The relationships between memory systems and sleep stages

Rauchs, Géraldine; Desgranges, Béatrice; Foret, Jean; Eustache, Francis

doi:10.1111/j.1365-2869.2005.00450.x

Cited by 227 publications

(150 citation statements)

References 115 publications

(161 reference statements)

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“…A significant group by performance interaction was observed in the right caudate nucleus (8,22,4; Z ϭ 3.45; p svc(10 mm) Ͻ0.05), in which blood-oxygen-level-dependent response was positively coupled with retrieval performance in RS (r ϭ 0.41) but negatively coupled in TSD (r ϭ Ϫ0.80) participants (Fig. 3b).…”

Section: Resultsmentioning

confidence: 90%

“…T he hypothesis that sleep represents a crucial, albeit not always indispensable, neurophysiological state that actively promotes learning-dependent brain plasticity (1)(2)(3)(4)(5) has become a main topic of interest in neuroscience. In this view, an active processing of freshly acquired memories may occur in the sleeping brain, supporting the gradual consolidation process by which labile recent memories are restructured and incorporated into stable memories for the long term (6,7).…”

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confidence: 99%

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Sleep after spatial learning promotes covert reorganization of brain activity

Orban

Rauchs

Balteau

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

154

130

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Sleep promotes the integration of recently acquired spatial memories into cerebral networks for the long term. In this study, we examined how sleep deprivation hinders this consolidation process. Using functional MRI, we mapped regional cerebral activity during place-finding navigation in a virtual town, immediately after learning and 3 days later, in subjects either allowed regular sleep (RS) or totally sleep-deprived (TSD) on the first posttraining night. At immediate and delayed retrieval, place-finding navigation elicited increased brain activity in an extended hippocamponeocortical network in both RS and TSD subjects. Behavioral performance was equivalent between groups. However, striatal navigation-related activity increased more at delayed retrieval in RS than in TSD subjects. Furthermore, correlations between striatal response and behavioral performance, as well as functional connectivity between the striatum and the hippocampus, were modulated by posttraining sleep. These data suggest that brain activity is restructured during sleep in such a way that navigation in the virtual environment, initially related to a hippocampus-dependent spatial strategy, becomes progressively contingent in part on a response-based strategy mediated by the striatum. Both neural strategies eventually relate to equivalent performance levels, indicating that covert reorganization of brain patterns underlying navigation after sleep is not necessarily accompanied by overt changes in behavior.functional MRI ͉ hippocampus ͉ sleep deprivation ͉ memory consolidation ͉ striatum T he hypothesis that sleep represents a crucial, albeit not always indispensable, neurophysiological state that actively promotes learning-dependent brain plasticity (1-5) has become a main topic of interest in neuroscience. In this view, an active processing of freshly acquired memories may occur in the sleeping brain, supporting the gradual consolidation process by which labile recent memories are restructured and incorporated into stable memories for the long term (6, 7).Memories that can be consciously and symbolically expressed belong to the declarative memory system. At the neuroanatomical level, their encoding and initial maintenance rely upon the integrity of the medial temporal lobe, with the hippocampus at its core (8, 9). Episodic memory for personally experienced events set in a spatiotemporal context is defined as a subclass of declarative memory (10). Animal (11) and human (12) studies suggest that the hippocampus is involved in spatial learning, because encoding is based on a flexible knowledge of relationships between environmental cues. Hippocampus-dependent spatial memory in animals is thus phylogenetically viewed as a homologue of human episodic͞ declarative memory (13,14). However, spatial navigation in a well learned environment may also be mediated by the striatum through the expression of stimulus-response associations (15, 16). Current research further suggests that rodents (17, 18) and humans (19) tend to initially use a hippocampus-de...

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Section: Resultsmentioning

confidence: 90%

mentioning

confidence: 99%

Sleep after spatial learning promotes covert reorganization of brain activity

Orban

Rauchs

Balteau

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

154

130

View full text Add to dashboard Cite

show abstract

“…Carefully designed experiments in humans have already revealed relationships between specific types of memory and different sleep stages (Rauchs et al, 2005). These studies have led to much speculation about the underlying neurophysiological mechanisms.…”

Section: Discussionmentioning

confidence: 99%

“…A recent surge of rigorous studies in humans reaffirms the beneficial effects of sleep on memory. Previous studies had focused on the rapid eye movement (REM) phase; slow-wave sleep (SWS) has been strongly implicated now, as well (for review, see Gais and Born, 2004;Rauchs et al, 2005;Walker and Stickgold, 2006). Sleep spindles, 12-15 Hz oscillations superimposed on slow waves , may promote neural plasticity underlying learning and memory (Steriade and Timofeev, 2003;Rosanova and Ulrich, 2005).…”

Section: Introductionmentioning

confidence: 99%

Elevated Sleep Spindle Density after Learning or after Retrieval in Rats

Eschenko

Mölle²,

Born³

et al. 2006

J. Neurosci.

227

199

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Non-rapid eye movement sleep has been strongly implicated in consolidation of both declarative and procedural memory in humans. Elevated sleep-spindle density in slow-wave sleep after learning has been shown recently in humans. It has been proposed that sleep spindles, 12-15 Hz oscillations superimposed on slow waves (Ͻ1 Hz), in concert with high-frequency hippocampal sharp waves/ripples, promote neural plasticity underlying remote memory formation. The present study reports the first indication of learning-associated increase in spindle density in the rat, providing an animal model to study the role of brain oscillations in memory consolidation during sleep. An odor-reward association task, analogous in many respects to human paired-associate learning, is rapidly learned and leads to robust memory in rats. Rats learned the task over 10 massed trials within a single session, and EEG was monitored for 3 h after learning. Learning-induced increase in spindle density is reliably reproduced in rats in two different learning situations, differing primarily in the behavioral component of the task. This increase in spindle density is also present after reactivation of remote memory and in situations when memory update is required; it is not observed after noncontingent exposure to reward and training context. The latter results substantially extend findings in humans. The magnitude of increase (ϳ25%) and the time window of maximal effect (ϳ1 h after sleep onset) were remarkably similar to human data, making this a valid rodent model to study network interactions through the use of simultaneous unit recordings and local field potentials during postlearning sleep.

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“…As numerous studies indicate a beneficial role of sleep for memory consolidation [2], we investigated the potential link between sleep changes and episodic memory decline in AD. Fourteen patients with mild to moderate AD (MMSE: 24.9 ± 2; age: 76.9 ± 4) and 10 healthy elderly controls paired in age participated in the study.…”

Section: P477mentioning

confidence: 99%

Learning, Memory, Cognition ‐ 2

2006

Journal of Sleep Research

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Growing evidence supports the role of sleep in consolidation of motor learning tasks. However, mechanisms involved in the consolidation process are not well understood. We investigated sleep spindles by comparing sleep following training on a motor sequence task for which significant overnight gains were anticipated, and sleep after training on a control task where no such consolidation was expected. After a screening night in our laboratory, 12 young healthy participants were submitted to two PSG sleep recordings, separated by one week. Before each recording night, subjects were trained in the evening on either a specific motor sequence (SEQ), or on a control task consisting to press the response key according to the displayed number (1-4) appearing in a random order (CTRL). They were retested 12 h later in the morning. The two tasks were counterbalanced across the two nights. Sleep spindles were visually counted (frequency 12-16 Hz, duration > 0.5 s) for the total non-REM sleep at sites FZ, CZ and PZ. Significant gains in the number of sequences (14%, P < 0.0001) were observed at retest for the SEQ task, but only minimal gains for the CTRL task (4%, P = 0.02). Higher amount of sleep spindles was found in the posttraining sleep associated to the SEQ, compared to the CTRL task in all three sites: Fz [t (11) = 4.42, P = 0.001], Cz [t (11) = 4.35, P = 0.001] and Pz [t (11) = 3.91, P = 0.002]. Overnight gains were correlated (r = 0.63, P = 0.03) with sleep spindles increase at site Cz in the last third of post-training non-REM sleep. No difference was observed in PSG sleep parameters between the SEQ and CTRL nights including amount of sleep stages. These results demonstrate that sleep spindles increase in post-training sleep is not simply related to the motor activity generated by the task, but to the consolidation process per se. More interestingly, they suggest that consolidation-based enhancement effects are associated with enhanced sleep spindles during the night, and show that spindles may be an efficient consolidation indicator. We propose that sleep spindles may trigger cellular mechanisms that initiate neuronal plasticity related to motor memory consolidation. P476Neuronal correlates of sleep-dependent declarative memory consolidation Sleep essentially participates in memory consolidation, a process that converts newly acquired memory traces into a long-lasting form. Whereas the enhancing effect of sleep on procedural memory has been well established in humans, evidence for a similar improving influence of sleep on declarative memory mainly derives from spatial learning in rodents. Hippocampal ensembles modified by spatial experience during waking have been shown to be spontaneously reactivated during subsequent sleep. During this offline reprocessing the newly encoded memory traces are supposed to be translated from short-term hippocampal to long-lasting structures within the neocortex. In humans, declarative learning likewise depends on the integrity of the hippocampus. Here, using functional magnetic res...

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The relationships between memory systems and sleep stages

Cited by 227 publications

References 115 publications

Sleep after spatial learning promotes covert reorganization of brain activity

Sleep after spatial learning promotes covert reorganization of brain activity

Elevated Sleep Spindle Density after Learning or after Retrieval in Rats

Learning, Memory, Cognition ‐ 2

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