Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation

Gais, Steffen; Born, Jan

doi:10.1073/pnas.0305404101

Cited by 356 publications

(245 citation statements)

References 41 publications

(46 reference statements)

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“…Sleep-dependent memory improvement in hippocampalrelated tasks appears to be reliant on SWS (Gais et al 2000). In particular, Gais and Born have demonstrated that low acetylcholine during SWS is important for explicit verbal memory (Gais et al 2004), but not implicit memory. Acetylcholine naturally decreases during sleep, whereas caffeine has been shown to increase hippocampal acetylcholine via antagonism of local adenosine A 1 receptors (Carter et al 1995).…”

Section: Resultsmentioning

confidence: 99%

Comparing the benefits of caffeine, naps and placebo on verbal, motor and perceptual memory

Mednick

Cai

Kanady

et al. 2008

Behavioural Brain Research

108

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Caffeine, the world's most common psychoactive substance, is used by approximately 90% of North Americans everyday. Little is known, however, about its benefits for memory. Napping has been shown to increase alertness and promote learning on some memory tasks. We directly compared caffeine (200mg) with napping (60-90 minutes) and placebo on three distinct memory processes: declarative verbal memory, procedural motor skills, and perceptual learning. In the verbal task, recall and recognition for unassociated words were tested after a 7hr retention period (with a betweensession nap or drug intervention). A second, different, word list was administered post-intervention and memory was tested after a 20min retention period. The non-declarative tasks (finger tapping task and texture discrimination task) were trained before the intervention and then retested afterwards. Naps enhanced recall of words after a 7hr and 20min retention interval relative to both caffeine and placebo. Caffeine significantly impaired motor learning compared to placebo and naps. Napping produced robust perceptual learning compared with placebo; however, naps and caffeine were not significantly different. These findings provide evidence of the limited benefits of caffeine for memory improvement compared with napping. We hypothesize that impairment from caffeine may be restricted to tasks that contain explicit information; whereas strictly implicit learning is less compromised.

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Section: Resultsmentioning

confidence: 99%

Comparing the benefits of caffeine, naps and placebo on verbal, motor and perceptual memory

Mednick

Cai

Kanady

et al. 2008

Behavioural Brain Research

108

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“…Third, the comparatively low level of sensory input experienced during SWS is an important way of minimising interference from external sources. Finally, the drastic reduction in acetylcholine that occurs during SWS, and that is essential for the transfer of information from hippocampal to neocortical memory stores [42], could also facilitate abstraction. Our proposal that SWS facilitates abstraction builds upon several influential theories of consolidation [14,17,34,43] which argue that slow waves assist the transfer of hippocampal memories to the neocortex (Box 2).…”

Section: Why Sleep?mentioning

confidence: 99%

Overlapping memory replay during sleep builds cognitive schemata

Lewis

Durrant

2011

Trends in Cognitive Sciences

450

437

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Sleep enhances integration across multiple stimuli, abstraction of general rules, insight into hidden solutions and false memory formation. Newly learned information is better assimilated if compatible with an existing cognitive framework or schema. This article proposes a mechanism by which the reactivation of newly learned memories during sleep could actively underpin both schema formation and the addition of new knowledge to existing schemata. Under this model, the overlapping replay of related memories selectively strengthens shared elements. Repeated reactivation of memories in different combinations progressively builds schematic representations of the relationships between stimuli. We argue that this selective strengthening forms the basis of cognitive abstraction, and explain how it facilitates insight and false memory formation.What's the gist? I do not remember many details about childhood birthday parties. There was one when we played blind man's bluff, and another with cucumber sandwiches, but in general these affairs blur together under the broad heading of birthdays. About this category I have much information: I know the parties involved hordes of children, that there were presents and invariably a cake. However, which birthday belonged to whom, and exactly what was done there escapes me. This is unsurprising as chronologically old memories rarely include clear episodic details but these aspects of a situation or memory type that are repeated again and again are normally recalled with ease. Central shared concepts of this type can be thought of as the 'gist' (see Glossary), or essential features, of a set of memories, and taken together can form a cognitive framework of expectations or schema (Box 1). This article proposes a physiological mechanism by which memory replay during sleep could be responsible for the abstraction of gist information from newly encoded memories to form cognitive schemata.Recent research has shown that sleep facilitates abstraction of gist information [1][2][3][4][5] as well as integration across multiple memories [6][7][8], insight into hidden solutions [9], and even the ability to make creative connections between distantly related ideas and concepts [10]. These findings build upon a strong body of work demonstrating that sleep plays a crucial role in memory consolidation (for reviews [11][12][13]), as well as a highly influential model of how memories are re-organised and strengthened by replay during slow wave sleep (SWS) (see [11,12,[14][15][16][17] and Box 2). This model elegantly explains how the specific physiology of SWS, in combination with the replay of memories that has been observed in both rats and humans during this sleep stage (Box 3), could assist consolidation by transferring memories from a short-term store in the hippocampus to longer term cortical representations. Importantly, however, this model cannot presently explain why sleep is beneficial for gist extraction, insight or the formation of false memories.A separate line of research investigating th...

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“…Although consolidation of declarative, hippocampus-dependent memories of events and facts depends particularly on periods of SWS and on low cholinergic activity after learning (Marshall and Born, 2007;Gais and Born, 2004;Rasch et al, 2006), long-term acquisition of skills has been associated repeatedly with REM sleep after training , during which cholinergic tone regains wake-like levels. Numerous animal studies have shown that REM sleep is enhanced after learning of complex procedural tasks, and deprivation of REM sleep, by selective awakenings during certain time windows after learning, impairs subsequent task performance (see Smith, 1995;Peigneux et al, 2001, for a review).…”

Section: Introductionmentioning

confidence: 99%

Impaired Off-Line Consolidation of Motor Memories After Combined Blockade of Cholinergic Receptors During REM Sleep-Rich Sleep

Rasch

Gais

Born

2009

Neuropsychopharmacol

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Rapid eye movement (REM) sleep has been considered important for the consolidation of memories, particularly of procedural skills. REM sleep, in contrast to slow-wave sleep (SWS), is hallmarked by the high, wake-like activity of the neurotransmitter acetylcholine (ACh), which promotes certain synaptic plastic processes underlying the formation of memories. Here, we show in healthy young men that off-line consolidation of a motor skill during a period of late sleep with high amounts of REM sleep depends essentially on high cholinergic activity. After a 3-h sleep period during the early night to satisfy the need for SWS, subjects learned a procedural finger sequence tapping task and a declarative word-pair learning task. After learning, they received either placebo or a combination of the muscarinic receptor antagonist scopolamine (4 mg/kg bodyweight, intravenously) and the nicotinic receptor antagonist mecamylamine (5 mg, orally), and then slept for another 3 h, ie, the late nocturnal sleep period, which is dominated by REM sleep. Retrieval was tested the following evening. Combined cholinergic receptor blockade significantly impaired motor skill consolidation, whereas word-pair memory remained unaffected. Additional data show that the impairing effect of cholinergic receptor blockade is specific to sleepdependent consolidation of motor skill and does not occur during a wake-retention interval. Taken together, these results identify high cholinergic activity during late, REM sleep-rich sleep as an essential factor promoting sleep-dependent consolidation of motor skills.

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Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation

Cited by 356 publications

References 41 publications

Comparing the benefits of caffeine, naps and placebo on verbal, motor and perceptual memory

Comparing the benefits of caffeine, naps and placebo on verbal, motor and perceptual memory

Overlapping memory replay during sleep builds cognitive schemata

Impaired Off-Line Consolidation of Motor Memories After Combined Blockade of Cholinergic Receptors During REM Sleep-Rich Sleep

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