Sleep ability mediates individual differences in the vulnerability to sleep loss: evidence from a PER3 polymorphism.
Sleep deprivation is highly prevalent in our 24/7 society with harmful consequences on daytime functioning on the individual level. Genetically determined, trait-like vulnerability contributes to prominent inter-individual variability in the behavioral responses to sleep loss and adverse circadian phase. We aimed at investigating the effects of differential sleep pressure levels (high vs low) on the circadian modulation of neurobehavioral performance, sleepiness correlates, and nap sleep in individuals genotyped for a polymorphism in the clock gene PERIOD3. Fourteen homozygous long (PER3(5/5)) and 15 homozygous short (PER3(4/4)) allele carriers underwent both a 40-h sleep deprivation and multiple nap protocol under controlled laboratory conditions. We compared genotypes regarding subjective and ocular correlates of sleepiness, unintentional sleep episodes as well as psychomotor vigilance during both protocols. Nap sleep was monitored by polysomnography and visually scored according to standard criteria. The detrimental effects of high sleep pressure on sleepiness correlates and psychomotor vigilance were more pronounced in PER3(5/5) than PER3(4/4) carriers. Under low sleep pressure, both groups showed similar circadian time courses. Concomitantly, nap sleep efficiency and subjective sleep quality across all naps tended to be higher in the more vulnerable PER3(5/5) carriers. In addition, PER3-dependent sleep-loss-related attentional lapses were mediated by sleep efficiency across the circadian cycle. Our data corroborate a greater detrimental impact of sleep deprivation in PER3(5/5) compared to PER3(4/4) carriers. They further suggest that the group with greater attentional performance impairment due to sleep deprivation (PER3(5/5) carriers) is superior at initiating sleep over the 24-h cycle. This higher sleep ability may mirror a faster sleep pressure build-up between the multiple sleep opportunities and thus a greater flexibility in sleep initiation. Finally, our data show that this higher nap sleep efficiency is positively related to attentional failures under sleep loss conditions and might thus be used as a marker for inter-individual vulnerability to elevated sleep pressure.
Centre for Chronobiology, Psychiatric University Hospital of the University of Basel, Basel, Switzerland.
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Maire
Centre for Chronobiology, Psychiatric University Hospital of the University of Basel, Basel, Switzerland.
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Reichert
Centre for Chronobiology, Psychiatric University Hospital of the University of Basel, Basel, Switzerland.
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Gabel
Centre for Chronobiology, Psychiatric University Hospital of the University of Basel, Basel, Switzerland.
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Viola
Respiratory Medicine, Department of Internal Medicine, University Hospital Basel, Basel, Switzerland.
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Strobel
Centre for Chronobiology, Psychiatric University Hospital of the University of Basel, Basel, Switzerland.
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Krebs
Institute of Pharmacology and Toxicology, University of Zürich, Zürich, Switzerland; Clinical Research Priority Program "Sleep & Health", University of Zürich, Zürich, Switzerland.
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Landolt
Institute of Pharmacology and Toxicology, University of Zürich, Zürich, Switzerland.
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Bachmann
Centre for Chronobiology, Psychiatric University Hospital of the University of Basel, Basel, Switzerland. Electronic address: christian.cajochen@upkbs.ch.
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Cajochen
Centre for Chronobiology, Psychiatric University Hospital of the University of Basel, Basel, Switzerland.
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Schmidt
D000328:Adult; D000483:Alleles; D001288:Attention / Q000502:physiology; D002940:Circadian Rhythm / Q000235:genetics*; D005260:Female; D056726:Genetic Association Studies; D005838:Genotype; D006801:Humans; D007206:Individuality; D008297:Male; D056950:Period Circadian Proteins / Q000235:genetics*; D020641:Polymorphism, Single Nucleotide; D017286:Polysomnography; D011597:Psychomotor Performance / Q000502:physiology; D012890:Sleep / Q000235:genetics*; D012892:Sleep Deprivation / Q000235:genetics*; D055815:Young Adult
C512644:PER3 protein, human; D056950:Period Circadian Proteins
Attentional performance; Circadian phase; Inter-individual variability; Nap sleep; PER3 VNTR polymorphism; Sleep deprivation