Effects of Partial and Acute Total Sleep Deprivation on Performance across Cognitive Domains, Individuals and Circadian Phase

PLOS ONE, Dec 2019

Background Cognitive performance deteriorates during extended wakefulness and circadian phase misalignment, and some individuals are more affected than others. Whether performance is affected similarly across cognitive domains, or whether cognitive processes involving Executive Functions are more sensitive to sleep and circadian misalignment than Alertness and Sustained Attention, is a matter of debate. Methodology/Principal Findings We conducted a 2 × 12-day laboratory protocol to characterize the interaction of repeated partial and acute total sleep deprivation and circadian phase on performance across seven cognitive domains in 36 individuals (18 males; mean ± SD of age = 27.6±4.0 years). The sample was stratified for the rs57875989 polymorphism in PER3, which confers cognitive susceptibility to total sleep deprivation. We observed a deterioration of performance during both repeated partial and acute total sleep deprivation. Furthermore, prior partial sleep deprivation led to poorer cognitive performance in a subsequent total sleep deprivation period, but its effect was modulated by circadian phase such that it was virtually absent in the evening wake maintenance zone, and most prominent during early morning hours. A significant effect of PER3 genotype was observed for Subjective Alertness during partial sleep deprivation and on n-back tasks with a high executive load when assessed in the morning hours during total sleep deprivation after partial sleep loss. Overall, however, Subjective Alertness and Sustained Attention were more affected by both partial and total sleep deprivation than other cognitive domains and tasks including n-back tasks of Working Memory, even when implemented with a high executive load. Conclusions/Significance Sleep loss has a primary effect on Sleepiness and Sustained Attention with much smaller effects on challenging Working Memory tasks. These findings have implications for understanding how sleep debt and circadian rhythmicity interact to determine waking performance across cognitive domains and individuals.

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Effects of Partial and Acute Total Sleep Deprivation on Performance across Cognitive Domains, Individuals and Circadian Phase

Individuals and Circadian Phase. PLoS ONE 7(9): e45987. doi:10.1371/journal.pone.0045987 Effects of Partial and Acute Total Sleep Deprivation on Performance across Cognitive Domains, Individuals and Circadian Phase June C. Lo 0 John A. Groeger 0 Nayantara Santhi 0 Emma L. Arbon 0 Alpar S. Lazar 0 Sibah Hasan 0 Malcolm von Schantz 0 Simon N. Archer 0 Derk-Jan Dijk 0 Shin Yamazaki, Vanderbilt University, United States of America 0 1 Surrey Sleep Research Centre, Faculty of Health and Medical Sciences, University of Surrey, Guildford, United Kingdom, 2 Department of Psychology, University of Hull , Hull , United Kingdom , 3 Department of Biochemistry and Physiology, Faculty of Health and Medical Sciences, University of Surrey , Guildford , United Kingdom Background: Cognitive performance deteriorates during extended wakefulness and circadian phase misalignment, and some individuals are more affected than others. Whether performance is affected similarly across cognitive domains, or whether cognitive processes involving Executive Functions are more sensitive to sleep and circadian misalignment than Alertness and Sustained Attention, is a matter of debate. Methodology/Principal Findings: We conducted a 2 6 12-day laboratory protocol to characterize the interaction of repeated partial and acute total sleep deprivation and circadian phase on performance across seven cognitive domains in 36 individuals (18 males; mean 6 SD of age = 27.664.0 years). The sample was stratified for the rs57875989 polymorphism in PER3, which confers cognitive susceptibility to total sleep deprivation. We observed a deterioration of performance during both repeated partial and acute total sleep deprivation. Furthermore, prior partial sleep deprivation led to poorer cognitive performance in a subsequent total sleep deprivation period, but its effect was modulated by circadian phase such that it was virtually absent in the evening wake maintenance zone, and most prominent during early morning hours. A significant effect of PER3 genotype was observed for Subjective Alertness during partial sleep deprivation and on n-back tasks with a high executive load when assessed in the morning hours during total sleep deprivation after partial sleep loss. Overall, however, Subjective Alertness and Sustained Attention were more affected by both partial and total sleep deprivation than other cognitive domains and tasks including n-back tasks of Working Memory, even when implemented with a high executive load. Conclusions/Significance: Sleep loss has a primary effect on Sleepiness and Sustained Attention with much smaller effects on challenging Working Memory tasks. These findings have implications for understanding how sleep debt and circadian rhythmicity interact to determine waking performance across cognitive domains and individuals. - Funding: This study was funded by AFOSR award FA9550-08-1-0080. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: This is not an Industry sponsored study. The authors have declared that no competing interests exist. How sleep loss and circadian clocks affect brain function is a question with topical relevance because of the negative consequences of inadequate sleep and circadian disruption on health and cognition [1,2,3,4]. Cognitive performance deteriorates during total sleep deprivation (TSD) [5,6] and the magnitude of this deterioration is considerable such that already after 24 h of wakefulness, performance on a range of measures is as poor as during alcohol intoxication [7]. Cognitive performance also deteriorates during repeated partial sleep deprivation (PSD), and studies have shown that to maintain brain function during the day, young adults require as much as 89 h of sleep [8,9]. Cognitive performance is markedly affected by circadian rhythmicity, independent of sleep. Performance is jeopardized during the circadian night and early morning, even when participants have been awake for less than 16 h [10,11], but performance is relatively spared in the evening hours during the wake maintenance zone, even when wake duration exceeds 24 h and participants carry a chronic sleep debt [12,13]. These experiments have established that performance at any given time is determined by an interaction of the duration of the preceding wake episode, the chronic sleep debt carried by the individual, as well as the circadian phase at which performance is assessed. Nevertheless, several issues central to a basic understanding of the modulation of cognitive performance by the sleepwake cycle and circadian rhythmicity remain unresolved - not least whether the cognitive control processes underpinning the tasks used in these studies are all similarly affected by sleep history and circadian phase. Such underpinning control processes allow us to determine and achieve task goals [14,15] and include different aspects of Attention (e.g. S (...truncated)


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June C. Lo, John A. Groeger, Nayantara Santhi, Emma L. Arbon, Alpar S. Lazar, Sibah Hasan, Malcolm von Schantz, Simon N. Archer, Derk-Jan Dijk. Effects of Partial and Acute Total Sleep Deprivation on Performance across Cognitive Domains, Individuals and Circadian Phase, PLOS ONE, 2012, 9, DOI: 10.1371/journal.pone.0045987