Sleep is necessary to maintain brain functional efficiency, as shown by the well-known consequences of sleep deprivation – including attention lapses, confusion, emotional instability, etc. - that often result in car accidents or behavioral mistakes. Previous studies carried out in animal models at the Center for Sleep and Consciousness (University of Wisconsin, Madison, WI-USA) demonstrated that extended wakefulness is associated with the occurrence of temporary "local sleep episodes" (neuronal off-periods), potentially leading to behavioral errors.
Now, a novel study performed in a collaboration between the Clinical Psychology Branch at the University Hospital of Pisa, (Pisa, Italy), headed by Prof. Pietro Pietrini, and the Center for Sleep and Consciousness, headed by Prof. Giulio Tononi, revealed that similar local sleep events can occur also in awake humans and may potentially have negative effects on cognitive skills.
In their study, entitled "Neural and behavioral correlates of extended training during sleep deprivation in humans: evidence for local, task-specific effects" and published today by the Journal of Neuroscience, Giulio Bernardi and co-workers asked whether lengthy utilization of specific cognitive functions would exhaust cortical areas devoted to those functions. Specifically, the researchers questioned whether a prolonged practice with tasks requiring self-control would lead to a less efficient impulse control due to fatigue in frontal cortical areas. To test this hypothesis, a group of 16 young healthy subjects performed a series of executive function tasks, known to involve frontal cortical areas, continuously for a 24-hour period with no sleep. As a control task, on a separate day, the same individuals practiced again for 24 hours without sleeping with tasks requiring eye-hand coordination (a driving simulator). The two experimental days were randomized across subjects to avoid any learning or habituation effect.
The authors also used high-density electroencephalography (EEG) to monitor participant brain activity before and during the execution of the specific behavioral tests related to the two distinct cognitive domains. Prolonged exercise in the absence of any sleep recovery resulted in significant behavioral errors during either tasks. Interestingly, errors were associated with the occurrence of slow frequency oscillations (similar to those normally observed during sleep) within the brain regions that were associated to the specific task.
These findings expand previous data from the same groups in animals by showing that prolonged practice with specific activities can lead to progressively increasing "functional fatigue" in those brain regions that are maximally involved in task execution. In these conditions, although individuals may appear fully awake based on their general behavior and scalp EEG, some brain areas may be actually turning off at unpredictable times, with potential negative effects on cognitive performance as well as on behavioral control.
These findings indicate that temporary deactivations of brain areas involved in specific activities could be responsible for relevant behavioral alterations in humans. In fact, these results may contribute elucidating the mechanisms leading to performance failures, impulsiveness or dis-inhibition during acute sleep deprivation or chronic sleep restriction, and open the doors for the development of new approaches for their identification and prevention. "Frontal functional fatigue in individuals who are for long time under undue stressful situations may contribute to the sudden loss of impulse control that often we observe in forensic psychiatric examinations - concludes Prof. Pietrini (on the right, with the researcher Emiliano Ricciardi) - These results prompt novel insights into the genesis and dynamics of explosive antisocial behaviors".
Further studies are being developed to determine whether specific factors - such as genetic predisposition, brain morphological or functional abnormalities and environmental issues - may be associated to a particular vulnerability to cognitive fatigue and to the occurrence of local sleep episodes.
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Neural and Behavioral Correlates of Extended Training during Sleep Deprivation in Humans: Evidence for Local, Task-Specific Effects
Bernardi Giulio 1,2,3, Siclari Francesca 1, Yu Xiaoqian 1, Zennig Corinna 1, Bellesi Michele 1, Ricciardi Emiliano 2,3, Cirelli Chiara 1, Ghilardi Maria Felice 4, Pietrini Pietro 2,3*, Tononi Giulio 1*
1 Department of Psychiatry, University of Wisconsin, Madison, Wisconsin, USA
2 Laboratory of Clinical Biochemistry and Molecular Biology, University of Pisa, Italy
3 Clinical Psychology Branch, University of Pisa, AOUP Santa Chiara, Pisa, Italy
4 Department of Physiology and Pharmacology, City University of New York Medical School, New York, NY