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

Abstract

BackgroundCognitive 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 FindingsWe 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/SignificanceSleep 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.

Adenosine, Caffeine, and Performance: From Cognitive Neuroscience of Sleep to Sleep Pharmacogenetics

“…Adenosine induces global cortical disfacilitation by reducing the activating input from the ascending arousal pathways and actively excites sleep-active neurons in the ventro-lateral-preoptic area of the hypothalamus. We, thus, hypothesized that adenosine contributes to the regulation of brain functions modulated by the sleep-wake cycle, in particular to sleepiness and sustained attention which are heavily affected by sleep loss (Lo et al 2012). Indeed, convergent pharmacologic and genetic data in animals and humans support the notion that differences in adenosinergic tone in the central nervous system primarily affect vigilant attention.…”

Effects of insufficient sleep on circadian rhythmicity and expression amplitude of the human blood transcriptome

“…Assessments of sleepiness were based on the well-validated and sensitive Karolinska Sleepiness Scale (51), which is a 9-point Likert scale (1 = very alert to 9 = very sleepy, great effort to keep awake). We also report lapses of attention (reaction time > 500 ms) on the psychomotor vigilance task, which are also among the most sensitive indicators of effects of sleep loss (52,53). Please see SI Methods for a description of the constant routine protocol.…”

Response to chronic sleep restriction, extension, and subsequent total sleep deprivation in humans: adaptation or preserved sleep homeostasis?

“…Total sleep deprivation was followed by 12 hr recovery sleep, starting at participants' habitual time (same clock time as in baseline). During all wake episodes, participants completed a battery of performance tests and these results have been reported elsewhere [6].…”

“…Chronically restricted sleep is probably the most widely cited condition associated with negative health consequences, but long self-reported sleep duration also increases the risk of conditions such as type 2 diabetes, cardiovascular disease, and increased risk of all-cause mortality [2][3][4]. In addition, laboratory studies of altered sleep duration have documented changes in waking performance, primarily in response to sleep restriction [5,6]. It is therefore relevant to investigate how sleep is affected and regulated under such conditions.…”

“…Studies investigating the effects of acute total sleep deprivation on cognitive performance have indicated that the sleep loss-related deterioration of cognitive performance during acute total sleep loss depends on prior sleep history. Thus, prior sleep extension (sleep banking) attenuates the negative effects of sleep loss on performance [29], whereas sleep restriction exacerbates these effects [6,30,31]. However, how and whether prior sleep history affects the changes in sleep structure and SWA induced by total sleep deprivation has not been studied extensively.…”