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      Differential Associations of Early- and Late-Night Sleep with Functional Brain States Promoting Insight to Abstract Task Regularity

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          Abstract

          Background

          Solving a task with insight has been associated with occipital and right-hemisphere activations. The present study tested the hypothesis if sleep-related alterations in functional activation states modulate the probability of insight into a hidden abstract regularity of a task.

          Methodology

          State-dependent functional activation was measured by beta and alpha electroencephalographic (EEG) activity and spatial synchronization. Task-dependent functional activation was assessed by slow cortical potentials (SPs). EEG parameters during the performance of the Number Reduction Task (NRT) were compared between before sleep and after sleep sessions. In two different groups, the relevant sleep occurred either in the first or in the second half of the night, dominated by slow wave sleep (SWS) or by rapid eye movement (REM) sleep.

          Principal Findings

          Changes in EEG parameters only occurred in the early-night group, not in the late-night group and indicated occipital and right-hemisphere functional alterations. These changes were associated with off-line consolidation of implicit task representations and with the amount of SWS but they did not predict subsequent insight. The gain of insight was, however, independently associated with changes of spectral beta and alpha measures only in those subjects from the two sleep groups who would subsequently comprehend the hidden regularity of the task. Insight-related enhancement of right frontal asymmetry after sleep did not depend on sleep stages.

          Significance

          It is concluded that off-line restructuring of implicit information during sleep is accompanied by alterations of functional activation states after sleep. This mechanism is promoted by SWS but not by REM sleep and may contribute to attaining insight after sleep. Original neurophysiologic evidence is provided for alterations of the functional activation brain states after sleep. These alterations are associated with a decrease in controlled processing within the visual system and with an increase in the functional connectivity of the right hemisphere, and are supported by SWS in the first half of the night.

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          Most cited references51

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          The associative basis of the creative process.

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            Sleep-dependent memory consolidation.

            The concept of 'sleeping on a problem' is familiar to most of us. But with myriad stages of sleep, forms of memory and processes of memory encoding and consolidation, sorting out how sleep contributes to memory has been anything but straightforward. Nevertheless, converging evidence, from the molecular to the phenomenological, leaves little doubt that offline memory reprocessing during sleep is an important component of how our memories are formed and ultimately shaped.
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              New vistas for alpha-frequency band oscillations.

              The amplitude of alpha-frequency band (8-14 Hz) activity in the human electroencephalogram is suppressed by eye opening, visual stimuli and visual scanning, whereas it is enhanced during internal tasks, such as mental calculation and working memory. alpha-Frequency band oscillations have hence been thought to reflect idling or inhibition of task-irrelevant cortical areas. However, recent data on alpha-amplitude and, in particular, alpha-phase dynamics posit a direct and active role for alpha-frequency band rhythmicity in the mechanisms of attention and consciousness. We propose that simultaneous alpha-, beta- (14-30 Hz) and gamma- (30-70 Hz) frequency band oscillations are required for unified cognitive operations, and hypothesize that cross-frequency phase synchrony between alpha, beta and gamma oscillations coordinates the selection and maintenance of neuronal object representations during working memory, perception and consciousness.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                26 February 2010
                : 5
                : 2
                : e9442
                Affiliations
                [1 ]Department of Neurology, University of Lübeck, Lübeck, Germany
                [2 ]Department of Neuroendocrinology, University of Lübeck, Lübeck, Germany
                [3 ]Department of Cognitive Psychophysiology, Institute of Neurobiology, Bulgarian Academy of Sciences, Sofia, Bulgaria
                [4 ]School of Psychology, Bangor University, Gwynedd, United Kingdom
                Cuban Neuroscience Center, Cuba
                Author notes

                Conceived and designed the experiments: UW RV. Performed the experiments: UW RV. Analyzed the data: JY VK. Contributed reagents/materials/analysis tools: JY VK. Wrote the paper: JY VK. Developed additional software for data analysis: VK.

                Article
                09-PONE-RA-12019R2
                10.1371/journal.pone.0009442
                2829083
                20195475
                9a3c6167-030b-4683-b332-74eac6679f74
                Yordanova et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 1 August 2009
                : 8 February 2010
                Page count
                Pages: 14
                Categories
                Research Article
                Neuroscience
                Neuroscience/Behavioral Neuroscience
                Neuroscience/Cognitive Neuroscience
                Neuroscience/Experimental Psychology

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                Uncategorized

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