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Literature Reviews Sleep Is Central to Memory Consolidation and Learning Literature reviews Sleep is central to memory consolidation and learning NREM sleep contributes to and nonrapid eye movement (NREM) sleep. For example, total sleep time was 448 and 472 min- memory performance utes on nights 1 and 2 for the gifted individual compared with a mean of 455 minutes in controls vidence for a relationship between sleep, learn- with normal memory function. However, cyclic Eing and memory has been provided by behav- alternating pattern (CAP) analysis of the gifted ioral and neurocognitive studies, and it is thought individuals sleep revealed interesting features that that sleep influences the plastic cerebral changes differed from the norm (table I). CAP is thought that underlie learning and memory. How sleep to be responsible for NREM sleep stability, as it is relates to the exceptionally good memory of gifted involved in the structural organization of NREM individuals – the focus of a recent case study by sleep. It corresponds to prolonged oscillation of Ferini-Strambi and colleagues – has, however, the cortical electrical activity evaluated through received little attention. electroencephalogram (EEG) patterns between two reciprocal functional states termed phase A and Ferini-Strambi et al. assessed the sleep patterns of phase B. In humans, phase A of the CAP is classi- a male subject with an outstanding memory per- fied into three subtypes: phase A , characterized by formance to understand the specific structural 1 synchronized EEG patterns; phase A , character- components of sleep that were associated with 2 ized by a balanced mixture of synchronized and superior memory. The exceptional memory per- desynchronized EEG patterns; and phase A , char- formance of this individual was confirmed by a 3 acterized mostly by desynchronized EEG patterns. variety of standard psychometric tests, including The investigators recorded a CAP that was typified short-term memory (span), logical memory and by an increased number of periodic fluctuations verbal episodic learning tasks. during NREM sleep (7–8 SD units above the The patient’s sleep structure was assessed by number observed in age-matched controls). polysomnography on two consecutive nights and Indeed, evaluation of the phase A sleep subtypes was found to be similar to that of control individ- demonstrated that phase A1, in particular, was uals, in terms of sleep induction and maintenance, increased (68.2% and 69.1% on nights 1 and 2, as well as percentage rapid eye movement (REM) respectively) compared with controls (61.4%). As Table I. Cyclic alternating pattern (CAP) rate by sleep stage on two nights in an individual with superior memory and in individuals with normal memory function (n=10).1 Sleep stage CAP rate (%) Individual with superior memory Normal individuals (mean ± standard Night 1 Night 2 deviation) Non-rapid eye movement 63.2 64.5 31.9 ± 7.0 Stage 1 39.3 38.2 38.3 ± 16.4 Stage 2 66.5 70.7 32.6 ± 6.4 Stage 3 78.3 79.1 44.0 ± 16.3 Stage 4 68.7 69.8 24.4 ± 11.5 LITERATURE 10 INSOM Issue 5 June 2005 REVIEWS Literature reviews phase A1 is related to the achievement and main- sleep, REM sleep, and pre- and postsleep wakeful- tenance of slow-wave sleep (SWS), this individual ness) following an extended period of training in had particularly efficient SWS. This is noteworthy, the topographical memory task; and Group 3 was as SWS itself is believed to generate conditions monitored during all stages of nocturnal sleep favorable for the consolidation of memory traces without prior training. Sleep was monitored by acquired during wakefulness. polysomnography and changes in rCBF were measured by positron-emission tomography. The authors conclude that their observations are in line with the hypothesis for a link between NREM To determine the specificity of rCBF patterns for sleep and declarative memory performance, as has spatial declarative, rather than procedural impli- been put forward in previous publications that cit, learning, the investigators included rCBF data implicate the early period of sleep, dominated by previously obtained from another study, in which SWS, in the consolidation of declarative memory. subjects had been extensively trained for a proce- Although confirmatory studies in larger cohorts are dural serial reaction time (SRT) task (Group 4). needed, the results of the present case study pro- The investigators found that, during wakefulness, vide an insight into the relationship between sleep the rCBF pattern in subjects who were scanned and memory performance in gifted individuals. ■ while practicing the topographical memory task Ferini-Strambi L, Ortelli P, Castronovo V, Cappa S. differed significantly from the pattern for the SRT Increased periodic arousal fluctuations during task, confirming that the navigation network was non-REM sleep are associated with superior activated. The specific regions of the brain collec- memory. Brain Res Bull 2004;63(6):439–42. tively known as the navigation network are pre- dominantly responsible for spatial learning and include the right hippocampus, the right caudate Slow-wave sleep and nucleus, and the right inferior parietal and bilat- eral medial parietal regions.2 The authors also spatial memory found a correlation between performance in the consolidation topographical task and increases of rCBF in specific areas of the hippocampal region, indicating that nformation acquired during wakefulness is hippocampal activity positively relates to the accur- Ibelieved to be actively restructured and strength- acy of route finding. ened during sleep, facilitating memory formation Compared with wakefulness, rCBF was markedly and consolidation. Observations from rodent stud- increased during SWS, stage 2 sleep and REM ies support this hypothesis, as they suggest that the sleep across all groups, regardless of the presleep same sets of neurons that are activated in the hip- experience (trained in the topographical memory pocampal region of the brain during spatial learn- task, not trained in this task or trained in the SRT ing are reactivated during subsequent NREM task). However, although the broad pattern of rCBF sleep. This ‘off-line’ replay of hippocampal activ- observed during sleep was similar between groups, ity might be involved in the consolidation of newly significant differences in the amplitude of rCBF acquired spatial information and its gradual trans- reactivation were identified through a series of lation into long-term memory stores. interaction analyses. These analyses showed that In their study, Peigneux and colleagues focused on topographical training vs no training was associated spatial memory formation in humans. They moni- with greater activity in hippocampal and parahip- tored regional cerebral blood flow (rCBF), a pocampal regions during posttraining NREM sleep marker of local synaptic activity, in healthy male (especially SWS sleep) when compared either with subjects (aged 18.3–29.9 years) under three circum- REM sleep or wakefulness. Interestingly, interac- stances: Group 1 was monitored during training tion analyses comparing topographic task-trained for a topographical memory task (the subjects had subjects with SRT-trained subjects generated simi- to find their way inside a complex three- lar results, indicating that the observed neuronal dimensional virtual town); Group 2 was monitored activation depends on the type of learning and not during all stages of nocturnal sleep (SWS, stage 2 simply on intensive stimulation prior to sleep. LITERATURE LITERATURE INSOM Issue 5 June 2005 11 REVIEWS REVIEWS Literature reviews Importantly, performance in the topographic task mean IQ scores as determined by a general intel- improved following a night’s sleep. Trained sub- ligence test based on verbal and performance jects in Group 3 came closer to their target desti- potential (HiQ=125.8, MedQ=114.7, LoQ=102.5, nation in the virtual town within an allotted time Control=108.3). Following acclimatization to the limit than on the previous day. This overnight gain sleep laboratory (two nights), baseline values in performance occurred in all subjects and was were recorded for EEG, electrooculograms and strongly correlated with the amplitude of rCBF in electromyograms. Prior to the post-training distinct hippocampal and the parahippocampal polysomnographic evaluation, subjects in the regions during SWS (r=0.94). active group performed two learning tasks (‘mirror trace’ task and ‘tower of Hanoi’ task), while con- The authors conclude that, in humans, hippocam- trol subjects watched movies or read. The follow- pal activity during SWS is modulated by recent ing day, subjects in the active group were retested waking spatial experience and, furthermore, that on the learning tasks. the greater the amplitude of hippocampal reactiva- tion during SWS sleep the greater the overnight The authors found that the time taken to finish the improvement in performance of a spatial memory learning tasks dropped significantly from training task. According to the authors, these results sup- to retest in all learning groups (P<0.0000), regard- port the hypothesis that enhanced hippocampal less of IQ. Unsurprisingly, they also found that IQ activity during posttraining SWS reflects off-line affected performance, as the HiQ group made processing of memory traces, which eventually fewer errors during training than the MedQ leads to the improvement in performance the next group, who in turn made fewer errors than the day. ■ LoQ group on the ‘tower of Hanoi’ task. For the ‘mirror trace’ task, there was no difference
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