Sleep Deprivation Diminishes Attentional Control Effectiveness and Impairs Flexible Adaptation to Changing Conditions

Abstract

Insufficient sleep is a global public health problem resulting in catastrophic accidents, increased mortality, and hundreds of billions of dollars in lost productivity. Yet the effect of sleep deprivation (SD) on decision making and performance is often underestimated by fatigued individuals and is only beginning to be understood by scientists. The deleterious impact of SD is frequently attributed to lapses in vigilant attention, but this account fails to explain many SD-related problems, such as loss of situational awareness and perseveration. Using a laboratory study protocol, we show that SD individuals can maintain information in the focus of attention and anticipate likely correct responses, but their use of such a top-down attentional strategy is less effective at preventing errors caused by competing responses. Moreover, when the task environment requires flexibility, performance under SD suffers dramatically. The impairment in flexible shifting of attentional control we observed is distinct from lapses in vigilant attention, as corroborated by the specificity of the influence of a genetic biomarker, the dopaminergic polymorphism DRD2 C957T. Reduced effectiveness of top-down attentional control under SD, especially when conditions require flexibility, helps to explain maladaptive performance that is not readily explained by lapses in vigilant attention.

Mouse Gambling Task reveals differential effects of acute sleep debt on decision-making and associated neurochemical changes

“…Besides, and more importantly, these ASD-related behavioral modifications were associated with a decrease of cognitive flexibility. These results match previous ones showing that ASD is responsible for perseverative behaviors in humans [ 6 , 8 , 9 ]. Our control experiments ruled out the effect of stress related to ASD, as plasma corticosterone measures did not show any difference between control and ASD mice.…”

The circadian clock regulates cisplatin-induced toxicity and tumor regression in melanoma mouse and human models

“…Healthy human subjects with normal sleep were recruited to the Sleep and Performance Research Center at Washington State University Spokane. Subjects met inclusion criteria described by us previously [ 66 ]. They had no current cancer or history of cancer, chemotherapy treatment, or radiation treatment.…”

Clinical and Experimental Human Sleep-Wake Pharmacogenetics

“…A recent study confirmed that homozygous carriers of the C allele of the DRD2 c.957C>T polymorphism are impaired by sleep deprivation in vigilant attention (Whitney et al, 2017). Remarkably, however, the same individuals were resilient to the effects of prolonged waking on reversal learning, a measure of cognitive flexibility (Whitney et al, 2017). Consistent with the notion that the consequences of sleep deprivation are trait-like but task-specific, the data collectively suggest that striato-thalamo-cortical dopaminergic pathways contribute to the regulation of neurophysiological and neurobehavioral consequences of sleep loss in humans.…”

“…More specifically, individuals homozygous for the C allele of DRD2 and the 10R allele of DAT1 were more severely affected with attentional lapses after 40 hours of wakefulness than other genotypic variants. A recent study confirmed that homozygous carriers of the C allele of the DRD2 c.957C>T polymorphism are impaired by sleep deprivation in vigilant attention (Whitney et al, 2017). Remarkably, however, the same individuals were resilient to the effects of prolonged waking on reversal learning, a measure of cognitive flexibility (Whitney et al, 2017).…”

“…Taken together, the systematic human pharmacogenetic dissection of adenosine-associated loci and dopamine-related loci demonstrates that the distinct signaling pathways differently modulate the response to sleep loss and wake-promoting agents on neurophysiological markers of sleep need and neurobehavioral deficits (Figure 3). The ADORA2A c.1976T>C polymorphism (Rétey et al, 2007;Rupp et al, 2013), an ADORA2A haplotype (Bodenmann et al, 2012), the DAT1 VNTR polymorphism (Holst et al, 2014;Satterfield et al, 2017), and the DRD2 c.957C>T polymorphism (Holst et al, 2017;Whitney et al, 2017) modulate both, EEG and distinct behavioral markers of elevated sleep need and the effects of caffeine and modafinil on these markers. The findings suggest that striatal iMSNs, which co-express high densities of adenosine A2A and dopamine D2 receptors mediate these consequences of sleep loss.…”