[en] OBJECTIVE: Even though wakefulness at night leads to profound performance deterioration and is regularly experienced by shift workers, its cerebral correlates remain virtually unexplored. METHODS: We assessed brain activity in young healthy adults during a vigilant attention task under high and low sleep pressure during night-time, coinciding with strongest circadian sleep drive. We examined sleep-loss-related attentional vulnerability by considering a PERIOD3 polymorphism presumably impacting on sleep homeostasis. RESULTS: Our results link higher sleep-loss-related attentional vulnerability to cortical and subcortical deactivation patterns during slow reaction times (i.e., suboptimal vigilant attention). Concomitantly, thalamic regions were progressively less recruited with time-on-task and functionally less connected to task-related and arousal-promoting brain regions in those volunteers showing higher attentional instability in their behavior. The data further suggest that the latter is linked to shifts into a task-inactive default-mode network in between task-relevant stimulus occurrence. INTERPRETATION: We provide a multifaceted view on cerebral correlates of sleep loss at night and propose that genetic predisposition entails differential cerebral coping mechanisms, potentially compromising adequate performance during night work.
Wright KP, Lowry CA, Lebourgeois MK,. Circadian and wakefulness-sleep modulation of cognition in humans. Front Mol Neurosci 2012; 5: 50.
Dijk DJ, Czeisler CA,. Paradoxical timing of the circadian rhythm of sleep propensity serves to consolidate sleep and wakefulness in humans. Neurosci Lett 1994; 166: 63-68.
Borbely AA,. A two process model of sleep regulation. Hum Neurobiol 1982; 1: 195-204.
Doran SM, Van Dongen HP, Dinges DF,. Sustained attention performance during sleep deprivation: evidence of state instability. Arch Ital Biol 2001; 139: 253-267.
Lim J, Dinges DF,. Sleep deprivation and vigilant attention. Ann N Y Acad Sci 2008; 1129: 305-322.
Graw P, Krauchi K, Knoblauch V, et al., Circadian and wake-dependent modulation of fastest and slowest reaction times during the psychomotor vigilance task. Physiol Behav 2004; 80: 695-701.
Van Dongen HP, Baynard MD, Maislin G, Dinges DF,. Systematic interindividual differences in neurobehavioral impairment from sleep loss: evidence of trait-like differential vulnerability. Sleep 2004; 27: 423-433.
Lo JC, Groeger JA, Santhi N, et al., Effects of partial and acute total sleep deprivation on performance across cognitive domains, individuals and circadian phase. PLoS ONE 2012; 7: e45987.
Maire M, Reichert CF, Gabel V, et al., Sleep ability mediates individual differences in the vulnerability to sleep loss: evidence from a PER3 polymorphism. Cortex 2014; 52: 47-59.
Groeger JA, Viola AU, Lo JC, et al., Early morning executive functioning during sleep deprivation is compromised by a PERIOD3 polymorphism. Sleep 2008; 31: 1159-1167.
Viola AU, Archer SN, James LM, et al., PER3 polymorphism predicts sleep structure and waking performance. Curr Biol 2007; 17: 613-618.
Dijk DJ, Archer SN,. PERIOD3, circadian phenotypes, and sleep homeostasis. Sleep Med Rev 2010; 14: 151-160.
Goel N, Banks S, Mignot E, Dinges DF,. PER3 polymorphism predicts cumulative sleep homeostatic but not neurobehavioral changes to chronic partial sleep deprivation. PLoS ONE 2009; 4: e5874.
Vandewalle G, Archer SN, Wuillaume C, et al., Functional magnetic resonance imaging-assessed brain responses during an executive task depend on interaction of sleep homeostasis, circadian phase, and PER3 genotype. J Neurosci 2009; 29: 7948-7956.
Chee MW, Asplund CL,. Neuroimaging of attention and alterations of processing capacity in sleep-deprived persons. In:, Nofzinger EA, Maquet P, Thorpy MJ, eds. Neuroimaging of Sleep and Sleep Disorders. Cambridge, UK: Cambridge University Press, 2013: 137-144.
Dorrian J, Rogers N, Dinges D,. Psychomotor vigilance performance: a neurocognitive assay sensitive to sleep loss. In:, Kushida C, ed. Sleep Deprivation: Clinical Issues, Pharmacology, and Sleep Loss Effects. New York: Marcel Dekker, 2005: 39-70.
Cajochen C, Knoblauch V, Krauchi K, et al., Dynamics of frontal EEG activity, sleepiness and body temperature under high and low sleep pressure. Neuroreport 2001; 12 (10): 2277-81.
Drummond SP, Bischoff-Grethe A, Dinges DF, et al., The neural basis of the psychomotor vigilance task. Sleep 2005; 28: 1059-1068.
Weissman DH, Roberts KC, Visscher KM, Woldorff MG,. The neural bases of momentary lapses in attention. Nat Neurosci 2006; 9: 971-978.
Maire M, Reichert CF, Gabel V, et al., Time-on-task decrement in vigilance is modulated by inter-individual vulnerability to homeostatic sleep pressure manipulation. Front Behav Neurosci 2014; 8: 59.
Knoblauch V, Krauchi K, Renz C, et al., Homeostatic control of slow-wave and spindle frequency activity during human sleep: effect of differential sleep pressure and brain topography. Cereb Cortex 2002; 12: 1092-1100.
Dinges DF, Powell JW,. Microcomputer analyses of performance on a portable, simple visual RT task during sustained operations. Behav Res Methods Instrum. Comput 1985; 17: 625-655.
Akerstedt T, Gillberg M,. Subjective and objective sleepiness in the active individual. Int J Neurosci 1990; 52: 29-37.
Kenward MG, Roger JH,. Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 1997; 53: 983-997.
Basner M, Dinges DF,. Maximizing sensitivity of the psychomotor vigilance test (PVT) to sleep loss. Sleep 2011; 34: 581-591.
Schmidt C, Collette F, Leclercq Y, et al., Homeostatic sleep pressure and responses to sustained attention in the suprachiasmatic area. Science 2009; 324: 516-519.
Muto V, Shaffii-le Bourdiec A, Matarazzo L, et al., Influence of acute sleep loss on the neural correlates of alerting, orientating and executive attention components. J Sleep Res 2012; 21: 648-658.
Tomasi D, Wang RL, Telang F, et al., Impairment of attentional networks after 1 night of sleep deprivation. Cereb Cortex 2009; 19: 233-240.
Thomas M, Sing H, Belenky G, et al., Neural basis of alertness and cognitive performance impairments during sleepiness. I. Effects of 24 h of sleep deprivation on waking human regional brain activity. J Sleep Res 2000; 9: 335-352.
Laird AR, Eickhoff SB, Li K, et al., Investigating the functional heterogeneity of the default mode network using coordinate-based meta-analytic modeling. J Neurosci 2009; 29: 14496-14505.
Gujar N, Yoo SS, Hu P, Walker MP,. The unrested resting brain: sleep deprivation alters activity within the default-mode network. J Cogn Neurosci 2010; 22: 1637-1648.
Leech R, Kamourieh S, Beckmann CF, Sharp DJ,. Fractionating the default mode network: distinct contributions of the ventral and dorsal posterior cingulate cortex to cognitive control. J Neurosci 2011; 31: 3217-3224.
Fransson P, Marrelec G,. The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: evidence from a partial correlation network analysis. Neuroimage 2008; 42: 1178-1184.
Gitelman DR, Penny WD, Ashburner J, Friston KJ,. Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. Neuroimage 2003; 19: 200-207.
O'Reilly JX, Woolrich MW, Behrens TE, et al., Tools of the trade: psychophysiological interactions and functional connectivity. Soc Cogn Affect Neurosci 2012; 7: 604-609.
Maquet P, Degueldre C, Delfiore G, et al., Functional neuroanatomy of human slow wave sleep. J Neurosci 1997; 17: 2807-2812.
Henson R, Friston K,. Convolution models for fMRI. In:, Penny WD, Friston KJ, Ashburner JT, eds. Statistical Parametrical Mapping: The Analysis of Functional Brain Images, 1st ed. New York: Academic, 2007: 178-192.
Mantini D, Vanduffel W,. Emerging roles of the brain's default network. Neuroscientist 2013; 19: 76-87.
Buckner RL, Andrews-Hanna JR, Schacter DL,. The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 2008; 1124: 1-38.
Chee MW, Tan JC,. Lapsing when sleep deprived: neural activation characteristics of resistant and vulnerable individuals. Neuroimage 2010; 51: 835-843.
Chee MW, Tan JC, Zheng H, et al., Lapsing during sleep deprivation is associated with distributed changes in brain activation. J Neurosci 2008; 28: 5519-5528.
Czisch M, Wehrle R, Harsay HA, et al., On the need of objective vigilance monitoring: effects of sleep loss on target detection and task-negative activity using combined EEG/fMRI. Front Neurol 2012; 3: 67.
Drummond SP, Gillin JC, Brown GG,. Increased cerebral response during a divided attention task following sleep deprivation. J Sleep Res 2001; 10: 85-92.
Drummond SP, Brown GG, Gillin JC, et al., Altered brain response to verbal learning following sleep deprivation. Nature 2000; 403: 655-657.
Portas CM, Rees G, Howseman AM, et al., A specific role for the thalamus in mediating the interaction of attention and arousal in humans. J Neurosci 1998; 18: 8979-8989.
Steriade M, Llinas RR,. The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 1988; 68: 649-742.
Sonuga-Barke EJ, Castellanos FX,. Spontaneous attentional fluctuations in impaired states and pathological conditions: a neurobiological hypothesis. Neurosci Biobehav Rev 2007; 31: 977-986.
Asplund CL, Chee MW,. Time-on-task and sleep deprivation effects are evidenced in overlapping brain areas. Neuroimage 2013; 82: 326-335.
Buysse DJ, Reynolds CF 3rd, Monk TH, et al., The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res 1989; 28: 193-213.
Johns MW,. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep 1991; 14: 540-545.
Horne JA, Östberg O,. A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int J Chronobiol 1976; 4: 97-110.
Roenneberg T, Wirz-Justice A, Merrow M,. Life between clocks: daily temporal patterns of human chronotypes. J Biol Rhythms 2003; 18: 80-90.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.
