Modeling interindividual differences in spontaneous internal desynchrony patterns

Journal of Biological Rhythms

Volumn 28, Issue 5, 2013, Pages 339-355

  Gleit, Rebecca D ^a   Diniz Behn, Cecilia G ^b   Booth, Victoria ^a,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b Department of Metallurgical and Materials Engineering   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

bicircadian; circadian rhythm; internal desynchrony; mathematical model; phase trapping; REM sleep; sleep; temporal isolation

Indexed keywords

ARTICLE; BICIRCADIAN; BIOLOGICAL MODEL; CIRCADIAN RHYTHM; HUMAN; INTERNAL DESYNCHRONY; MATHEMATICAL MODEL; PHASE TRAPPING; PHYSIOLOGY; REM SLEEP; SLEEP; SUPRACHIASMATIC NUCLEUS; TEMPORAL ISOLATION; WAKEFULNESS;

BICIRCADIAN; CIRCADIAN RHYTHM; INTERNAL DESYNCHRONY; MATHEMATICAL MODEL; PHASE TRAPPING; REM SLEEP; SLEEP; TEMPORAL ISOLATION;

CIRCADIAN RHYTHM; HUMANS; MODELS, BIOLOGICAL; SLEEP; SLEEP, REM; SUPRACHIASMATIC NUCLEUS; WAKEFULNESS;

EID: 84885773673     PISSN: 07487304     EISSN: 15524531     Source Type: Journal    
DOI: 10.1177/0748730413504277     Document Type: Article

References (82)

1. Abrahamson EE, Leak RK, Moore RY. The suprachiasmatic nucleus projects to posterior hypothalamic arousal systems. Neuroreport. 2001 ; 12: 435-440
2. Achermann P, Dijk DJ, Brunner DP, Borbely AA. A model of human sleep homeostasis based on EEG slow-wave activity: quantitative comparison of data and simulations. Brain Res Bull. 1993 ; 31: 97-113
3. Aston-Jones G, Chen S, Zhu Y, Oshinsky ML. A neural circuit for circadian regulation of arousal. Nat Neurosci. 2001 ; 4: 732-738
4. Basheer R, Strecker RE, Thakkar MM, McCarley RW. Adenosine and sleep-wake regulation. Prog Neurobiol. 2004 ; 73: 379-396
5. Belle MD, Diekman CO, Forger DB, Piggins HD. Daily electrical silencing in the mammalian circadian clock. Science. 2009 ; 326: 281-284
6. Bina KG, Rusak B, Semba K. Localization of cholinergic neurons in the forebrain and brainstem that project to the suprachiasmatic nucleus of the hypothalamus in rat. J Comp Neurol. 1993 ; 335: 295-307
7. Brown RE, McKenna JT, Winston S, Basheer R, Yanagawa Y, Thakkar MM, McCarley RW. Characterization of GABAergic neurons in rapid-eye-movement sleep controlling regions of the brainstem reticular formation in GAD67-green fluorescent protein knock-in mice. Eur J Neurosci. 2008 ; 27: 352-363
8. Buijs RM, Hou YX, Shinn S, Renaud LP. Ultrastructural evidence for intra- and extranuclear projections of GABAergic neurons of the suprachiasmatic nucleus. J Comp Neurol. 1994 ; 340: 381-391
9. Buijs RM, Wortel J, Hou YX. Colocalization of gamma-aminobutyric acid with vasopressin, vasoactive intestinal peptide, and somatostatin in the rat suprachiasmatic nucleus. J Comp Neurol. 1995 ; 358: 343-352
10. Burlet S, Tyler CJ, Leonard CS. Direct and indirect excitation of laterodorsal tegmental neurons by hypocretin/orexin peptides: implications for wakefulness and narcolepsy. J Neurosci. 2002 ; 22: 2862-2872
11. Carskadon M, Dement WC Principles and Practice of Sleep Medicine. Kryger MH Roth T Dement WC, ed. Philadelphia (PA): Saunders/Elsevier ; 2011: 16-26.
12. Carskadon MA, Dement WC. Distribution of REM-sleep on a 90 minute sleep-wake schedule. Sleep. 1980 ; 2: 309-317
13. Chou TC, Scammell TE, Gooley JJ, Gaus SE, Saper CB, Lu J. Critical role of dorsomedial hypothalamic nucleus in a wide range of behavioral circadian rhythms. J Neurosci. 2003 ; 23: 10691-10702
14. Clausen J, Sersen EA, Lidsky A. Variability of sleep measures in normal subjects. Psychophysiology. 1974 ; 11: 509-516
15. Colwell CS. Linking neural activity and molecular oscillations in the SCN. Nat Rev Neurosci. 2011 ; 12: 553-569
16. Czeisler CA, Duffy JF, Shanahan TL, Brown EN, Mitchell JF, Rimmer DW, Ronda JM, Silva EJ, Allan JS, Emens JS, et al. Stability, precision, and near-24-hour period of the human circadian pacemaker. Science. 1999 ; 284: 2177-2181
17. Czeisler CA, Weitzman E, Moore-Ede MC, Zimmerman JC, Knauer RS. Human sleep: its duration and organization depend on its circadian phase. Science. 1980a ; 210: 1264-1267
18. Czeisler CA, Zimmerman JC, Ronda JM, Moore-Ede MC, Weitzman ED. Timing of REM sleep is coupled to the circadian rhythm of body temperature in man. Sleep. 1980b ; 2: 329-346
19. Daan S, Beersma DG, Borbely AA. Timing of human sleep: recovery process gated by a circadian pacemaker. Am J Physiol. 1984 ; 246: R161 - R183
20. Datta S, Maclean RR. Neurobiological mechanisms for the regulation of mammalian sleep-wake behavior: reinterpretation of historical evidence and inclusion of contemporary cellular and molecular evidence. Neurosci Biobehav Rev. 2007 ; 31: 775-824
21. Deboer T, Vansteensel MJ, Detari L, Meijer JH. Sleep states alter activity of suprachiasmatic nucleus neurons. Nat Neurosci. 2003 ; 6: 1086-1090
22. Dijk DJ, Czeisler CA. Contribution of the circadian pacemaker and the sleep homeostat to sleep propensity, sleep structure, electroencephalographic slow waves, and sleep spindle activity in humans. J Neurosci. 1995 ; 15: 3526-3538
23. Dijk DJ, Duffy JF, Riel E, Shanahan TL, Czeisler CA. Ageing and the circadian and homeostatic regulation of human sleep during forced desynchrony of rest, melatonin and temperature rhythms. J Physiol. 1999 ; 516: 611-627
24. Dijk DJ, Lockley SW. Functional genomics of sleep and circadian rhythm - invited review: integration of human sleep-wake regulation and circadian rhythmicity. J Appl Physiol. 2002 ; 92: 852-862
25. Diniz Behn CG, Ananthasubramaniam A, Booth V. Contrasting existence and robustness of REM/non-REM cycling in physiologically based models of REM sleep regulatory networks. Siam J Appl Dyn Syst. 2013 ; 12: 279-314
26. Diniz Behn CG, Booth V. Simulating microinjection experiments in a novel model of the rat sleep-wake regulatory network. J Neurophysiol. 2010 ; 103: 1937-1953
27. Diniz Behn CG, Booth V. A fast-slow analysis of the dynamics of REM sleep. SIAM J Appl Dyn Sys. 2012 ; 11: 212-242
28. Diniz Behn CG, Brown EN, Scammell TE, Kopell NJ. Mathematical model of network dynamics governing mouse sleep-wake behavior. J Neurophysiol. 2007 ; 97: 3828-3840
29. 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: 1065-1079
30. Endo S, Kobayashi T, Yamamoto T, Fukuda H, Sasaki M, Ohta T. Persistence of the circadian rhythm of REM sleep: a variety of experimental manipulations of the sleep-wake cycle. Sleep. 1981 ; 4: 319-328
31. Fleshner M, Booth V, Forger DB, Diniz Behn CG. Circadian regulation of sleep-wake behaviour in nocturnal rats requires multiple signals from suprachiasmatic nucleus. Philos Transact A Math Phys Eng Sci. 2011 ; 369: 3855-3883
32. Forger DB, Jewett ME, Kronauer RE. A simpler model of the human circadian pacemaker. J Biol Rhythms. 1999 ; 14: 532-537
33. Forger DB, Peskin CS. A detailed predictive model of the mammalian circadian clock. Proc Natl Acad Sci U S A. 2003 ; 100: 14806-14811
34. Gillette MU, Reppert SM. The hypothalamic suprachiasmatic nuclei: circadian patterns of vasopressin secretion and neuronal activity in vitro. Brain Res Bull. 1987 ; 19: 135-139
35. Gooley JJ, Schomer A, Saper CB. The dorsomedial hypothalamic nucleus is critical for the expression of food-entrainable circadian rhythms. Nat Neurosci. 2006 ; 9: 398-407
36. Hofstra WA, de Weerd AW. How to assess circadian rhythm in humans: a review of literature. Epilepsy Behav. 2008 ; 13: 438-444
37. Huang ZL, Urade Y, Hayaishi O. Prostaglandins and adenosine in the regulation of sleep and wakefulness. Curr Opin Pharmacol. 2007 ; 7: 33-38
38. Jagota A, de la Iglesia HO, Schwartz WJ. Morning and evening circadian oscillations in the suprachiasmatic nucleus in vitro. Nat Neurosci. 2000 ; 3: 372-376
39. Kim JK, Forger DB. A mechanism for robust circadian timekeeping via stoichiometric balance. Mol Syst Biol. 2012 ; 8: 630
40. Klein T, Martens H, Dijk DJ, Kronauer RE, Seely EW, Czeisler CA. Circadian sleep regulation in the absence of light perception: chronic non-24-hour circadian rhythm sleep disorder in a blind man with a regular 24-hour sleep-wake schedule. Sleep. 1993 ; 16: 333-343
41. Klerman EB, Dijk DJ, Kronauer RE, Czeisler CA. Simulations of light effects on the human circadian pacemaker: implications for assessment of intrinsic period. Am J Physiol.. 1996 ; 270: R271 - R282
42. Klerman EB, Rimmer DW, Dijk DJ, Kronauer RE, Rizzo JF, Czeisler CA. Nonphotic entrainment of the human circadian pacemaker. Am J Physiol. 1998 ; 274: R991 - R996
43. Kronauer RE Mathematical Models of the Circadian Sleep-Wake Cycle. Moore-Ede MC Czeisler CA, ed. New York: Raven Press ; 1984: 105-128.
44. Kronauer RE, Czeisler CA, Pilato SF, Moore-Ede MC, Weitzman ED. Mathematical model of the human circadian system with two interacting oscillators. Am J Physiol. 1982 ; 242: R3 - R17
45. Kumar R, Bose A, Mallick BN. A mathematical model towards understanding the mechanism of neuronal regulation of wake-NREMS-REMS states. PLoS One. 2012 ; 7: e42059
46. Lee ML, Swanson BE, de la Iglesia HO. Circadian timing of REM sleep is coupled to an oscillator within the dorsomedial suprachiasmatic nucleus. Curr Biol. 2009 ; 19: 848-852
47. Leloup JC, Goldbeter A. Toward a detailed computational model for the mammalian circadian clock. Proc Natl Acad Sci U S A. 2003 ; 100: 7051-7056
48. Lu J, Sherman D, Devor M, Saper CB. A putative flip-flop switch for control of REM sleep. Nature. 2006 ; 441: 589-594
49. Luppi PH, Gervasoni D, Verret L, Goutagny R, Peyron C, Salvert D, Leger L, Fort P. Paradoxical (REM) sleep genesis: the switch from an aminergic-cholinergic to a GABAergic-glutamatergic hypothesis. J Physiol Paris. 2006 ; 100: 271-283
50. Massaquoi SG, McCarley RW. Extension of the limit cycle reciprocal interaction model of REM cycle control: an integrated sleep control model. J Sleep Res. 1992 ; 1: 138-143
51. McCarley RW, Hobson JA. Neuronal excitability modulation over the sleep cycle: a structural and mathematical model. Science. 1975 ; 189: 58-60
52. McCarley RW, Massaquoi SG. A limit-cycle mathematical-model of the REM-sleep oscillator system. Am J Physiol. 1986 ; 251: R1011 - R1029
53. McCarley RW, Massaquoi SG. Neurobiological structure of the revised limit cycle reciprocal interaction model of REM cycle control. J Sleep Res. 1992 ; 1: 132-137
54. Mirsky HP, Liu AC, Welsh DK, Kay SA, Doyle FJ. A model of the cell-autonomous mammalian circadian clock. Proc Natl Acad Sci U S A. 2009 ; 106: 11107-11112
55. Mistlberger RE. Circadian regulation of sleep in mammals: role of the suprachiasmatic nucleus. Brain Res Brain Res Rev. 2005 ; 49: 429-454
56. Moore RY, Halaris AE, Jones BE. Serotonin neurons of the midbrain raphe: ascending projections. J Comp Neurol. 1978 ; 180: 417-438
57. Moore RY, Speh JC. GABA is the principal neurotransmitter of the circadian system. Neurosci Lett. 1993 ; 150: 112-116
58. Morairty S, Rainnie D, McCarley R, Greene R. Disinhibition of ventrolateral preoptic area sleep-active neurons by adenosine: a new mechanism for sleep promotion. Neuroscience. 2004 ; 123: 451-457
59. Morin LP, Goodless-Sanchez N, Smale L, Moore RY. Projections of the suprachiasmatic nuclei, subparaventricular zone and retrochiasmatic area in the golden hamster. Neuroscience. 1994 ; 61: 391-410
60. Nakao M, Sakai H, Yamamoto M. An interpretation of the internal desynchronizations based on dynamics of the two-process model. Methods Inf Med. 1997 ; 36: 282-285
61. Novak CM, Nunez AA. A sparse projection from the suprachiasmatic nucleus to the sleep active ventrolateral preoptic area in the rat. Neuroreport. 2000 ; 11: 93-96
62. Phillips AJ, Chen PY, Robinson PA. Probing the mechanisms of chronotype using quantitative modeling. J Biol Rhythms. 2010a ; 25: 217-227
63. Phillips AJ, Robinson PA, Kedziora DJ, Abeysuriya RG. Mammalian sleep dynamics: how diverse features arise from a common physiological framework. PLoS Comput Biol. 2010b ; 6: e1000826
64. Phillips AJ, Robinson PA, Klerman EB. Arousal state feedback as a potential physiological generator of the ultradian REM/NREM sleep cycle. J Theor Biol. 2013 ; 319: 75-87
65. Phillips AJK, Czeisler CA, Klerman EB. Revisiting spontaneous internal desynchrony using a quantitative model of sleep physiology. J Biol Rhythms. 2011 ; 26: 441-453
66. 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
67. Relogio A, Westermark PO, Wallach T, Schellenberg K, Kramer A, Herzel H. Tuning the mammalian circadian clock: robust synergy of two loops. PLoS Comput Biol. 2011 ; 7: e1002309
68. Rempe MJ, Best J, Terman D. A mathematical model of the sleep/wake cycle. J Math Biol. 2010 ; 60: 615-644
69. Sakurai T. The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci. 2007 ; 8: 171-181
70. Saper CB, Chou TC, Scammell TE. The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci. 2001 ; 24: 726-731
71. Saper CB, Scammell TE, Lu J. Hypothalamic regulation of sleep and circadian rhythms. Nature. 2005 ; 437: 1257-1263
72. Sapin E, Lapray D, Berod A, Goutagny R, Leger L, Ravassard P, Clement O, Hanriot L, Fort P, Luppi PH. Localization of the brainstem GABAergic neurons controlling paradoxical (REM) sleep. PLoS One. 2009 ; 4: e4272
73. Schaap J, Pennartz CM, Meijer JH. Electrophysiology of the circadian pacemaker in mammals. Chronobiol Int. 2003 ; 20: 171-188
74. Scheer FA, Wright KP, Kronauer RE, Czeisler CA. Plasticity of the intrinsic period of the human circadian timing system. PLoS One. 2007 ; 2: e721
75. Schwartz WJ, Reppert SM, Eagan SM, Moore-Ede MC. In vivo metabolic activity of the suprachiasmatic nuclei: a comparative study. Brain Res. 1983 ; 274: 184-187
76. Sun X, Whitefield S, Rusak B, Semba K. Electrophysiological analysis of suprachiasmatic nucleus projections to the ventrolateral preoptic area in the rat. Eur J Neurosci. 2001 ; 14: 1257-1274
77. Tamakawa Y, Karashima A, Koyama Y, Katayama N, Nakao M. A quartet neural system model orchestrating sleep and wakefulness mechanisms. J Neurophysiol. 2006 ; 95: 2055-2069
78. Tobler II, Franken P, Trachsel L, Borbely AA. Models of sleep regulation in mammals. J Sleep Res. 1992 ; 1: 125-127
79. Weitzman ED, Czeisler CA, Zimmerman JC, Ronda JM. Timing of REM and stages 3 + 4 sleep during temporal isolation in man. Sleep. 1980 ; 2: 391-407
80. Wever R The Circadian System of Man: Results of Experiments Under Temporal Isolation. New York: Springer-Verlag ; 1979:
81. Zulley J. Distribution of REM-sleep in entrained 24 hour and free-running sleep-wake cycles. Sleep. 1980 ; 2: 377-389
82. Zulley J, Wever R, Aschoff J. The dependence of onset and duration of sleep on the circadian rhythm of rectal temperature. Pflugers Arch. 1981 ; 391: 314-318