Dataset Information

Local experience-dependent changes in the wake EEG after prolonged wakefulness.

ABSTRACT:

Study objectives

Prolonged wakefulness leads to a progressive increase in sleep pressure, reflected in a global increase in slow wave activity (SWA, 0.5-4.5 Hz) in the sleep electroencephalogram (EEG). A global increase in wake theta activity (5-9 Hz) also occurs. Recently, it was shown that prolonged wakefulness in rodents leads to signs of "local sleep" in an otherwise awake brain, accompanied by a slow/theta wave (2-6 Hz) in the local EEG that occurs at different times in different cortical areas. Compelling evidence in animals and humans also indicates that sleep is locally regulated by the amount of experience-dependent plasticity. Here, we asked whether the extended practice of tasks that involve specific brain circuits results in increased occurrence of local intermittent theta waves in the human EEG, above and beyond the global EEG changes previously described.

Design

Participants recorded with high-density EEG completed 2 experiments during which they stayed awake ? 24 h practicing a language task (audiobook listening [AB]) or a visuomotor task (driving simulator [DS]).

Setting

Sleep laboratory.

Patients or participants

16 healthy participants (7 females).

Interventions

Two extended wake periods.

Measurements and results

Both conditions resulted in global increases in resting wake EEG theta power at the end of 24 h of wake, accompanied by increased sleepiness. Moreover, wake theta power as well as the occurrence and amplitude of theta waves showed regional, task-dependent changes, increasing more over left frontal derivations in AB, and over posterior parietal regions in DS. These local changes in wake theta power correlated with similar local changes in sleep low frequencies including SWA.

Conclusions

Extended experience-dependent plasticity of specific circuits results in a local increase of the wake theta EEG power in those regions, followed by more intense sleep, as reflected by SWA, over the same areas.

SUBMITTER: Hung CS

PROVIDER: S-EPMC3524543 | biostudies-literature | 2013 Jan

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Local experience-dependent changes in the wake EEG after prolonged wakefulness.

Hung Ching-Sui CS Sarasso Simone S Ferrarelli Fabio F Riedner Brady B Ghilardi M Felice MF Cirelli Chiara C Tononi Giulio G

Sleep 20130101 1

<h4>Study objectives</h4>Prolonged wakefulness leads to a progressive increase in sleep pressure, reflected in a global increase in slow wave activity (SWA, 0.5-4.5 Hz) in the sleep electroencephalogram (EEG). A global increase in wake theta activity (5-9 Hz) also occurs. Recently, it was shown that prolonged wakefulness in rodents leads to signs of "local sleep" in an otherwise awake brain, accompanied by a slow/theta wave (2-6 Hz) in the local EEG that occurs at different times in different co ...[more]

PMID: 23288972

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Project description:Sleep and wakefulness are no longer to be considered as discrete states. During wakefulness brain regions can enter a sleep-like state (off-periods) in response to a prolonged period of activity (local use-dependent sleep). Similarly, during nonREM sleep the slow-wave activity, the hallmark of sleep plasticity, increases locally in brain regions previously involved in a learning task. Recent studies have demonstrated that behavioral performance may be impaired by off-periods in wake in task-related regions. However, the relation between off-periods in wake, related performance errors and learning is still untested in humans. Here, by employing high density electroencephalographic (hd-EEG) recordings, we investigated local use-dependent sleep in wake, asking participants to repeat continuously two intensive spatial navigation tasks. Critically, one task relied on previous map learning (Wayfinding) while the other did not (Control). Behaviorally awake participants, who were not sleep deprived, showed progressive increments of delta activity only during the learning-based spatial navigation task. As shown by source localization, delta activity was mainly localized in the left parietal and bilateral frontal cortices, all regions known to be engaged in spatial navigation tasks. Moreover, during the Wayfinding task, these increments of delta power were specifically associated with errors, whose probability of occurrence was significantly higher compared to the Control task. Unlike the Wayfinding task, during the Control task neither delta activity nor the number of errors increased progressively. Furthermore, during the Wayfinding task, both the number and the amplitude of individual delta waves, as indexes of neuronal silence in wake (off-periods), were significantly higher during errors than hits. Finally, a path analysis linked the use of the spatial navigation circuits undergone to learning plasticity to off periods in wake. In conclusion, local sleep regulation in wakefulness, associated with performance failures, could be functionally linked to learning-related cortical plasticity.

Dataset Information

Local experience-dependent changes in the wake EEG after prolonged wakefulness.

Study objectives

Design

Setting

Patients or participants

Interventions

Measurements and results

Conclusions

Publications

Local experience-dependent changes in the wake EEG after prolonged wakefulness.

Similar Datasets

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