.…”

mentioning

confidence: 99%

Sleep enhances category learning

Djonlagic¹,

Rosenfeld²,

Shohamy³

et al. 2009

Learn. Mem.

102

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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Posttraining increases in REM sleep intensity implicate REM sleep in memory processing and provide a biological marker of learning potential

Cited by 146 publications

References 30 publications

Slow wave sleep and REM sleep awakenings do not affect sleep dependent memory consolidation

Slow wave sleep and REM sleep awakenings do not affect sleep dependent memory consolidation

Fear conditioning increases NREM sleep.

Sleep enhances category learning

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