A mathematical model towards understanding the mechanism of neuronal regulation of wake-NREMS-REMS states

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Kumar, Rupesh ^a   Bose, Amitabha ^a,b   Mallick, Birendra Nath ^a  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

^b NEW JERSEY INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRAIN NERVE CELL; CELL ACTIVITY; CIRCADIAN RHYTHM; DYNAMICS; HOMEOSTASIS; MATHEMATICAL MODEL; NONHUMAN; NONREM SLEEP; PATHOPHYSIOLOGY; PRESYNAPTIC INHIBITION; REGULATORY MECHANISM; REM SLEEP; SIMULATION; SLEEP PATTERN; SLEEP WAKING CYCLE; SUBSTANTIA NIGRA; WAKEFULNESS;

ANIMALS; CIRCADIAN RHYTHM; COMPUTER SIMULATION; HOMEOSTASIS; HUMANS; HYPOTHALAMUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, NEUROLOGICAL; MODELS, THEORETICAL; NEURONS; NEUROPEPTIDES; SLEEP; SLEEP, REM; SUBSTANTIA NIGRA; WAKEFULNESS;

ANIMALIA;

EID: 84864686063     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042059     Document Type: Article

References (96)

1. Moruzzi G, (1972) The sleep-waking cycle. Ergeb Physiol 64: 1-165.
2. Mallick BN, Inoue S, (1999) Rapid Eye Movement Sleep. New York: Marcel Dekker. 419 p.
3. Mallick BN, Singh A, (2011) REM sleep loss increases brain excitability: role of noradrenaline and its mechanism of action. Sleep Med Rev 15: 165-178.
4. Steriade M, McCarley RW, (2005) Brain control of wakefulness and sleep. 1st ed. New York: Kluwer Acedemic/Plenum. 728 p.
5. Mallick BN, Pandi-Perumal SR, McCarley RW, Morrison AR, (2011) Rapid Eye Movement Sleep: Regulation and Function. New York: Cambridge. 478 p.
6. Moruzzi G, Magoun HW, (1949) Brain stem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1: 455-473.
7. Nauta WJ, (1946) Hypothalamic regulation of sleep in rats; an experimental study. J Neurophysiol 9: 285-316.
8. Bremer F, (1973) Preoptic hypnogenic area and reticular activating system. Arch Ital Biol 111: 85-111.
9. Bremer F, (1975) Existence of a mutal tonic inhibitory interaction between the preoptic hypnogenic structure and the midbrain reticular formation. Brain Res 96: 71-75.
10. Mallick BN, Mohan Kumar V, Chhina GS, Singh B, (1984) Responses of preoptic neurons to stimulation of caudal and rostral brain stem reticular structures. Brain Res Bull 13: 353-356.
11. Mallick BN, Kumar VM, Chhina GS, Singh B, (1986) Comparison of rostro-caudal brain stem influence on preoptic neurons and cortical EEG. Brain Res Bull 16: 121-125.
12. Szymusiak R, McGinty D, (1989) Effects of basal forebrain stimulation on the waking discharge of neurons in the midbrain reticular formation of cats. Brain Res 498: 355-359.
13. Mancia M, Mariotti M, Spreafico R, (1974) Caudo-rostral brain stem reciprocal influences in the cat. Brain Res 80: 41-51.
14. Okudzhava VM, Mestvirishvili LP, Papuashvili NS, Bagashvili TI, (1985) [Interaction of reticular structures in the brain of the cat]. Zh Vyssh Nerv Deiat Im I P Pavlova 35: 891-899.
15. Rosina A, Mancia M, (1966) Electrophysiological and behavioural changes following selective and reversible inactivation of lower brain-stem structures in chronic cats. Electroencephalogr Clin Neurophysiol 21: 157-167.
16. Mohan Kumar V, Mallick BN, Chhina GS, Singh B, (1985) Alterations in preoptic unit activity on stimulation of caudal brain stem EEG-synchronizing structures. Exp Neurol 89: 304-313.
17. Aston-Jones G, Bloom FE, (1981) Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli. J Neurosci 1: 887-900.
18. Chu N, Bloom FE, (1973) Norepinephrine-containing neurons: changes in spontaneous discharge patterns during sleeping and waking. Science 179: 908-910.
19. Hobson JA, McCarley RW, Wyzinski PW, (1975) Sleep cycle oscillation: reciprocal discharge by two brainstem neuronal groups. Science 189: 55-58.
20. Jacobs BL, (1986) Single unit activity of locus coeruleus neurons in behaving animals. Prog Neurobiol 27: 183-194.
21. Dominguez JM, Hull EM, (2005) Dopamine, the medial preoptic area, and male sexual behavior. Physiol Behav 86: 356-368.
22. Gvilia I, Turner A, McGinty D, Szymusiak R, (2006) Preoptic area neurons and the homeostatic regulation of rapid eye movement sleep. J Neurosci 26: 3037-3044.
23. McGinty D, Szymusiak R, (1990) Keeping cool: a hypothesis about the mechanisms and functions of slow-wave sleep. Trends Neurosci 13: 480-487.
24. Li Y, Gao XB, Sakurai T, van den Pol AN, (2002) Hypocretin/Orexin excites hypocretin neurons via a local glutamate neuron-A potential mechanism for orchestrating the hypothalamic arousal system. Neuron 36: 1169-1181.
25. Methippara MM, Alam MN, Szymusiak R, McGinty D, (2000) Effects of lateral preoptic area application of orexin-A on sleep-wakefulness. Neuroreport 11: 3423-3426.
26. Kaur S, Panchal M, Faisal M, Madan V, Nangia P, et al. (2004) Long term blocking of GABA-A receptor in locus coeruleus by bilateral microinfusion of picrotoxin reduced rapid eye movement sleep and increased brain Na-K ATPase activity in freely moving normally behaving rats. Behav Brain Res 151: 185-190.
27. Mallick BN, Singh S, Pal D, (2005) Role of alpha and beta adrenoceptors in locus coeruleus stimulation-induced reduction in rapid eye movement sleep in freely moving rats. Behav Brain Res 158: 9-21.
28. Kaur S, Saxena RN, Mallick BN, (2001) GABAergic neurons in prepositus hypoglossi regulate REM sleep by its action on locus coeruleus in freely moving rats. Synapse 42: 141-150.
29. Pal D, Madan V, Mallick BN, (2005) Neural mechanism of rapid eye movement sleep generation: Cessation of locus coeruleus neurons is a necessity. Sheng Li Xue Bao 57: 401-413.
30. Pal D, Mallick BN, (2006) Role of noradrenergic and GABA-ergic inputs in pedunculopontine tegmentum for regulation of rapid eye movement sleep in rats. Neuropharmacology 51: 1-11.
31. Pal D, Mallick BN, (2009) GABA in pedunculopontine tegmentum increases rapid eye movement sleep in freely moving rats: possible role of GABA-ergic inputs from substantia nigra pars reticulata. Neuroscience 164: 404-414.
32. Mallick BN, Singh A, Khanday MA, (2012) Activation of inactivation process initiates rapid eye movement sleep. Prog Neurobiol 97: 259-276.
33. Nishino S, Sakurai T, (2006) The orexin/hypocretin system: physiology and pathophysiology. New Jersey: Humana Press. 397 p.
34. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, et al. (1998) Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18: 9996-10015.
35. Borbely AA, (1982) A two process model of sleep regulation. Hum Neurobiol 1: 195-204.
36. Borbely AA, Achermann P, (1999) Sleep homeostasis and models of sleep regulation. J Biol Rhythms 14: 557-568.
37. Tamakawa Y, Karashima A, Koyama Y, Katayama N, Nakao M, (2006) A quartet neural system model orchestrating sleep and wakefulness mechanisms. J Neurophysiol 95: 2055-2069.
38. Behn CG, Brown EN, Scammell TE, Kopell NJ, (2007) Mathematical model of network dynamics governing mouse sleep-wake behavior. J Neurophysiol 97: 3828-3840.
39. Phillips AJ, Robinson PA, (2007) A quantitative model of sleep-wake dynamics based on the physiology of the brainstem ascending arousal system. J Biol Rhythms 22: 167-179.
40. Diniz Behn CG, Kopell N, Brown EN, Mochizuki T, Scammell TE, (2008) Delayed orexin signaling consolidates wakefulness and sleep: physiology and modeling. J Neurophysiol 99: 3090-3103.
41. Phillips AJ, Robinson PA, (2008) Sleep deprivation in a quantitative physiologically based model of the ascending arousal system. J Theor Biol 255: 413-423.
42. Postnova S, Voigt K, Braun HA, (2009) A mathematical model of homeostatic regulation of sleep-wake cycles by hypocretin/orexin. J Biol Rhythms 24: 523-535.
43. Diniz Behn CG, Booth V, (2010) Simulating microinjection experiments in a novel model of the rat sleep-wake regulatory network. J Neurophysiol 103: 1937-1953.
44. Rempe MJ, Best J, Terman D, (2010) A mathematical model of the sleep/wake cycle. J Math Biol 60: 615-644.
45. Fleshner M, Booth V, Forger DB, Diniz Behn CG, (2011) Circadian regulation of sleep-wake behaviour in nocturnal rats requires multiple signals from suprachiasmatic nucleus. Philos Transact A Math Phys Eng Sci 369: 3855-3883.
46. Morris C, Lecar H, (1981) Voltage oscillations in the barnacle giant muscle fiber. Biophys J 35: 193-213.
47. Sterman MB, Clemente CD, (1962) Forebrain inhibitory mechanisms: sleep patterns induced by basal forebrain stimulation in the behaving cat. Exp Neurol 6: 103-117.
48. Sterman MB, Clemente CD, (1962) Forebrain inhibitory mechanisms: cortical synchronization induced by basal forebrain stimulation. Exp Neurol 6: 91-102.
49. Hernandez Peon R, Chavez Ibarra G, (1963) Sleep induced by electrical or chemical stimulation of the forebrain. Electroencephalogr Clin Neurophysiol: Suppl 24: 188+.
50. Mallick BN, Chhina GS, Sundaram KR, Singh B, Kumar VM, (1983) Activity of preoptic neurons during synchronization and desynchronization. Exp Neurol 81: 586-597.
51. Favale E, Loeb C, Rossi GF, Sacco G, (1961) EEG synchronization and behavioral signs of sleep following low frequency stimulation of the brain stem reticular formation. Arch Ital Biol 99: 1-22.
52. Magni FM, Rossi GF, Zanchetti A, (1959) EEG arousal following inactivation of the lower brain stem by selective injection of barbiturate into the vertebral circulation. Arch ital Biol 97: 33-46.
53. Magnes J, Moruzzi G, Pompeiano O, (1961) Synchronization of the EEG produced by low frequency electrical stimulation of the region of the solitary tract. Arch Ital Biol 99: 33-67.
54. Bremer F, (1970) Preoptic hypnogenic focus and mesencephalic reticular formation. Brain Res 21: 132-134.
55. De Armond SJ, Fusco MM, (1971) The effect of preoptic warming on the arousal system of the mesencephalic reticular formation. Exp Neurol 33: 653-670.
56. Saper CB, Scammell TE, Lu J, (2005) Hypothalamic regulation of sleep and circadian rhythms. Nature 437: 1257-1263.
57. Mancia M, Grantyn A, Broggi G, Margnelli M, (1971) Synaptic linkage between mesencephalic and bulbo-pontine reticular structures as revealed by intracellular recording. Brain Res 33: 491-494.
58. Espana RA, Baldo BA, Kelley AE, Berridge CW, (2001) Wake-promoting and sleep-suppressing actions of hypocretin (orexin): basal forebrain sites of action. Neuroscience 106: 699-715.
59. Anaclet C, Parmentier R, Ouk K, Guidon G, Buda C, et al. (2009) Orexin/hypocretin and histamine: distinct roles in the control of wakefulness demonstrated using knock-out mouse models. J Neurosci 29: 14423-14438.
60. Lu J, Sherman D, Devor M, Saper CB, (2006) A putative flip-flop switch for control of REM sleep. Nature 441: 589-594.
61. Mallick BN, Kaur S, Saxena RN, (2001) Interactions between cholinergic and GABAergic neurotransmitters in and around the locus coeruleus for the induction and maintenance of rapid eye movement sleep in rats. Neuroscience 104: 467-485.
62. Mallick BN, Thankachan S, Islam F, (2004) Influence of hypnogenic brain areas on wakefulness- and rapid-eye-movement sleep-related neurons in the brainstem of freely moving cats. J Neurosci Res 75: 133-142.
63. Thankachan S, Islam F, Mallick BN, (2001) Role of wake inducing brain stem area on rapid eye movement sleep regulation in freely moving cats. Brain Res Bull 55: 43-49.
64. Bourgin P, Huitron-Resendiz S, Spier AD, Fabre V, Morte B, et al. (2000) Hypocretin-1 modulates rapid eye movement sleep through activation of locus coeruleus neurons. J Neurosci 20: 7760-7765.
65. Hagan JJ, Leslie RA, Patel S, Evans ML, Wattam TA, et al. (1999) Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proc Natl Acad Sci U S A 96: 10911-10916.
66. Yamanaka A, Muraki Y, Tsujino N, Goto K, Sakurai T, (2003) Regulation of orexin neurons by the monoaminergic and cholinergic systems. Biochem Biophys Res Commun 303: 120-129.
67. Espana RA, Scammell TE, (2006) Orexin and hypothalamic control of sleep and waking. In: Nishino S, Sakurai, T, editors. The Orexin/Hypocretin System: Physiology and Pathophysiology. New Jersey: Humana Press. pp. 189-207.
68. Yoshida K, McCormack S, Espana RA, Crocker A, Scammell TE, (2006) Afferents to the orexin neurons of the rat brain. J Comp Neurol 494: 845-861.
69. Crocker A, Espana RA, Papadopoulou M, Saper CB, Faraco J, et al. (2005) Concomitant loss of dynorphin, NARP, and orexin in narcolepsy. Neurology 65: 1184-1188.
70. Sherin JE, Elmquist JK, Torrealba F, Saper CB, (1998) Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. J Neurosci 18: 4705-4721.
71. Daan S, Beersma DG, Borbely AA, (1984) Timing of human sleep: recovery process gated by a circadian pacemaker. Am J Physiol 246: R161-183.
72. Achermann P, Borbely AA, (1994) Simulation of daytime vigilance by the additive interaction of a homeostatic and a circadian process. Biol Cybern 71: 115-121.
73. Abrahamson EE, Leak RK, Moore RY, (2001) The suprachiasmatic nucleus projects to posterior hypothalamic arousal systems. Neuroreport 12: 435-440.
74. Skinner FK, Kopell N, Marder E, (1994) Mechanisms for oscillation and frequency control in reciprocally inhibitory model neural networks. J Comput Neurosci 1: 69-87.
75. Trachsel L, Tobler I, Borbely AA, (1986) Sleep regulation in rats: effects of sleep deprivation, light, and circadian phase. Am J Physiol 251: R1037-1044.
76. Borbely AA, Baumann F, Brandeis D, Strauch I, Lehmann D, (1981) Sleep deprivation: effect on sleep stages and EEG power density in man. Electroencephalogr Clin Neurophysiol 51: 483-495.
77. Akerstedt T, Gillberg M, (1986) Sleep duration and the power spectral density of the EEG. Electroencephalogr Clin Neurophysiol 64: 119-122.
78. Saper CB, Chou TC, Scammell TE, (2001) The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci 24: 726-731.
79. Benington JH, Heller HC, (1994) Does the function of REM sleep concern non-REM sleep or waking? Prog Neurobiol 44: 433-449.
80. Benington JH, Heller HC, (1994) REM-sleep timing is controlled homeostatically by accumulation of REM-sleep propensity in non-REM sleep. Am J Physiol 266: R1992-2000.
81. Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, et al. (1999) Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 98: 437-451.
82. Mochizuki T, Crocker A, McCormack S, Yanagisawa M, Sakurai T, et al. (2004) Behavioral state instability in orexin knock-out mice. J Neurosci 24: 6291-6300.
83. Nishino S, Ripley B, Overeem S, Lammers GJ, Mignot E, (2000) Hypocretin (orexin) deficiency in human narcolepsy. Lancet 355: 39-40.
84. Nambu T, Sakurai T, Mizukami K, Hosoya Y, Yanagisawa M, et al. (1999) Distribution of orexin neurons in the adult rat brain. Brain Res 827: 243-260.
85. Edgar DM, Dement WC, Fuller CA, (1993) Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation. J Neurosci 13: 1065-1079.
86. Nishino S, (2007) Narcolepsy: pathophysiology and pharmacology. J Clin Psychiatry 68 Suppl 13: 9-15.
87. Mallick BN, Jha SK, Islam F, (2004) Wakefulness-inducing area in the brainstem excites warm-sensitive and inhibits cold-sensitive neurons in the medial preoptic area in anesthetized rats. Synapse 51: 59-70.
88. Guzman-Marin R, Alam MN, Szymusiak R, Drucker-Colin R, Gong H, et al. (2000) Discharge modulation of rat dorsal raphe neurons during sleep and waking: effects of preoptic/basal forebrain warming. Brain Res 875: 23-34.
89. Suntsova N, Szymusiak R, Alam MN, Guzman-Marin R, McGinty D, (2002) Sleep-waking discharge patterns of median preoptic nucleus neurons in rats. J Physiol 543: 665-677.
90. Everson CA, Gilliland MA, Kushida CA, Pilcher JJ, Fang VS, et al. (1989) Sleep deprivation in the rat: IX. Recovery. Sleep 12: 60-67.
91. Gilliland MA, Bergmann BM, Rechtschaffen A, (1989) Sleep deprivation in the rat: VIII. High EEG amplitude sleep deprivation. Sleep 12: 53-59.
92. McCarley RW, Hobson JA, (1975) Neuronal excitability modulation over the sleep cycle: a structural and mathematical model. Science 189: 58-60.
93. Nishino S, (2007) Clinical and neurobiological aspects of narcolepsy. Sleep Med 8: 373-399.
94. Willie JT, Chemelli RM, Sinton CM, Tokita S, Williams SC, et al. (2003) Distinct narcolepsy syndromes in Orexin receptor-2 and Orexin null mice: molecular genetic dissection of Non-REM and REM sleep regulatory processes. Neuron 38: 715-730.
95. Singh S, Mallick BN, (1996) Mild electrical stimulation of pontine tegmentum around locus coeruleus reduces rapid eye movement sleep in rats. Neurosci Res 24: 227-235.
96. Sakurai T, (2007) The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci 8: 171-181.