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

Sleep

Volumn 36, Issue 12, 2013, Pages 1987-1997

  McCauley, Peter ^a,b   Kalachev, Leonid V ^b   Mollicone, Daniel J ^c   Banks, Siobhan ^d   Dinges, David F ^e   Van Dongen, Hans P A ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MONTANA   (United States)

^c Pulsar Informatics Inc   (United States)

^d UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Alertness; Allostatic regulation; Dynamic circadian amplitude; Fatigue and performance models; Markov chain Monte Carlo (MCMC); Model based fatigue risk management; Nonlinear interaction; Sigmoidal dynamics; Sleep deprivation; Sleep homeostasis

Indexed keywords

ADULT; ALERTNESS; AROUSAL; ARTICLE; CIRCADIAN RHYTHM; COGNITION; DAY LENGTH; FATIGUE; HOMEOSTASIS; HUMAN; HUMAN EXPERIMENT; MATHEMATICAL MODEL; NIGHT SLEEP; NIGHT WORK; NORMAL HUMAN; PRIORITY JOURNAL; PSYCHOMOTOR ACTIVITY; SHIFT WORKER; SLEEP DEPRIVATION; SLEEP TIME; SLEEP WAKING CYCLE; TASK PERFORMANCE; WAKEFULNESS; WORK SCHEDULE;

ALERTNESS; ALLOSTATIC REGULATION; DYNAMIC CIRCADIAN AMPLITUDE; FATIGUE AND PERFORMANCE MODELS; MARKOV CHAIN MONTE CARLO (MCMC); MODEL-BASED FATIGUE RISK MANAGEMENT; NONLINEAR INTERACTION; SIGMOIDAL DYNAMICS; SLEEP DEPRIVATION; SLEEP HOMEOSTASIS;

CIRCADIAN RHYTHM; HUMANS; MODELS, BIOLOGICAL; PSYCHOMOTOR PERFORMANCE; SLEEP; SLEEP DEPRIVATION; SLEEP DISORDERS, CIRCADIAN RHYTHM; TIME FACTORS; YOUNG ADULT;

EID: 84889034835     PISSN: 01618105     EISSN: 15509109     Source Type: Journal    
DOI: 10.5665/sleep.3246     Document Type: Article

References (67)

1. Borbély AA. A two process model of sleep regulation. Hum Neurobiol 1982;1:195-204.
2. Daan S, Beersma DGM, Borbély AA. Timing of human sleep: recovery process gated by a circadian pacemaker. Am J Physiol 1984;246: R161-78.
3. Hursh SR, Van Dongen HPA. Fatigue and performance modeling. In: Kryger MH, Roth T, Dement WC, eds. Principles and practice of sleep medicine, 5th ed. St. Louis, MO: Elsevier Saunders; 2010:745-52.
4. Van Dongen HPA, Belenky G. Model-based fatigue risk management. In: Matthews G, Desmond PA, Neubauer C, Hancock PA, eds. The handbook of operator fatigue. Farnham, England: Ashgate Publishing; 2012:487-506.
5. McCauley P, Kalachev LV, Smith AD, Belenky G, Dinges DF, Van Dongen HPA. A new mathematical model for the homeostatic effects of sleep loss on neurobehavioral performance. J Theor Biol 2009;256:227-39.
6. Belenky G, Wesensten NJ, Thorne DR, et al. Patterns of performance degradation and restoration during sleep restriction and subsequent recovery: a sleep dose-response study. J Sleep Res 2003;12:1-12.
7. Van Dongen HPA, Maislin G, Mullington JM, Dinges DF. The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. Sleep 2003;26:117-28.
8. Aeschbach D, Cajochen C, Landolt H, Borbély AA. Homeostatic sleep regulation in habitual short sleepers and long sleepers. Am J Physiol 1996;270:R41-53.
9. Grant DA, Van Dongen HPA. Individual differences in sleep duration and responses to sleep loss. In: Shaw PJ, Tafti M, Thorpy MJ, eds. The genetic basis of sleep and sleep disorders. Cambridge, England: Cambridge University Press; in press.
10. McCauley P, McCauley ME, Van Dongen HPA. Mathematical model of sleep loss. Sleep Res Soc Bull 2009;15:17-8.
11. Rupp TL, Wesensten NJ, Bliese PD, Balkin TJ. Banking sleep: realization of benefits during subsequent sleep restriction and recovery. Sleep 2009;32:311-21.
12. Rupp TL, Wesensten NJ, Balkin TJ. Sleep history affects task acquisition during subsequent sleep restriction and recovery. J Sleep Res 2010;19:289-97.
13. Van Dongen HPA, Dinges DF. Sleep debt and cumulative excess wakefulness. Sleep 2003;26:249.
14. Dijk DJ, Duffy JF, Czeisler CA. Circadian and sleep/wake dependent aspects of subjective alertness and cognitive performance. J Sleep Res 1992;1:112-7.
15. Van Dongen HPA, Dinges DF. Investigating the interaction between the homeostatic and circadian processes of sleep-wake regulation for the prediction of waking neurobehavioural performance. J Sleep Res 2003;12:181-7.
16. Mollicone DJ, Van Dongen HPA, Rogers NL, Banks S, Dinges DF. Time of day effects on neurobehavioral performance during chronic sleep restriction. Aviat Space Environ Med 2010;81:735-44.
17. Achermann P, Borbély AA. Simulation of daytime vigilance by the additive interaction of a homeostatic and a circadian process. Biol Cybern 1994;71:115-21.
18. Jewett ME, Kronauer RE. Interactive mathematical models of subjective alertness and cognitive throughput in humans. J Biol Rhythms 1999;14:588-97.
19. Hursh SR, Redmond DP, Johnson ML, et al. Fatigue models for applied research in warfighting. Aviat Space Environ Med 2004;75:A44-53.
20. Johnson ML, Belenky G, Redmond DP, et al. Modulating the homeostatic process to predict performance during chronic sleep restriction. Aviat Space Environ Med 2004;75:A141-6.
21. Roach GD, Fletcher A, Dawson D. A model to predict work-related fatigue based on hours of work. Aviat Space Environ Med 2004;75:A61-9.
22. Åkerstedt T, Ingre M, Kecklund G, Folkard S, Axelsson J. Accounting for partial sleep deprivation and cumulative sleepiness in the three-process model of alertness regulation. Chronobiol Int 2008;25:309-19.
23. Postnova S, Layden A, Robinson PA, Phillips AJK, Abeysuriya RG. Exploring sleepiness and entrainment on permanent shift schedules in a physiologically based model. J Biol Rhythms 2012;27:91-102.
24. Borbély AA, Achermann P. Sleep homeostasis and models of sleep regulation. J Biol Rhythms 1999;14:557-68.
25. Van Dongen HPA, Belenky G, Vila BJ. The efficacy of a restart break for recycling with optimal performance depends critically on circadian timing. Sleep 2011;34:917-29.
26. DeBoer T, Vansteensel MJ, Détári L, Meijer JH. Sleep states alter activity of suprachiasmatic nucleus neurons. Nat Neurosci 2003;6:1086-90.
27. 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.
28. Indic P, Forger DB, St. Hilaire MA, et al. Comparison of amplitude recovery dynamics of two limit cycle oscillator models of the human circadian pacemaker. Chronobiol Int 2005;22:613-29.
29. Lim J, Dinges DF. Sleep deprivation and vigilant attention. Ann N Y Acad Sci 2008;1129:305-22.
30. Basner M, Dinges DF. Maximizing sensitivity of the psychomotor vigilance test (PVT) to sleep loss. Sleep 2011;34:581-91.
31. Dinges DF. Are you awake? Cognitive performance and reverie during the hypnopompic state. In: Bootzin RR, Kihlstrom JF, Schacter DL, eds. Sleep and cognition. Washington, DC: American Psychological Association; 1990:159-75.
32. Mollicone DJ, Van Dongen HPA, Rogers NL, Dinges DF. Response surface mapping of neurobehavioral performance: testing the feasibility of split sleep schedules for space operations. Act Astronaut 2008;63:833-40.
33. Tucker AM, Whitney P, Belenky G, Hinson JM, Van Dongen HPA. Effects of sleep deprivation on dissociated components of executive functioning. Sleep 2010;33:47-57.
34. Doran SM, Van Dongen HPA, Dinges DF. Sustained attention performance during sleep deprivation: evidence of state instability. Arch Ital Biol 2001;139:253-67.
35. Banks S, Van Dongen HPA, Maislin G, Dinges DF. Neurobehavioral dynamics following chronic sleep restriction: dose-response effects of one night for recovery. Sleep 2010;33:1013-26.
36. Dorrian J, Rogers NL, Dinges DF. Psychomotor vigilance performance: neurocognitive assay sensitive to sleep loss. In: Kushida CA, ed. Sleep deprivation. Clinical issues, pharmacology, and sleep loss effects. New York, NY: Marcel Dekker; 2005:39-70.
37. Haario H, Laine M, Mira A, Saksman E. DRAM: efficient adaptive MCMC. Stat Comp 2006;16:339-54.
38. Brooks S, Gelman A, Jones GL, Meng XL, eds. Handbook on Markov Chain Monte Carlo. London, UK: CRC Press; 2011.
39. Olofsen E, Van Dongen HPA, Mott CG, Balkin TJ, Terman D. Current approaches and challenges to development of an individualized sleep and performance prediction model. Open Sleep J 2010;3:24-43.
40. Van Dongen HPA. Comparison of mathematical model predictions to experimental data of fatigue and performance. Aviat Space Environ Med 2004;75:A15-36.
41. Roehrs T, Timms V, Zwyghuizen-Doorenbos A, Roth T. Sleep extension in sleepy and alert normals. Sleep 1989;12:449-57.
42. Roehrs T, Shore E, Papineau K, Rosenthal L, Roth T. A two-week sleep extension in sleepy normals. Sleep 1996;19:576-82.
43. Zhou X, Ferguson SA, Matthews RW, et al. Sleep, wake and phase dependent changes in neurobehavioral function under forced desynchrony. Sleep 2011;34:931-41.
44. Jewett ME, Dijk DJ, Kronauer RE, Czeisler CA. Sigmoidal decline of homeostatic component in subjective alertness and cognitive throughput. Sleep 1999;22:S94-5.
45. Krueger JM, Taishi P, De A, et al. ATP and the purine type 2 X7 receptor affect sleep. J Appl Physiol 2010;109:1318-27.
46. Sengupta P, Roy S, Krueger JM. The ATP-cytokine-adenosine hypothesis: how the brain translates past activity into sleep. Sleep Biol Rhythms 2011;9(Suppl. 1):29-33.
47. Krueger JM, Obál F. A neuronal group theory of sleep function. J Sleep Res 1993;2:63-9.
48. Krueger JM, Rector DM, Roy S, Van Dongen HPA, Belenky G, Panksepp J. Sleep as a fundamental property of neuronal assemblies. Nat Rev Neurosci 2008;9:910-9.
49. Van Dongen HPA, Belenky G, Krueger JM. A local, bottom-up perspective on sleep deprivation and neurobehavioral performance. Curr Top Med Chem 2011;11:2414-22.
50. Jackson ML, Gunzelmann G, Whitney P, et al. Deconstructing and reconstructing cognitive performance in sleep deprivation. Sleep Med Rev 2013;17:215-25.
51. Windels F. Neuronal activity: from in vitro preparation to behaving animals. Mol Neurobiol 2006;34:1-26.
52. Mendoza J, Challet E. Brain clocks: from the suprachiasmatic nuclei to a cerebral network. Neuroscientist 2009;15:477-88.
53. Edgar DM, Dement WC, Fuller CA. Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation. J Neurosci 1993;13:1065-79.
54. Kronauer RE, Gunzelmann G, Van Dongen HPA, Doyle FJ III, Klerman EB. Uncovering physiologic mechanisms of circadian rhythms and sleep/wake regulation through mathematical modeling. J Biol Rhythms 2007;22:233-45.
55. Rogers NL, Van Dongen HPA, Powell JW, et al. Neurobehavioural functioning during chronic sleep restriction at an adverse circadian phase. Sleep 2002;25(Abstract Supplement):A126-7.
56. Mallis MM, Mejdal S, Nguyen TT, Dinges DF. Summary of the key features of seven biomathematical models of human fatigue and performance. Aviat Space Environ Med 2004;75:A4-A14.
57. Dinges DF. Critical research issues in development of biomathematical models of fatigue and performance. Aviat Space Environ Med 2004;75:A181-91.
58. Jackson ML, Van Dongen HPA. Cognitive effects of sleepiness. In: Thorpy MJ, Billiard M, eds. Sleepiness: causes, consequences and treatment. Cambridge, England: Cambridge University Press; 2011:72-81.
59. Van Dongen HPA, Olofsen E, Dinges DF, Maislin G. Mixed-model regression analysis and dealing with interindividual differences. Methods Enzymol 2004;384:139-71.
60. Van Dongen HPA, Belenky G, Krueger JM. Investigating the temporal dynamics and underlying mechanisms of cognitive fatigue. In: Ackerman PL, ed. Cognitive fatigue. Washington, DC: American Psychological Association; 2010:127-47.
61. Wesensten NJ, Belenky G, Thorne DR, Kautz MA, Balkin TJ. Modafinil vs. caffeine: effects on fatigue during sleep deprivation. Aviat Space Environ Med 2004;75:520-25.
62. Elmenhorst D, Meyer PT, Winz OH, et al. Sleep deprivation increases A1 adenosine receptor binding in the human brain: a positron emission tomography study. J Neurosci 2007;27:2410-5.
63. Churchill L, Yasuda K, Yasuda T, et al. Unilateral cortical application of tumor necrosis factor a induces asymmetry in Fos- and interleukin-1β- immunoreactive cells within the corticothalamic projection. Brain Res 2005;1055:15-24.
64. Yasuda K, Churchill L, Yasuda T, Blindheim K, Falter M, Krueger JM. Unilateral cortical application of interleukin-1β (IL1β) induces asymmetry in Fos- and IL1β-immunoreactivity: implication for sleep regulation. Brain Res 2007;1131:44-59.
65. Fuller PM, Gooley JJ, Saper CB. Neurobiology of the sleep-wake cycle: sleep architecture, circadian regulation, and regulatory feedback. J Biol Rhythms 2006;21:482-93.
66. Starzyk J, Van Dongen HPA, Rogers NL, Dinges DF. Circadian adaptation during chronic sleep restriction at different circadian phases. Sleep 2004;27(Abstract Supplement):A74-5.
67. Rangan S, Van Dongen HPA. Quantifying fatigue risk in model-based fatigue risk management. Aviat Space Environ Med 2013;84:155-7.