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      Sleep spindles in midday naps enhance learning in preschool children

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      Proceedings of the National Academy of Sciences
      Proceedings of the National Academy of Sciences

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          Abstract

          Despite the fact that midday naps are characteristic of early childhood, very little is understood about the structure and function of these sleep bouts. Given that sleep benefits memory in young adults, it is possible that naps serve a similar function for young children. However, children transition from biphasic to monophasic sleep patterns in early childhood, eliminating the nap from their daily sleep schedule. As such, naps may contain mostly light sleep stages and serve little function for learning and memory during this transitional age. Lacking scientific understanding of the function of naps in early childhood, policy makers may eliminate preschool classroom nap opportunities due to increasing curriculum demands. Here we show evidence that classroom naps support learning in preschool children by enhancing memories acquired earlier in the day compared with equivalent intervals spent awake. This nap benefit is greatest for children who nap habitually, regardless of age. Performance losses when nap-deprived are not recovered during subsequent overnight sleep. Physiological recordings of naps support a role of sleep spindles in memory performance. These results suggest that distributed sleep is critical in early learning; when short-term memory stores are limited, memory consolidation must take place frequently.

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          Most cited references33

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          Fast and slow spindles during the sleep slow oscillation: disparate coalescence and engagement in memory processing.

          Thalamo-cortical spindles driven by the up-state of neocortical slow (< 1 Hz) oscillations (SOs) represent a candidate mechanism of memory consolidation during sleep. We examined interactions between SOs and spindles in human slow wave sleep, focusing on the presumed existence of 2 kinds of spindles, i.e., slow frontocortical and fast centro-parietal spindles. Two experiments were performed in healthy humans (24.5 ± 0.9 y) investigating undisturbed sleep (Experiment I) and the effects of prior learning (word paired associates) vs. non-learning (Experiment II) on multichannel EEG recordings during sleep. Only fast spindles (12-15 Hz) were synchronized to the depolarizing SO up-state. Slow spindles (9-12 Hz) occurred preferentially at the transition into the SO down-state, i.e., during waning depolarization. Slow spindles also revealed a higher probability to follow rather than precede fast spindles. For sequences of individual SOs, fast spindle activity was largest for "initial" SOs, whereas SO amplitude and slow spindle activity were largest for succeeding SOs. Prior learning enhanced this pattern. The finding that fast and slow spindles occur at different times of the SO cycle points to disparate generating mechanisms for the 2 kinds of spindles. The reported temporal relationships during SO sequences suggest that fast spindles, driven by the SO up-state feed back to enhance the likelihood of succeeding SOs together with slow spindles. By enforcing such SO-spindle cycles, particularly after prior learning, fast spindles possibly play a key role in sleep-dependent memory processing.
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            Development of the EEG from 5 months to 4 years of age.

            This report provides a systematic longitudinal analysis of the EEG from infancy into early childhood. Particular emphasis is placed on the empirical confirmation of a 6-9 Hz alpha-range frequency band that has previously been used in the infant EEG literature. EEG data in 1-Hz bins from 3 to 12 Hz were analyzed from a longitudinal sample of 29 participants at 5, 10, 14, 24, and 51 months of age. Inspection of power spectra averaged across the whole sample indicated the emergence of a peak in the 6-9 Hz range across multiple scalp regions. Coding of peaks in the power spectra of individual infants showed a clear developmental increase in the frequency of this peak. A rhythm in the 6-9 Hz emerged at central sites that was independent of the classical alpha rhythm at posterior sites. The relative amplitude of this central rhythm peaked in the second year of life, when major changes are occurring in locomotor behavior. The 6-9 Hz band is a useful alpha-range band from the end of the first year of life into early childhood. The findings also complement other research relating the infant central rhythm with the adult sensorimotor mu rhythm.
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              Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation?

              Sleep spindles are thought to induce synaptic changes and thereby contribute to memory consolidation during sleep. Patients with schizophrenia show dramatic reductions of both spindles and sleep-dependent memory consolidation, which may be causally related. To examine the relations of sleep spindle activity to sleep-dependent consolidation of motor procedural memory, 21 chronic, medicated schizophrenia outpatients and 17 healthy volunteers underwent polysomnography on two consecutive nights. On the second night, participants were trained on the finger-tapping motor sequence task (MST) at bedtime and tested the following morning. The number, density, frequency, duration, amplitude, spectral content, and coherence of stage 2 sleep spindles were compared between groups and examined in relation to overnight changes in MST performance. Patients failed to show overnight improvement on the MST and differed significantly from control participants who did improve. Patients also exhibited marked reductions in the density (reduced 38% relative to control participants), number (reduced 36%), and coherence (reduced 19%) of sleep spindles but showed no abnormalities in the morphology of individual spindles or of sleep architecture. In patients, reduced spindle number and density predicted less overnight improvement on the MST. In addition, reduced amplitude and sigma power of individual spindles correlated with greater severity of positive symptoms. The observed sleep spindle abnormalities implicate thalamocortical network dysfunction in schizophrenia. In addition, the findings suggest that abnormal spindle generation impairs sleep-dependent memory consolidation in schizophrenia, contributes to positive symptoms, and is a promising novel target for the treatment of cognitive deficits in schizophrenia. Copyright © 2012 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.
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                Author and article information

                Journal
                Proceedings of the National Academy of Sciences
                Proceedings of the National Academy of Sciences
                Proceedings of the National Academy of Sciences
                0027-8424
                1091-6490
                October 22 2013
                October 22 2013
                September 23 2013
                October 22 2013
                : 110
                : 43
                : 17267-17272
                Article
                10.1073/pnas.1306418110
                3808582
                24062429
                2ae341d1-316b-4874-a534-89a3e8345689
                © 2013
                History

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