An N-methyl-d-aspartate receptor agonist facilitates sleep-independent synaptic plasticity associated with working memory capacity enhancement

Kuriyama, Kenichi; Honma, Motoyasu; Shimazaki, Miyuki; Horie, Michiko; Yoshiike, Takashi; Koyama, Sayori; Kim, Yoshiharu

doi:10.1038/srep00127

Cited by 11 publications

(10 citation statements)

References 68 publications

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“…after sleep for emotional and neutral pictures, which might reflect that sleep-associated consolidation of these memories is not primarily a consequence of hippocampal reactivation (Debas et al, 2010;Diekelmann and Born, 2010;Karni et al, 1998;Wagner et al, 2001 but see also Albouy et al, 2008). The findings concur with previous studies that likewise failed to observe DCS-induced changes in overnight gains in cognitive skill, although benefits in retention occurred for working memory training and emotional memories when participants were awake (Kalisch et al, 2009;Kuriyama et al, 2011b). Interestingly, in a previous study of ours both blocking of NMDA receptors and of AMPA receptors impaired sleep-dependent gains in a procedural visual texture discrimination task (Gais et al, 2008).…”

Section: Discussionsupporting

confidence: 89%

Sleep-Dependent Declarative Memory Consolidation—Unaffected after Blocking NMDA or AMPA Receptors but Enhanced by NMDA Coagonist D-Cycloserine

Feld

Lange

Gais

et al. 2013

Neuropsychopharmacol

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Sleep has a pivotal role in the consolidation of declarative memory. The coordinated neuronal replay of information encoded before sleep has been identified as a key process. It is assumed that the repeated reactivation of firing patterns in glutamatergic neuron assemblies translates into plastic synaptic changes underlying the formation of longer-term neuronal representations. Here, we tested the effects of blocking and enhancing glutamatergic neurotransmission during sleep on declarative memory consolidation in humans. We conducted three placebo-controlled, crossover, double-blind studies in which participants learned a word-pair association task. Afterwards, they slept in a sleep laboratory and received glutamatergic modulators. Our first two studies aimed at impairing consolidation by administering the NMDA receptor blocker ketamine and the AMPA receptor blocker caroverine during retention sleep, which, paradoxically, remained unsuccessful, inasmuch as declarative memory performance was unaffected by the treatment. However, in the third study, administration of the NMDA receptor coagonist D-cycloserine (DCS) during retention sleep facilitated consolidation of declarative memory (word pairs) but not consolidation of a procedural control task (finger sequence tapping). Administration of DCS during a wake interval remained without effect on retention of word pairs but improved encoding of numbers. From the overall pattern, we conclude that the consolidation of hippocampus-dependent declarative memory during sleep relies on NMDA-related plastic processes that differ from those processes leading to wake encoding. We speculate that glutamatergic activation during sleep is not only involved in consolidation but also in forgetting of hippocampal memory with both processes being differentially sensitive to DCS and unselective blockade of NMDA and AMPA receptors.

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Section: Discussionsupporting

confidence: 89%

Sleep-Dependent Declarative Memory Consolidation—Unaffected after Blocking NMDA or AMPA Receptors but Enhanced by NMDA Coagonist D-Cycloserine

Feld

Lange

Gais

et al. 2013

Neuropsychopharmacol

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“…The concept of WM refers to the temporary storage and manipulation of information. Previous investigations suggest improvements of executive aspects of WM performance, for instance in monitoring and manipulation of information held online, by training [21] as well as positive effects of night-time sleep [22] , [23] . Moreover, we recently observed increased WM performance during a multiple nap compared to sleep deprivation protocol, specifically driven by heterozygous carriers of the ADA polymorphism [17] .…”

Section: Introductionmentioning

confidence: 98%

The Circadian Regulation of Sleep: Impact of a Functional ADA-Polymorphism and Its Association to Working Memory Improvements

et al. 2014

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Sleep is regulated in a time-of-day dependent manner and profits working memory. However, the impact of the circadian timing system as well as contributions of specific sleep properties to this beneficial effect remains largely unexplored. Moreover, it is unclear to which extent inter-individual differences in sleep-wake regulation depend on circadian phase and modulate the association between sleep and working memory. Here, sleep electroencephalography (EEG) was recorded during a 40-h multiple nap protocol, and working memory performance was assessed by the n-back task 10 times before and after each scheduled nap sleep episode. Twenty-four participants were genotyped regarding a functional polymorphism in adenosine deaminase (rs73598374, 12 G/A-, 12 G/G-allele carriers), previously associated with differences in sleep-wake regulation. Our results indicate that genotype-driven differences in sleep depend on circadian phase: heterozygous participants were awake longer and slept less at the end of the biological day, while they exhibited longer non rapid eye movement (NREM) sleep and slow wave sleep concomitant with reduced power between 8–16 Hz at the end of the biological night. Slow wave sleep and NREM sleep delta EEG activity covaried positively with overall working memory performance, independent of circadian phase and genotype. Moreover, REM sleep duration benefitted working memory particularly when occurring in the early morning hours and specifically in heterozygous individuals. Even though based on a small sample size and thus requiring replication, our results suggest genotype-dependent differences in circadian sleep regulation. They further indicate that REM sleep, being under strong circadian control, boosts working memory performance according to genotype in a time-of-day dependent manner. Finally, our data provide first evidence that slow wave sleep and NREM sleep delta activity, majorly regulated by sleep homeostatic mechanisms, is linked to working memory independent of the timing of the sleep episode within the 24-h cycle.

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“…Contrary to Goshen et al the animals we used for our study were not raised in reverse cycle, and we thus performed all our behavioural studies during their less active period. Interestingly, several studies have demonstrated the influence of sleep and time of day on hippocampal-dependent plasticity and subsequent behavioural abilities [34], [35], [36], [37]. In addition, a recent paper revealed that, under physiological conditions, time of day influenced IL-1β and IL-1RI expression and speculated that IL-1 may contribute to the basal functioning of the suprachiasmatic nucleus (SNC) clock [38].…”

Section: Discussionmentioning

confidence: 99%

Endogenous IL-1 in Cognitive Function and Anxiety: A Study in IL-1RI−/− Mice

et al. 2013

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Interleukin-1 (IL-1) is a key pro-inflammatory cytokine, produced predominantly by peripheral immune cells but also by glia and some neuronal populations within the brain. Its signalling is mediated via the binding of IL-1α or IL-1β to the interleukin-1 type one receptor (IL-1RI). IL-1 plays a key role in inflammation-induced sickness behaviour, resulting in depressed locomotor activity, decreased exploration, reduced food and water intake and acute cognitive deficits. Conversely, IL-1 has also been suggested to facilitate hippocampal-dependent learning and memory: IL-1RI−/− mice have been reported to show deficits on tasks of visuospatial learning and memory. We sought to investigate whether there is a generalised hippocampal deficit in IL-1RI−/− animals. Therefore, in the current study we compared wildtype (WT) mice to IL-1RI−/− mice using a variety of hippocampal-dependent learning and memory tasks, as well as tests of anxiety and locomotor activity. We found no difference in performance of the IL-1RI−/− mice compared to WT mice in a T-maze working memory task. In addition, the IL-1RI−/− mice showed normal learning in various spatial reference memory tasks including the Y-maze and Morris mater maze, although there was a subtle deficit in choice behaviour in a spatial discrimination, beacon watermaze task. IL-1RI−/− mice also showed normal memory for visuospatial context in the contextual fear conditioning paradigm. In the open field, IL-1RI−/− mice showed a significant increase in distance travelled and rearing behaviour compared to the WT mice and in the elevated plus-maze spent more time in the open arms than did the WT animals. The data suggest that, contrary to prior studies, IL-1RI−/− mice are not robustly impaired on hippocampal-dependent memory and learning but do display open field hyperactivity and decreased anxiety compared to WT mice. The results argue for a careful evaluation of the roles of endogenous IL-1 in hippocampal and limbic system function.

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An N-methyl-d-aspartate receptor agonist facilitates sleep-independent synaptic plasticity associated with working memory capacity enhancement

Cited by 11 publications

References 68 publications

Sleep-Dependent Declarative Memory Consolidation—Unaffected after Blocking NMDA or AMPA Receptors but Enhanced by NMDA Coagonist D-Cycloserine

Sleep-Dependent Declarative Memory Consolidation—Unaffected after Blocking NMDA or AMPA Receptors but Enhanced by NMDA Coagonist D-Cycloserine

The Circadian Regulation of Sleep: Impact of a Functional ADA-Polymorphism and Its Association to Working Memory Improvements

Endogenous IL-1 in Cognitive Function and Anxiety: A Study in IL-1RI−/− Mice

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