Removal of Synaptic Ca<sup>2+</sup>-Permeable AMPA Receptors during Sleep

Lanté, Fabien; Toledo-Salas, Juan-Carlos; Ondrejčák, Tomáš; Rowan, Michael J.; Ulrich, Daniel

doi:10.1523/jneurosci.3210-10.2011

Cited by 64 publications

(52 citation statements)

References 56 publications

(69 reference statements)

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“…Pairing synaptic inputs to postsynaptic bursts at frequencies typical for slow-wave sleep in layer V pyramidal cells of somatosensory cortex induced long-term depression of glutamatergic transmission through removal of Ca 2+ -permeable AMPARs [75]. In addition, AMPAR subunit content at these synapses displayed a time-of-day dependence consistent with a regulation through sleep-related plasticity [76]. Slow oscillations, mimicked through repetitive low-frequency discharge, have also been shown to potentiate inhibitory inputs in layer V in rat visual cortex [77].…”

Section: Novel Forms Of Synaptic Plasticitymentioning

confidence: 87%

Manipulating sleep spindles – expanding views on sleep, memory, and disease

Astori

Wimmer²,

Lüthi³

2013

Trends in Neurosciences

127

113

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Abstract:Sleep spindles are distinctive electroencephalographic (EEG) oscillations emerging during non-rapid-eye-movement sleep (NREMS) that have been implicated in multiple brain functions, including sleep quality, sensory gating, learning and memory. Despite considerable knowledge about the mechanisms underlying these neuronal rhythms, their function remains poorly understood and current views are largely based on correlational evidence. Here, we review recent studies in humans and rodents that have begun to broaden our understanding of the role of spindles in the normal and disordered brain. We show that newly identified molecular substrates of spindle oscillations, in combination with evolving technological progress, offer novel targets and tools to selectively manipulate spindles and dissect their role in sleep-dependent processes. Powered by Editorial Manager® and ProduXion Manager® from Aries Systems CorporationAstori et al. Highlights Newly recognized ion channel subtypes generating spindle rhythms are described. The contribution of spindles to arousal threshold and sleep quality is discussed. The proposed role of spindles in memory consolidation is examined. A function of thalamic spindles in neural development is suggested. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 4 Previous excellent reviews have thoroughly described cellular and network bases of spindle generation [3,6,7]. Here, we first review recent work on genetic models that has expanded the mechanistic understanding of this EEG rhythm through the modification of novel molecular substrates. We then discuss the current views about the functional aspects of spindles in brain physiology and pathology, as obtained from studies in naturally sleeping animals and humans. We highlight studies indicating that spindles are accessible for selective interventions, and that, with emerging technologies, will open avenues to decipher spindle function. Novel molecular aspects of spindle generationSleep spindles emerge from a limited set of cellular participants: the resonating core of these waxing-and-waning oscillations resides in the nRt-TC loop, which sustains repetitive burst discharges of its cellular components under the control of cortical inputs (Figure 1 Another important factor in the generation and maintenance of reticular intrinsic oscillations is the aforementioned SK2 or Kcnn2 channel. The vigorous Ca 2+ influx in nRt dendrites originating from Ca V 3.3 channels gates SK2 channels, thereby creating a burstafterhyperpolarization (bAHP) [12,19]. As T channels recover partially from inactivation duri...

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Section: Novel Forms Of Synaptic Plasticitymentioning

confidence: 87%

Manipulating sleep spindles – expanding views on sleep, memory, and disease

Astori

Wimmer²,

Lüthi³

2013

Trends in Neurosciences

127

113

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“…These receptors themselves and/or the Ca 2+ microdomains that they induce (34) may guide the incorporation of newly synthesized synaptic molecules (33) in the synapse-specific manner required for proper memory update on reconsolidation. Intriguingly, CP-AMPARs accumulate at synapses during the daytime and decrease during sleep (43,44). In light of the deep involvement of sleep in (Fig.…”

Section: Discussionmentioning

confidence: 98%

AMPA receptor exchange underlies transient memory destabilization on retrieval

Hong¹,

Kim²,

Kim³

et al. 2013

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

129

167

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The authors note, "For the 'hybrid' location discrimination task, we report data obtained from 27 electrodes, 16 of which were in area 1; the 11 electrodes in area 3b were divided evenly across the two animals (6 and 5). We had previously tested all of the electrodes, including those in area 3b, in the detection and discrimination tasks (as shown in Fig. 3) and found them all to yield approximately equivalent performance (see Fig 3A). We noticed in the hybrid location discrimination task, however, that one of the animals performed much more poorly based on stimulation of area 3b than it did based on stimulation of area 1 (while the other animal performed better based on stimulation of area 1). Having no reason to question any of the arrays, we attributed this discrepancy to differences across animals and arrived at the conclusion, based on pooled data from both animals, that stimulation of the two areas yields equivalent performance in the 'hybrid location discrimination' task. The overall conclusion, then, was that stimulation of neurons in area 3b and 1 evokes percepts that are equally localized on the skin."Shortly after publication of the paper, we repeated detection experiments across the arrays and found that the animal could no longer detect stimulation through the array in area 3b that had yielded poor performance in the hybrid location discrimination task. It is therefore likely that this array had failed between the time we conducted the initial detection and discrimination experiments and the time we conducted the hybrid location discrimination task (which required 2-3 months of retraining). If this is the case, and we eliminate data from that bad array, then the median performance on hybrid trials is 83% (up from the 80% that was originally reported), which is still statistically poorer than that on the location-matched mechanical trials [median difference between performance on mechanical and hybrid trials was 3.3% rather than 5.6%, t (119) = 6.1, P < 0.001] (see the corrected Fig. 2). Thus, we probably underestimated overall performance on hybrid trials, and thus the degree to which artificial percepts are localized, in the original publication. Importantly, however, performance on hybrid trials based on stimulation of area 3b was significantly better than performance based on stimulation of area 1 [median Δp = 0.028 and 0.054 for areas 3b and 1, respectively; t test: t (76) = 2.8, P < 0.01]. Thus, based on the data obtained from only one animal, it seems as though stimulation of area 3b elicits more localized percepts than does stimulation of area 1, as might be expected given that neurons in area 3b tend to have smaller receptive fields than their counterparts in area 1 (1, 2)."As a result of this error, Fig. 2 and its legend appeared incorrectly. The corrected figure and its corresponding legend appear below. On both mechanical and hybrid trials, the relative locations of stimuli applied to widely spaced digits were more accurately discriminated than were the relative locations of stimuli applie...

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“…72 NREMS is also associated with higher levels of insulin, which promotes the internalization of glutamate AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid) receptors that is essential for the expression of LTD. 73 In addition, in vivo and in vitro studies have shown that NREMS could induce LTD in the CA3 and CA1 hippocampal regions 74 by internalization of specific AMPA receptors subtypes. 75 We and others previously showed that inhibiting the protein phosphatase PP2A decreases the internalization of these AMPA receptors and the expression of NMDAR-dependent hippocampal LTD. 26,76 Blocking such LTD results in an increase in behavioral flexibility and WM performance in a T-maze task, suggesting that NMDAR-dependent LTD is required for behavioral flexibility and may act by weakening previously encoded memory traces when new information is learned. 26 On the opposite, we showed that inhibition of protein kinase A (PKA) leads to an increase in hippocampal LTD, cognitive flexibility and WM performance, specifically when repetitive information (proactive interference) are presented as it is the case in a HIWM task.…”

Section: Discussionmentioning

confidence: 95%

Levels of Interference in Long and Short-Term Memory Differentially Modulate Non-REM and REM Sleep

Fraize

Carponcy

Joseph

et al. 2016

Sleep

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Study Objectives: It is commonly accepted that sleep is beneficial to memory processes, but it is still unclear if this benefit originates from improved memory consolidation or enhanced information processing. It has thus been proposed that sleep may also promote forgetting of undesirable and non-essential memories, a process required for optimization of cognitive resources. We tested the hypothesis that non-rapid eye movement sleep (NREMS) promotes forgetting of irrelevant information, more specifically when processing information in working memory (WM), while REM sleep (REMS) facilitates the consolidation of important information. Methods: We recorded sleep patterns of rats trained in a radial maze in three different tasks engaging either the long-term or short-term storage of information, as well as a gradual level of interference. Results: We observed a transient increase in REMS amount on the day the animal learned the rule of a long-term/reference memory task (RM), and, in contrast, a positive correlation between the performance of rats trained in a WM task involving an important processing of interference and the amount of NREMS or slow wave activity. Various oscillatory events were also differentially modulated by the type of training involved. Notably, NREMS spindles and REMS rapid theta increase with RM training, while sharp-wave ripples increase with all types of training. Conclusions: These results suggest that REMS, but also rapid oscillations occurring during NREMS would be specifically implicated in the long-term memory in RM, whereas NREMS and slow oscillations could be involved in the forgetting of irrelevant information required for WM.

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Removal of Synaptic Ca²⁺-Permeable AMPA Receptors during Sleep

Cited by 64 publications

References 56 publications

Manipulating sleep spindles – expanding views on sleep, memory, and disease

Manipulating sleep spindles – expanding views on sleep, memory, and disease

AMPA receptor exchange underlies transient memory destabilization on retrieval

Levels of Interference in Long and Short-Term Memory Differentially Modulate Non-REM and REM Sleep

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Removal of Synaptic Ca2+-Permeable AMPA Receptors during Sleep

Cited by 64 publications

References 56 publications

Manipulating sleep spindles – expanding views on sleep, memory, and disease

Manipulating sleep spindles – expanding views on sleep, memory, and disease

AMPA receptor exchange underlies transient memory destabilization on retrieval

Levels of Interference in Long and Short-Term Memory Differentially Modulate Non-REM and REM Sleep

Contact Info

Product

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Removal of Synaptic Ca²⁺-Permeable AMPA Receptors during Sleep