System consolidation of memory during sleep

Department of Medical Psychology and Neurobiology, University of Tübingen, Gartenstr. 29, 72074, Tübingen, Germany.
Psychological Research (Impact Factor: 2.47). 05/2011; 76(2):192-203. DOI: 10.1007/s00426-011-0335-6
Source: PubMed


Over the past two decades, research has accumulated compelling evidence that sleep supports the formation of long-term memory. The standard two-stage memory model that has been originally elaborated for declarative memory assumes that new memories are transiently encoded into a temporary store (represented by the hippocampus in the declarative memory system) before they are gradually transferred into a long-term store (mainly represented by the neocortex), or are forgotten. Based on this model, we propose that sleep, as an offline mode of brain processing, serves the 'active system consolidation' of memory, i.e. the process in which newly encoded memory representations become redistributed to other neuron networks serving as long-term store. System consolidation takes place during slow-wave sleep (SWS) rather than rapid eye movement (REM) sleep. The concept of active system consolidation during sleep implicates that (a) memories are reactivated during sleep to be consolidated, (b) the consolidation process during sleep is selective inasmuch as it does not enhance every memory, and (c) memories, when transferred to the long-term store undergo qualitative changes. Experimental evidence for these three central implications is provided: It has been shown that reactivation of memories during SWS plays a causal role for consolidation, that sleep and specifically SWS consolidates preferentially memories with relevance for future plans, and that sleep produces qualitative changes in memory representations such that the extraction of explicit and conscious knowledge from implicitly learned materials is facilitated.

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    • "Scored data were then partitioned in terms of the percentage of total sleep time spent in stage 1 sleep (S1), stage 2 sleep (S2), SWS, and REM. To examine how SWS and REM, which have been previously implicated in the respective consolidation of neutral and emotional declarative memory (Wagner et al. 2001; Hu et al. 2006; Born and Wilhelm 2012), impacted upon subsequent remote memory performance, we separately correlated these sleep parameters with our scores of behavioral consolidation for positive, negative, and neutral images. "
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    ABSTRACT: Although rapid eye movement sleep (REM) is regularly implicated in emotional memory consolidation, the role of slow-wave sleep (SWS) in this process is largely uncharacterized. In the present study, we investigated the relative impacts of nocturnal SWS and REM upon the consolidation of emotional memories using functional magnetic resonance imaging (fMRI) and polysomnography (PSG). Participants encoded emotionally positive, negative, and neutral images (remote memories) before a night of PSG-monitored sleep. Twenty-four hours later, they encoded a second set of images (recent memories) immediately before a recognition test in an MRI scanner. SWS predicted superior memory for remote negative images and a reduction in right hippocampal responses during the recollection of these items. REM, however, predicted an overnight increase in hippocampal–neocortical connectivity associated with negative remote memory. These findings provide physiological support for sequential views of sleep-dependent memory processing, demonstrating that SWS and REM serve distinct but complementary functions in consolidation. Furthermore, these findings extend those ideas to emotional memory by showing that, once selectively reorganized away from the hippocampus during SWS, emotionally aversive representations undergo a comparably targeted process during subsequent REM.
    Cerebral Cortex 06/2015; DOI:10.1093/cercor/bht349 · 8.67 Impact Factor
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    • "In addition to the quantitative strengthening of memories, the hippocampaleneocortical dialogue may also result in qualitative changes at the behavioural level [97]. For example, correlations between relational memory and SWS [41] and between memory integration and sleep spindle activity [29] have been observed. "
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    • "On the other hand, previous studies showed that hippocampal delta oscillatory activity at 3 Hz increases during spatial navigation tasks (Ekstrom et al., 2005; Watrous et al., 2011; Clemens et al., 2013), a result that although not statistically significant we have replicated also in the present study (see below). Hence, one could speculate that the observed increase of the same slow rhythm during postlearning NREM sleep may be a marker of EEG replay, which redistributes memories in widespread neural networks serving as longterm store (Diekelmann and Born, 2010; Born and Wilhelm, 2012). The above mentioned spatial navigation data together with our observations during wakefulness and REM sleep (Moroni et al., 2007, 2012) strongly suggest that hippocampal delta oscillatory activity at 3 Hz is a marker of regional activation states. "
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    ABSTRACT: The hypothesis that sleep is instrumental in the process of memory consolidation is currently largely accepted. Hippocampal formation is involved in the acquisition of declarative memories and particularly of spatial memories. Nevertheless, although largely investigated in rodents, the relations between spatial memory and hippocampal EEG activity have been scarcely studied in humans. Aimed to evaluate the effects of spatial learning on human hippocampal sleep EEG activity, we recorded hippocampal Stereo-EEG (SEEG) in a group of refractory epilepsy patients undergoing presurgical clinical evaluation, after a training on a spatial navigation task. We observed that hippocampal high-delta (2-4 Hz range) activity increases during the first NREM episode after learning compared to the baseline night. Moreover, the amount of hippocampal NREM high-delta power was correlated with task performance at retest. The effect involved only the hippocampal EEG frequencies inasmuch no differences were observed at the neocortical electrodes and in the traditional polysomnographic measures. The present findings support the crucial role of hippocampal slow EEG frequencies during sleep in the memory consolidation processes. More generally, together with previous results, they suggest that slow frequency rhythms are a fundamental characteristic of human hippocampal EEG during both sleep and wakefulness, and are related to the consolidation of different types of memories. © 2014 Wiley Periodicals, Inc.
    Hippocampus 10/2014; 24(10). DOI:10.1002/hipo.22299 · 4.16 Impact Factor
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