Dynamic circadian modulation in a biomathematical model for the effects of sleep and sleep loss on waking neurobehavioral performance.

Recent experimental observations and theoretical advances have indicated that the homeostatic equilibrium for sleep/wake regulation--and thereby sensitivity to neurobehavioral impairment from sleep loss--is modulated by prior sleep/wake history. This phenomenon was predicted by a biomathematical model developed to explain changes in neurobehavioral performance across days in laboratory studies of total sleep deprivation and sustained sleep restriction. The present paper focuses on the dynamics of neurobehavioral performance within days in this biomathematical model of fatigue. Without increasing the number of model parameters, the model was updated by incorporating time-dependence in the amplitude of the circadian modulation of performance. The updated model was calibrated using a large dataset from three laboratory experiments on psychomotor vigilance test (PVT) performance, under conditions of sleep loss and circadian misalignment; and validated using another large dataset from three different laboratory experiments. The time-dependence of circadian amplitude resulted in improved goodness-of-fit in night shift schedules, nap sleep scenarios, and recovery from prior sleep loss. The updated model predicts that the homeostatic equilibrium for sleep/wake regulation--and thus sensitivity to sleep loss--depends not only on the duration but also on the circadian timing of prior sleep. This novel theoretical insight has important implications for predicting operator alertness during work schedules involving circadian misalignment such as night shift work.

[1]  G. Gunzelmann,et al.  Deconstructing and reconstructing cognitive performance in sleep deprivation. , 2013, Sleep medicine reviews.

[2]  Suresh Rangan,et al.  Quantifying fatigue risk in model-based fatigue risk management. , 2013, Aviation, space, and environmental medicine.

[3]  D. Grant,et al.  The Genetic Basis of Sleep and Sleep Disorders: Individual differences in sleep duration and responses to sleep loss , 2013 .

[4]  M. Thorpy,et al.  The Genetic Basis of Sleep and Sleep Disorders: List of Abbreviations , 2013 .

[5]  Emma L. Arbon,et al.  Effects of Partial and Acute Total Sleep Deprivation on Performance across Cognitive Domains, Individuals and Circadian Phase , 2012, PloS one.

[6]  Gerald Matthews,et al.  The Handbook of Operator Fatigue , 2012 .

[7]  Peter A Robinson,et al.  Exploring Sleepiness and Entrainment on Permanent Shift Schedules in a Physiologically Based Model , 2012, Journal of biological rhythms.

[8]  Gregory Belenky,et al.  A local, bottom-up perspective on sleep deprivation and neurobehavioral performance. , 2011, Current topics in medicinal chemistry.

[9]  C. Sargent,et al.  Sleep, wake and phase dependent changes in neurobehavioral function under forced desynchrony. , 2011, Sleep.

[10]  Gregory Belenky,et al.  The efficacy of a restart break for recycling with optimal performance depends critically on circadian timing. , 2011, Sleep.

[11]  Andrew Gelman,et al.  Handbook of Markov Chain Monte Carlo , 2011 .

[12]  D. Dinges,et al.  Maximizing sensitivity of the psychomotor vigilance test (PVT) to sleep loss. , 2011, Sleep.

[13]  J. Krueger,et al.  The ATP-cytokine-adenosine hypothesis: How the brain translates past activity into sleep , 2011 .

[14]  G. Belenky,et al.  Investigating the temporal dynamics and underlying mechanisms of cognitive fatigue. , 2011 .

[15]  H. V. Dongen,et al.  Cognitive effects of sleepiness , 2011 .

[16]  M. Thorpy,et al.  Sleepiness : causes, consequences, and treatment , 2011 .

[17]  Steven R. Hursh,et al.  Chapter 66 – Fatigue and Performance Modeling , 2010 .

[18]  J. Krueger,et al.  ATP and the purine type 2 X7 receptor affect sleep. , 2010, Journal of applied physiology.

[19]  D. Dinges,et al.  Neurobehavioral dynamics following chronic sleep restriction: dose-response effects of one night for recovery. , 2010, Sleep.

[20]  Hans P A Van Dongen,et al.  Time of day effects on neurobehavioral performance during chronic sleep restriction. , 2010, Aviation, space, and environmental medicine.

[21]  T. Balkin,et al.  Current Approaches and Challenges to Development of an Individualized Sleep and Performance Prediction Model , 2010 .

[22]  T. Balkin,et al.  Sleep history affects task acquisition during subsequent sleep restriction and recovery , 2009, Journal of sleep research.

[23]  P. Whitney,et al.  Effects of sleep deprivation on dissociated components of executive functioning. , 2010, Sleep.

[24]  T. Balkin,et al.  Banking sleep: realization of benefits during subsequent sleep restriction and recovery. , 2009, Sleep.

[25]  E. Challet,et al.  Brain Clocks: From the Suprachiasmatic Nuclei to a Cerebral Network , 2009, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[26]  D. Dinges,et al.  A new mathematical model for the homeostatic effects of sleep loss on neurobehavioral performance. , 2009, Journal of theoretical biology.

[27]  Peter Mccauley,et al.  Fatigue Risk Management: Modeling the Sleep/Wake-Based Dynamics of Performance , 2009 .

[28]  J. Panksepp,et al.  Sleep as a fundamental property of neuronal assemblies , 2008, Nature Reviews Neuroscience.

[29]  Hans P A Van Dongen,et al.  Response Surface Mapping of Neurobehavioral Performance: Testing the Feasibility of Split Sleep Schedules for Space Operations. , 2008, Acta astronautica.

[30]  D. Dinges,et al.  Sleep Deprivation and Vigilant Attention , 2008, Annals of the New York Academy of Sciences.

[31]  T. Åkerstedt,et al.  Accounting for Partial Sleep Deprivation and Cumulative Sleepiness in the Three‐Process Model of Alertness Regulation , 2008, Chronobiology international.

[32]  Glenn Gunzelmann,et al.  Uncovering Physiologic Mechanisms of Circadian Rhythms and Sleep/Wake Regulation through Mathematical Modeling , 2007, Journal of biological rhythms.

[33]  H. Haas,et al.  Sleep Deprivation Increases A1 Adenosine Receptor Binding in the Human Brain: A Positron Emission Tomography Study , 2007, The Journal of Neuroscience.

[34]  J. Krueger,et al.  Unilateral cortical application of interleukin-1β (IL1β) induces asymmetry in fos, IL1β and nerve growth factor immunoreactivity: Implications for sleep regulation , 2007, Brain Research.

[35]  Joshua J Gooley,et al.  Neurobiology of the Sleep-Wake Cycle: Sleep Architecture, Circadian Regulation, and Regulatory Feedback , 2006, Journal of biological rhythms.

[36]  Heikki Haario,et al.  DRAM: Efficient adaptive MCMC , 2006, Stat. Comput..

[37]  J. Krueger,et al.  Unilateral cortical application of tumor necrosis factor α induces asymmetry in Fos- and interleukin-1β-immunoreactive cells within the corticothalamic projection , 2005, Brain Research.

[38]  Elizabeth B. Klerman,et al.  Comparison of Amplitude Recovery Dynamics of Two Limit Cycle Oscillator Models of the Human Circadian Pacemaker , 2005, Chronobiology international.

[39]  D. Dinges,et al.  Psychomotor Vigilance Performance: Neurocognitive Assay Sensitive to Sleep Loss , 2004 .

[40]  T. Balkin,et al.  Modafinil vs. caffeine: effects on fatigue during sleep deprivation. , 2004, Aviation, space, and environmental medicine.

[41]  Hans P. A. Van Dongen,et al.  Comparison of mathematical model predictions to experimental data of fatigue and performance , 2004 .

[42]  David F Dinges,et al.  Critical research issues in development of biomathematical models of fatigue and performance. , 2004, Aviation, space, and environmental medicine.

[43]  Gregory Belenky,et al.  Modulating the homeostatic process to predict performance during chronic sleep restriction. , 2004, Aviation, space, and environmental medicine.

[44]  T. Balkin,et al.  Fatigue models for applied research in warfighting. , 2004, Aviation, space, and environmental medicine.

[45]  Adam Fletcher,et al.  A model to predict work-related fatigue based on hours of work. , 2004, Aviation, space, and environmental medicine.

[46]  D. Dinges,et al.  Summary of the key features of seven biomathematical models of human fatigue and performance. , 2004, Aviation, space, and environmental medicine.

[47]  Peter Achermann,et al.  Simulation of daytime vigilance by the additive interaction of a homeostatic and a circadian process , 1994, Biological Cybernetics.

[48]  Erik Olofsen,et al.  Mixed-model regression analysis and dealing with interindividual differences. , 2004, Methods in enzymology.

[49]  R. Kronauer,et al.  Comparison of Mathematical Model Predictions to Experimental Data of Fatigue and Performance , 2004 .

[50]  Mariska J Vansteensel,et al.  Sleep states alter activity of suprachiasmatic nucleus neurons , 2003, Nature Neuroscience.

[51]  D. Dinges,et al.  Investigating the interaction between the homeostatic and circadian processes of sleep–wake regulation for the prediction of waking neurobehavioural performance , 2003, Journal of sleep research.

[52]  D. Dinges,et al.  The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. , 2003, Sleep.

[53]  Maria L. Thomas,et al.  Patterns of performance degradation and restoration during sleep restriction and subsequent recovery: a sleep dose‐response study , 2003, Journal of sleep research.

[54]  Hans P. A. Van Dongen,et al.  Sleep debt and cumulative excess wakefulness , 2003 .

[55]  F. Netter,et al.  Supplemental References , 2002, We Came Naked and Barefoot.

[56]  S. Doran,et al.  Sustained attention performance during sleep deprivation: evidence of state instability. , 2001, Archives italiennes de biologie.

[57]  R. Kronauer,et al.  Interactive Mathematical Models of Subjective Alertness and Cognitive Throughput in Humans , 1999, Journal of biological rhythms.

[58]  P. Achermann,et al.  Sleep homeostasis and models of sleep regulation. , 1999, Journal of biological rhythms.

[59]  T. Roth,et al.  A two-week sleep extension in sleepy normals. , 1996, Sleep.

[60]  A A Borbély,et al.  Homeostatic sleep regulation in habitual short sleepers and long sleepers. , 1996, The American journal of physiology.

[61]  J. Krueger,et al.  A neuronal group theory of sleep function , 1993, Journal of sleep research.

[62]  DM Edgar,et al.  Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  D. Dijk,et al.  Circadian and sleep/wake dependent aspects of subjective alertness and cognitive performance , 1992, Journal of sleep research.

[64]  Daniel L. Schacter,et al.  Sleep and Cognition , 1990 .

[65]  David F. Dinges,et al.  Are you awake? Cognitive performance and reverie during the hypnopompic state. , 1990 .

[66]  M. Kryger,et al.  Principles And Practice Of Sleep Medicine , 1989 .

[67]  T. Roth,et al.  Sleep extension in sleepy and alert normals. , 1989, Sleep.

[68]  M. Kryger,et al.  Principles and Practice of Sleep Medicine , 1989 .

[69]  S. Daan,et al.  Timing of human sleep: recovery process gated by a circadian pacemaker. , 1984, The American journal of physiology.

[70]  A. Borbély A two process model of sleep regulation. , 1982, Human neurobiology.