Circadian regulation of sleep-wake behaviour in nocturnal rats requires multiple signals from suprachiasmatic nucleus

Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences

Volumn 369, Issue 1952, 2011, Pages 3855-3883

  Fleshner, Michelle ^a   Booth, Victoria ^a,b   Forger, Daniel B ^a   Behn, Cecilia G Diniz ^a,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c GETTYSBURG COLLEGE   (United States)

Author keywords

Firing rate model; Sleep wake model; Suprachiasmatic nucleus; Vasoactive intestinal peptide

Indexed keywords

BEHAVIORAL RESEARCH; BRAIN; DYNAMICS; MATHEMATICAL MODELS; PEPTIDES; PHYSIOLOGICAL MODELS; PHYSIOLOGY; RATS; WAKES;

CIRCADIAN CLOCK; CIRCADIAN REGULATION; CIRCADIAN VARIATION; DYNAMIC INTERACTION; FIRING PATTERNS; FIRING-RATE MODEL; INTERACTION DYNAMICS; MEDIATED SIGNALLING; NEURONAL POPULATIONS; PHYSIOLOGICAL SUBSTRATE; REGULATORY SYSTEMS; SLEEP-WAKE MODEL; SUPRACHIASMATIC NUCLEUS; VASOACTIVE INTESTINAL PEPTIDE;

SLEEP RESEARCH;

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; PEPTIDE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BIOLOGICAL MODEL; CIRCADIAN RHYTHM; CYTOLOGY; HOMEOSTASIS; METABOLISM; NERVE CELL; PHYSIOLOGY; RAT; SLEEP; SUPRACHIASMATIC NUCLEUS; WAKEFULNESS;

ANIMALS; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; HOMEOSTASIS; MODELS, NEUROLOGICAL; NEURONS; NEUROTRANSMITTER AGENTS; PEPTIDES; RATS; SLEEP; SUPRACHIASMATIC NUCLEUS; WAKEFULNESS;

EID: 80054984183     PISSN: 1364503X     EISSN: None     Source Type: Journal    
DOI: 10.1098/rsta.2011.0085     Document Type: Article

References (103)

1. Houben, T., Deboer, T., van Oosterhout, F. & Meijer, J. H. 2009 Correlation with behavioral activity and rest implies circadian regulation by SCN neuronal activity levels. J. Biol. Rhythms 24, 477-487. (doi:10.1177/ 0748730409349895)
2. Gillette, M. U. & Reppert, S. M. 1987 The hypothalamic suprachiasmatic nuclei: circadian patterns of vasopressin secretion and neuronal activity in vitro. Brain Res. Bull. 19, 135-139. (doi:10.1016/0361-9230(87) 90176-6) (Pubitemid 18037902)
3. Schaap, J., Pennartz, C. M. & Meijer, J. H. 2003 Electrophysiology of the circadian pacemaker in mammals. Chronobiol. Int. 20, 171-188. (doi:10.1081/CBI-120019311) (Pubitemid 36505395)
4. Schwartz, W. J., Reppert, S. M., Eagan, S. M. & Moore-Ede, M. C. 1983 In vivo metabolic activity of the suprachiasmatic nuclei: a comparative study. Brain Res. 274, 184-187. (doi:10.1016/0006-8993(83)90538-3) (Pubitemid 13031973)
5. Belle, M. D., Diekman, C. O., Forger, D. B. & Piggins, H. D. 2009 Daily electrical silencing in the mammalian circadian clock. Science 326, 281-284. (doi:10.1126/science.1169657)
6. Jagota, A., de la Iglesia, H. O. & Schwartz, W. J. 2000 Morning and evening circadian oscillations in the suprachiasmatic nucleus in vitro. Nat. Neurosci. 3, 372-376. (doi:10.1038/73943) (Pubitemid 30185488)
7. Schaap, J., Albus, H., VanderLeest, H. T., Eilers, P. H., Detari, L. & Meijer, J. H. 2003 Heterogeneity of rhythmic suprachiasmatic nucleus neurons: implications for circadian waveform and photoperiodic encoding. Proc. Natl Acad. Sci. USA 100, 15994-15 999. (doi:10.1073/pnas.2436298100) (Pubitemid 38021103)
8. Sun, X., Whitefield, S., Rusak, B. & Semba, K. 2001 Electrophysiological analysis of suprachiasmatic nucleus projections to the ventrolateral preoptic area in the rat. Eur. J. Neurosci. 14, 1257-1274. (doi:10.1046/j.0953-816x.2001.0001755.x) (Pubitemid 35463733)
9. Aston-Jones, G., Chen, S., Zhu, Y. & Oshinsky, M. L. 2001 A neural circuit for circadian regulation of arousal. Nat. Neurosci. 4, 732-738. (doi:10.1038/89522) (Pubitemid 32595412)
10. Gooley, J. J., Schomer, A. & Saper, C. B. 2006 The dorsomedial hypothalamic nucleus is critical for the expression of food-entrainable circadian rhythms. Nat. Neurosci. 9, 398-407. (doi:10.1038/nn1651) (Pubitemid 43290970)
11. Morin, L. P., Goodless-Sanchez, N., Smale, L. & Moore, R. Y. 1994 Projections of the suprachiasmatic nuclei, subparaventricular zone and retrochiasmatic area in the golden hamster. Neuroscience 61, 391-410. (doi:10.1016/0306-4522(94)90240-2) (Pubitemid 24219016)
12. Saper, C. B., Scammell, T. E. & Lu, J. 2005 Hypothalamic regulation of sleep and circadian rhythms. Nature 437, 1257-1263. (doi:10.1038/nature04284) (Pubitemid 41568665)
13. Buijs, R. M., Hou, Y. X., Shinn, S. & Renaud, L. P. 1994 Ultrastructural evidence for intra-and extranuclear projections of GABAergic neurons of the suprachiasmatic nucleus. J. Comp. Neurol. 340, 381-391. (doi:10.1002/cne.903400308) (Pubitemid 24042212)
14. Buijs, R. M., Wortel, J. & Hou, Y. X. 1995 Colocalization of gamma-aminobutyric acid with vasopressin, vasoactive intestinal peptide, and somatostatin in the rat suprachiasmatic nucleus. J. Comp. Neurol. 358, 343-352. (doi:10.1002/cne.903580304)
15. Moore, R. Y. & Speh, J. C. 1993 GABA is the principal neurotransmitter of the circadian system. Neurosci. Lett. 150, 112-116. (doi:10.1016/0304-3940(93)90120-A) (Pubitemid 23142338)
16. Albers, H. E., Stopa, E. G., Zoeller, R. T., Kauer, J. S., King, J. C., Fink, J. S., Mobtaker, H. & Wolfe, H. 1990 Day-night variation in prepro vasoactive intestinal peptide/peptide histidine isoleucine mRNA within the rat suprachiasmatic nucleus. Mol. Brain Res. 7, 85-89. (doi:10.1016/0169-328X(90) 90077-Q) (Pubitemid 20020908)
17. Deurveilher, S. & Semba, K. 2005 Indirect projections from the suprachiasmatic nucleus to major arousal-promoting cell groups in rat: implications for the circadian control of behavioural state. Neuroscience 130, 165-183. (doi:10.1016/j.neuroscience.2004.08.030) (Pubitemid 39550423)
18. Hermes, M. L., Kolaj, M., Doroshenko, P., Coderre, E. & Renaud, L. P. 2009 Effects of VPAC2 receptor activation on membrane excitability and GABAergic transmission in subparaventricular zone neurons targeted by suprachiasmatic nucleus. J. Neurophysiol. 102, 1834-1842. (doi:10.1152/jn.91261. 2008)
19. Shinohara, K., Funabashi, T. & Kimura, F. 1999 Temporal profiles of vasoactive intestinal polypeptide precursor mRNA and its receptor mRNA in the rat suprachiasmatic nucleus. Mol. Brain Res. 63, 262-267. (doi:10.1016/S0169- 328X(98)00289-7) (Pubitemid 29036977)
20. Shinohara, K., Tominaga, K., Isobe, Y. & Inouye, S. T. 1993 Photic regulation of peptides located in the ventrolateral subdivision of the suprachiasmatic nucleus of the rat: daily variations of vasoactive intestinal polypeptide, gastrin-releasing peptide, and neuropeptide Y. J. Neurosci. 13, 793-800. (Pubitemid 23045159)
21. Deboer, T., Vansteensel, M. J., Detari, L. & Meijer, J. H. 2003 Sleep states alter activity of suprachiasmatic nucleus neurons. Nat. Neurosci. 6, 1086-1090. (doi:10.1038/nn1122) (Pubitemid 37186201)
22. Bina, K. G., Rusak, B. & Semba, K. 1993 Localization of cholinergic neurons in the forebrain and brainstem that project to the suprachiasmatic nucleus of the hypothalamus in rat. J. Comp. Neurol. 335, 295-307. (doi:10.1002/cne.903350212) (Pubitemid 23256194)
23. Moore, R. Y., Halaris, A. E. & Jones, B. E. 1978 Serotonin neurons of the midbrain raphe: ascending projections. J. Comp. Neurol. 180, 417-438. (doi:10.1002/cne.901800302)
24. Diekman, C. O. & Forger, D. B. 2009 Clustering predicted by an electrophysiological model of the suprachiasmatic nucleus. J. Biol. Rhythms 24, 322-333. (doi:10.1177/0748730409337601)
25. Goldbeter, A., Gerard, C. & Leloup, J. C. 2010 Circadian rhythms and systems biology. Med. Sci. (Paris) 26, 49-56. (doi:10.1051/medsci/201026149)
26. Jewett, M. E., Forger, D. B. & Kronauer, R. E. 1999 Revised limit cycle oscillator model of human circadian pacemaker. J. Biol. Rhythms 14, 493-499. (doi:10.1177/074873049901400608) (Pubitemid 30086857)
27. Leloup, J. C. & Goldbeter, A. 2008 Modeling the circadian clock: from molecular mechanism to physiological disorders. Bioessays 30, 590-600. (doi:10.1002/bies.20762) (Pubitemid 351859415)
28. Sim, C. K. & Forger, D. B. 2007 Modeling the electrophysiology of suprachiasmatic nucleus neurons. J. Biol. Rhythms 22, 445-453. (doi:10.1177/0748730407306041) (Pubitemid 47507057)
29. Vasalou, C. & Henson, M. A. 2010 A multiscale model to investigate circadian rhythmicity of pacemaker neurons in the suprachiasmatic nucleus. PLoS Comput. Biol. 6, e1000706. (doi:10.1371/journal.pcbi.1000706)
30. Diniz Behn, C. & Booth, V. 2011 A population network model of neuronal and neurotransmitter interactions regulating mammalian sleep-wake behavior. In Anesthesia and sleep: recent theoretical and experimental aspects (ed. A. Hutt). New York, NY: Springer.
31. Diniz Behn, C. G., Brown, E. N., Scammell, T. E. & Kopell, N. J. 2007 A mathematical model of network dynamics governing mouse sleep-wake behavior. J. Neurophysiol. 97, 3828-3840. (doi:10.1152/jn.01184.2006) (Pubitemid 47080619)
32. McCarley, R. W. & Hobson, J. A. 1975 Neuronal excitability modulation over the sleep cycle: a structural and mathematical model. Science 189, 58-60. (doi:10.1126/science.1135627)
33. Phillips, A. J. & Robinson, P. A. 2007 A quantitative model of sleep-wake dynamics based on the physiology of the brainstem ascending arousal system. J. Biol. Rhythms 22, 167-179. (doi:10.1177/0748730406297512) (Pubitemid 46568647)
34. Diniz Behn, C. & Booth, V. 2010 Simulating microinjection experiments in a novel model of the rat sleep-wake regulatory network. J. Neurophysiol. 103, 1937-1953. (doi:10.1152/jn.00795.2009)
35. Rempe, M. J., Best, J. & Terman, D. 2010 A mathematical model of the sleep/wake cycle. J. Math. Biol. 60, 615-644. (doi:10.1007/s00285-009-0276-5)
36. 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. (doi:10.1152/jn.00575.2005)
37. Achermann, P., Dijk, D. J., Brunner, D. P. & Borbely, A. A. 1993 A model of human sleep homeostasis based on EEG slow-wave activity: quantitative comparison of data and simulations. Brain Res. Bull. 31, 97-113. (doi:10.1016/0361-9230(93)90016-5)
38. Borbely, A. A. 1982 A two process model of sleep regulation. Hum. Neurobiol. 1, 195-204.
39. Borbely, A. A. & Achermann, P. 1992 Concepts and models of sleep regulation: an overview. J. Sleep Res. 1, 63-79. (doi:10.1111/j.1365-2869.1992. tb00013.x)
40. Eastman, C. I., Mistlberger, R. E. & Rechtschaffen, A. 1984 Suprachiasmatic nuclei lesions eliminate circadian temperature and sleep rhythms in the rat. Physiol. Behav. 32, 357-368. (doi:10.1016/0031-9384(84)90248-8) (Pubitemid 14148105)
41. Edgar, D. M., Dement, W. C. & Fuller, C. A. 1993 Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation. J. Neurosci. 13, 1065-1079. (Pubitemid 23067594)
42. Mistlberger, R. E., Bergmann, B. M. & Rechtschaffen, A. 1987 Relationships among wake episode lengths, contiguous sleep episode lengths, and electroencephalographic delta waves in rats with suprachiasmatic nuclei lesions. Sleep 10, 12-24.
43. Mistlberger, R. E., Bergmann, B. M., Waldenar, W. & Rechtschaffen, A. 1983 Recovery sleep following sleep deprivation in intact and suprachiasmatic nuclei-lesioned rats. Sleep 6, 217-233. (Pubitemid 13005669)
44. Garris, P. A. & Wightman, R. M. 1994 Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo voltammetric study. J. Neurosci. 14, 442-450. (Pubitemid 24022128)
45. Saper, C. B., Lu, J., Chou, T. C. & Gooley, J. 2005 The hypothalamic integrator for circadian rhythms. Trends Neurosci. 28, 152-157. (doi:10.1016/j.tins.2004.12.009) (Pubitemid 40320761)
46. Thakkar, M. M., Strecker, R. E. & McCarley, R. W. 1998 Behavioral state control through differential serotonergic inhibition in the mesopontine cholinergic nuclei: a simultaneous unit recording and microdialysis study. J. Neurosci. 18, 5490-5497. (Pubitemid 28311963)
47. Saper, C. B., Chou, T. C. & Scammell, T. E. 2001 The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci. 24, 726-731. (doi:10.1016/S0166-2236(00)02002-6) (Pubitemid 33097540)
48. Massaquoi, S. G. & McCarley, R. W. 1992 Extension of the limit cycle reciprocal interaction model of REM cycle control. An integrated sleep control model. J. Sleep Res. 1, 138-143. (doi:10.1111/j.1365-2869.1992.tb00027.x)
49. Mistlberger, R. E. 2005 Circadian regulation of sleep in mammals: role of the suprachiasmatic nucleus. Brain Res. Rev. 49, 429-454. (doi:10.1016/j. brainresrev.2005.01.005) (Pubitemid 41546654)
50. Novak, C. M. & Nunez, A. A. 2000 A sparse projection from the suprachiasmatic nucleus to the sleep active ventrolateral preoptic area in the rat. Neuroreport 11, 93-96. (doi:10.1097/00001756-200001170-00019) (Pubitemid 30053397)
51. Chou, T. C., Scammell, T. E., Gooley, J. J., Gaus, S. E., Saper, C. B. & Lu, J. 2003 Critical role of dorsomedial hypothalamic nucleus in a wide range of behavioral circadian rhythms. J. Neurosci. 23, 10691-10 702.
52. Wilson, H. R. & Cowan, J. D. 1972 Excitatory and inhibitory interactions in localized populations of model neurons. Biophys. J. 12, 1-24. (doi:10.1016/S0006-3495(72)86068-5)
53. Dayan, P. & Abbott, L. F. 2001 Theoretical neuroscience: computational and mathematical modeling of neural systems. Cambridge, MA: MIT Press.
54. Deco, G., Jirsa, V. K., Robinson, P. A., Breakspear, M. & Friston, K. 2008 The dynamic brain: from spiking neurons to neural masses and cortical fields. PLoS Comput. Biol. 4, e1000092. (doi:10.1371/journal.pcbi.1000092)
55. Ermentrout, G. B. 1998 Neural networks as spatio-temporal pattern-forming systems. Rep. Prog. Phys. 61, 353-430. (doi:10.1088/0034-4885/61/4/002)
56. Basheer, R., Strecker, R. E., Thakkar, M. M. & McCarley, R. W. 2004 Adenosine and sleep-wake regulation. Prog. Neurobiol. 73, 379-396. (doi:10.1016/j.pneurobio.2004.06.004) (Pubitemid 39094087)
57. Huang, Z. L., Urade, Y. & Hayaishi, O. 2007 Prostaglandins and adenosine in the regulation of sleep and wakefulness. Curr. Opin. Pharmacol. 7, 33-38. (doi:10.1016/j.coph.2006.09.004) (Pubitemid 46238038)
58. Chamberlin, N. L., Arrigoni, E., Chou, T. C., Scammell, T. E., Greene, R. W. & Saper, C. B. 2003 Effects of adenosine on GABAergic synaptic inputs to identified ventrolateral preoptic neurons. Neuroscience 119, 913-918. (doi:10.1016/S0306-4522(03)00246-X) (Pubitemid 36776442)
59. Porkka-Heiskanen, T., Strecker, R. E. & McCarley, R. W. 2000 Brain site-specificity of extracellular adenosine concentration changes during sleep deprivation and spontaneous sleep: an in vivo microdialysis study. Neuroscience 99, 507-517. (doi:10.1016/S0306-4522(00)00220-7) (Pubitemid 30612453)
60. Scammell, T. E., Gerashchenko, D. Y., Mochizuki, T., McCarthy, M. T., Estabrooke, I. V., Sears, C. A., Saper, C. B., Urade, Y. & Hayaishi, O. 2001 An adenosine A2a agonist increases sleep and induces Fos in ventrolateral preoptic neurons. Neuroscience 107, 653-663. (doi:10.1016/S0306-4522(01)00383-9) (Pubitemid 33097501)
61. Strecker, R. E. et al. 2000 Adenosinergic modulation of basal forebrain and preoptic/anterior hypothalamic neuronal activity in the control of behavioral state. Behav. Brain Res. 115, 183-204. (doi:10.1016/S0166-4328(00) 00258-8)
62. Gallopin, T., Luppi, P. H., Cauli, B., Urade, Y., Rossier, J., Hayaishi, O., Lambolez, B. & Fort, P. 2005 The endogenous somnogen adenosine excites a subset of sleep-promoting neurons via A2A receptors in the ventrolateral preoptic nucleus. Neuroscience 134, 1377-1390. (doi:10.1016/j.neuroscience.2005. 05.045) (Pubitemid 41207385)
63. Morairty, S., Rainnie, D., McCarley, R. & Greene, R. 2004 Disinhibition of ventrolateral preoptic area sleep-active neurons by adenosine: a new mechanism for sleep promotion. Neuroscience 123, 451-457. (doi:10.1016/j.neuroscience.2003.08.066) (Pubitemid 38032921)
64. Takahashi, J. S., Hong, H. K., Ko, C. H. & McDearmon, E. L. 2008 The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat. Rev. Genet. 9, 764-775. (doi:10.1038/nrg2430)
65. Saeb-Parsy, K. & Dyball, R. E. 2003 Defined cell groups in the rat suprachiasmatic nucleus have different day/night rhythms of single-unit activity in vivo. J. Biol. Rhythms 18, 26-42. (doi:10.1177/0748730402239674) (Pubitemid 37187305)
66. Hokfelt, T. et al. 1986 Coexistence of neuronal messengers-an overview. Prog. Brain Res. 68, 33-70. (doi:10.1016/S0079-6123(08)60230-7)
67. Bartfai, T. 1985 Presynaptic aspects of the coexistence of classical neurotransmitters and peptides. Trends Pharm. Sci. 6, 331-334. (doi:10.1016/0165-6147(85)90153-1)
68. Lundberg, J. M. 1981 Evidence for coexistence of vasoactive intestinal polypeptide (VIP) and acetylcholine in neurons of cat exocrine glands. Morphological, biochemical and functional studies. Acta Physiol. Scand. Suppl. 496, 1-57.
69. Blanco-Centurion, C., Gerashchenko, D. & Shiromani, P. J. 2007 Effects of saporin-induced lesions of three arousal populations on daily levels of sleep and wake. J. Neurosci. 27, 14041-14 048. (doi:10.1523/JNEUROSCI.3217- 07.2007) (Pubitemid 351377867)
70. Ibuka, N., Inouye, S. I. & Kawamura, H. 1977 Analysis of sleep-wakefulness rhythms in male rats after suprachiasmatic nucleus lesions and ocular enucleation. Brain Res. 122, 33-47. (doi:10.1016/0006-8993(77)90660-6) (Pubitemid 8031615)
71. Lo, C. C., Chou, T., Penzel, T., Scammell, T. E., Strecker, R. E., Stanley, H. E. & Ivanov, P. Ch. 2004 Common scale-invariant patterns of sleep-wake transitions across mammalian species. Proc. Natl Acad. Sci. USA 101, 17545-17 548. (doi:10.1073/pnas.0408242101) (Pubitemid 39657440)
72. Blumberg, M. S., Coleman, C. M., Johnson, E. D. & Shaw, C. 2007 Developmental divergence of sleep-wake patterns in orexin knockout and wild-type mice. Eur. J. Neurosci. 25, 512-518. (doi:10.1111/j.1460-9568.2006.05292.x)
73. Diniz Behn, C. G., Kopell, N., Brown, E. N., Mochizuki, T. & Scammell, T. E. 2008 Delayed orexin signaling consolidates wakefulness and sleep: physiology and modeling. J. Neurophysiol. 99, 3090-3103. (doi:10.1152/jn.01243.2007)
74. Swihart, B. J., Caffo, B., Bandeen-Roche, K. & Punjabi, N. M. 2008 Characterizing sleep structure using the hypnogram. J. Clin. Sleep Med. 4, 349-355.
75. Marston, O. J., Williams, R. H., Canal, M. M., Samuels, R. E., Upton, N. & Piggins, H. D. 2008 Circadian and dark-pulse activation of orexin/hypocretin neurons. Mol. Brain 1, 19. (doi:10.1186/1756-6606-1-19)
76. Klisch, C., Inyushkin, A., Mordel, J., Karnas, D., Pevet, P. & Meissl, H. 2009 Orexin A modulates neuronal activity of the rodent suprachiasmatic nucleus in vitro. Eur. J. Neurosci. 30, 65-75. (doi:10.1111/j.1460-9568.2009.06794.x)
77. Mochizuki, T., Crocker, A., McCormack, S., Yanagisawa, M., Sakurai, T. & Scammell, T. E. 2004 Behavioral state instability in orexin knock-out mice. J. Neurosci. 24, 6291-6300. (doi:10.1523/JNEUROSCI.0586-04.2004) (Pubitemid 38944219)
78. Kantor, S., Mochizuki, T., Janisiewicz, A. M., Clark, E., Nishino, S. & Scammell, T. E. 2009 Orexin neurons are necessary for the circadian control of REM sleep. Sleep 32, 1127-1134.
79. Brown, T. M., Coogan, A. N., Cutler, D. J., Hughes, A. T. & Piggins, H. D. 2008 Electrophysiological actions of orexins on rat suprachiasmatic neurons in vitro. Neurosci. Lett. 448, 273-278. (doi:10.1016/j.neulet.2008.10. 058)
80. Postnova, S., Voigt, K. & Braun, H. A. 2009 A mathematical model of homeostatic regulation of sleep-wake cycles by hypocretin/orexin. J. Biol. Rhythms 24, 523-535. (doi:10.1177/0748730409346655)
81. Schwartz, M. D., Nunez, A. A. & Smale, L. 2004 Differences in the suprachiasmatic nucleus and lower subparaventricular zone of diurnal and nocturnal rodents. Neuroscience 127, 13-23. (doi:10.1016/j.neuroscience.2004.04. 049) (Pubitemid 38829147)
82. Hobson, J. A., McCarley, R. W. & Wyzinski, P. W. 1975 Sleep cycle oscillation: reciprocal discharge by two brainstem neuronal groups. Science 189, 55-58. (doi:10.1126/science.1094539)
83. Brown, R. E., McKenna, J. T., Winston, S., Basheer, R., Yanagawa, Y., Thakkar, M. M. & McCarley, R. W. 2008 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. 27, 352-363. (doi:10.1111/j.1460-9568.2008.06024.x)
84. Lu, J., Sherman, D., Devor, M. & Saper, C. B. 2006 A putative flip-flop switch for control of REM sleep. Nature 441, 589-594. (doi:10.1038/nature04767)
85. Luppi, P. H., Gervasoni, D., Verret, L., Goutagny, R., Peyron, C., Salvert, D., Leger, L. & Fort, P. 2006 Paradoxical (REM) sleep genesis: the switch from an aminergic-cholinergic to a GABAergic-glutamatergic hypothesis. J. Physiol. Paris 100, 271-283. (doi:10.1016/j.jphysparis.2007.05.006) (Pubitemid 47284832)
86. Sapin, E. et al. 2009 Localization of the brainstem GABAergic neurons controlling paradoxical (REM) sleep. PLoS ONE 4, e4272. (doi:10.1371/journal. pone.0004272)
87. Phillips, A. J. & Robinson, P. A. 2008 Sleep deprivation in a quantitative physiologically based model of the ascending arousal system. J. Theor. Biol. 255, 413-423. (doi:10.1016/j.jtbi. 2008.08.022)
88. Medanic, M. & Gillette, M. U. 1992 Serotonin regulates the phase of the rat suprachiasmatic circadian pacemaker in vitro only during the subjective day. J. Physiol. 450, 629-642.
89. Gillette, M. U. & Mitchell, J. W. 2002 Signaling in the suprachiasmatic nucleus: selectively responsive and integrative. Cell Tissue Res. 309, 99-107. (doi:10.1007/s00441-002-0576-1) (Pubitemid 34744032)
90. Earnest, D. J. & Turek, F. W. 1985 Neurochemical basis for the photic control of circadian rhythms and seasonal reproductive cycles: role for acetylcholine. Proc. Natl Acad. Sci. USA 82, 4277-4281. (doi:10.1073/pnas.82.12. 4277) (Pubitemid 15053627)
91. Summer, T. L., Ferraro, J. S. & McCormack, C. E. 1984 Phase-response and Aschoff illuminance curves for locomotor activity rhythm of the rat. Am. J. Physiol. 246, R299-R304. (Pubitemid 14147828)
92. Van Dongen, H. P. & Dinges, D. F. 2003 Investigating the interaction between the homeostatic and circadian processes of sleep-wake regulation for the prediction of waking neurobehavioural performance. J. Sleep Res. 12, 181-187. (doi:10.1046/j.1365-2869.2003.00357.x) (Pubitemid 37083016)
93. Borbely, A. A. & Achermann, P. 1999 Sleep homeostasis and models of sleep regulation. J. Biol. Rhythms 14, 559-570. (doi:10.1177/074873099129000894)
94. Bourgin, P., Lebrand, C., Escourrou, P., Gaultier, C., Franc, B., Hamon, M. & Adrien, J. 1997 Vasoactive intestinal polypeptide microinjections into the oral pontine tegmentum enhance rapid eye movement sleep in the rat. Neuroscience 77, 351-360. (doi:10.1016/S0306-4522(96)00455-1) (Pubitemid 27079607)
95. Riou, F., Cespuglio, R. & Jouvet, M. 1981 Hypnogenic properties of the vasoactive intestinal polypeptide in rats. C. R. Seances Acad. Sci. III 293, 679-682. (Pubitemid 12148113)
96. Mirmiran, M., Kruisbrink, J., Bos, N. P., Van der Werf, D. & Boer, G. J. 1988 Decrease of rapid-eye-movement sleep in the light by intraventricular application of a VIP-antagonist in the rat. Brain Res. 458, 192-194. (doi:10.1016/0006-8993(88)90516-1)
97. Shinohara, K., Honma, S., Katsuno, Y., Abe, H. & Honma, K. 1995 Two distinct oscillators in the rat suprachiasmatic nucleus in vitro. Proc. Natl Acad. Sci. USA 92, 7396-7400. (doi:10.1073/pnas.92.16.7396)
98. Aguilar-Roblero, R., Verduzco-Carbajal, L., Rodriguez, C., Mendez-Franco, J., Moran, J. & de la Mora, M. P. 1993 Circadian rhythmicity in the GABAergic system in the suprachiasmatic nuclei of the rat. Neurosci. Lett. 157, 199-202. (doi:10.1016/0304-3940(93)90736-5) (Pubitemid 23245528)
99. Francois-Bellan, A. M., Kachidian, P., Dusticier, G., Tonon, M. C., Vaudry, H. & Bosler, O. 1990 GABA neurons in the rat suprachiasmatic nucleus: involvement in chemospecific synaptic circuitry and evidence for GAD-peptide colocalization. J. Neurocytol. 19, 937-947. (doi:10.1007/BF01186821)
100. Saint-Mleux, B., Bayer, L., Eggermann, E., Jones, B. E., Muhlethaler, M. & Serafin, M. 2007 Suprachiasmatic modulation of noradrenaline release in the ventrolateral preoptic nucleus. J. Neurosci. 27, 6412-6416. (doi:10.1523/JNEUROSCI.1432-07.2007) (Pubitemid 46920362)
101. Aschoff, J. 1966 Circadian activity pattern with two peaks. Ecology 47, 657-662. (doi:10.2307/1933949)
102. Kuwabara, N., Seki, K. & Aoki, K. 1986 Circadian, sleep and brain temperature rhythms in cats under sustained daily light-dark cycles and constant darkness. Physiol. Behav. 38, 283-289. (doi:10.1016/0031-9384(86)90164-2) (Pubitemid 16028153)
103. Daan, S. & Berde, C. 1978 Two coupled oscillators: simulations of the circadian pacemaker in mammalian activity rhythms. J. Theor. Biol. 70, 297-313. (doi:10.1016/0022-5193(78)90378-8) (Pubitemid 8266939)