Suprachiasmatic nucleus and autonomic nervous system influences on awakening from sleep

International Review of Neurobiology

Volumn 93, Issue C, 2010, Pages 91-107

  Kalsbeek, Andries ^a,b   Yi, Chun Xia ^a,b   Fleur, Susanne E la ^a   Buijs, Ruud M ^c   Fliers, Eric ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Autonomic Nervous System; Circadian; Corticosterone; Cortisol; Glucose; Hypothalamus; Liver; Suprachiasmatic nucleus; Vasopressin

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; GLUCOSE; HYDROCORTISONE; MELATONIN; OREXIN;

AUTONOMIC NERVOUS SYSTEM FUNCTION; BEDTIME DOSAGE; BEHAVIOR CONTROL; BOOK; CARDIOVASCULAR EFFECT; CIRCADIAN RHYTHM; CLINICAL TRIAL; ENERGY YIELD; ESSENTIAL HYPERTENSION; GLUCOSE BLOOD LEVEL; HOMEOSTASIS; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; NERVE PROJECTION; NONHUMAN; PARASYMPATHETIC FUNCTION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SLEEP WAKING CYCLE; SUPRACHIASMATIC NUCLEUS; SYMPATHETIC FUNCTION; WAKEFULNESS;

EID: 77958137021     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0074-7742(10)93004-3     Document Type: Chapter

References (87)

1. Akhtar R.A., Reddy A.B., Maywood E.S., Clayton J.D., King V.M., Smith A.G., Gant T.W., Hastings M.H., Kyriacou C.P. Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr. Biol. 2002, 12:540-550.
2. Alam M.N., Kumar S., Bashir T., Suntsova N., Methippara M.M., Szymusiak R., McGinty D. GABA-mediated control of hypocretin- but not melanin-concentrating hormone-immunoreactive neurones during sleep in rats. J. Physiol. 2005, 563:569-582.
3. Avidor R., Eilam R., Malach R., Gozes I. VIP-mRNA is increased in hypertensive rats. Brain Res. 1989, 503:304-307.
4. Bellinger L.L., Mendel V.E., Moberg G.P. Circadian insulin, GH, prolactin, corticosterone and glucose rhythms in fed and fasted rats. Horm. Metab. Res. 1975, 7:132-135.
5. Bolli G.B., De Feo P., De Cosmo S., Perriello G., Ventura M.M., Calcinaro F., Lolli C., Campbell P., Brunetti P., Gerich J.E. Demonstration of a dawn phenomenon in normal human volunteers. Diabetes 1984, 33:1150-1153.
6. Born J., Hansen K., Marshall L., Mölle M., Fehm H.L. Timing the end of nocturnal sleep. Nature 1999, 397:29-30.
7. Buijs R.M., Hou Y.X., Shinn S., Renaud L.P. Ultrastructural evidence for intra- and extranuclear projections of GABAergic neurons of the suprachiasmatic nucleus. J. Comp. Neurol. 1994, 340:381-391.
8. Buijs R.M., Kalsbeek A. Hypothalamic integration of central and peripheral clocks. Nat. Rev. Neurosci. 2001, 2:521-526.
9. Buijs R.M., Markman M., Nunes-Cardoso B., Hou Y.-X., Shinn S. Projections of the suprachiasmatic nucleus to stress-related areas in the rat hypothalamus: A light and electron microscopic study. J. Comp. Neurol. 1993, 335:42-54.
10. Buijs R.M., Van Eden C.G. The integration of stress by the hypothalamus, amygdala and prefrontal cortex: Balance between the autonomic nervous system and the neuroendocrine system. Prog. Brain Res. 2000, 126:117-132.
11. Buijs R.M., Wortel J., Hou Y.X. Colocalization of gamma-aminobutyric acid with vasopressin, vasoactive intestinal peptide, and somatostatin in the rat suprachiasmatic nucleus. J. Comp. Neurol. 1995, 358:343-352.
12. Buijs R.M., Wortel J., Van Heerikhuize J.J., Feenstra M.G.P., Ter Horst G.J., Romijn H.J., Kalsbeek A. Anatomical and functional demonstration of a multisynaptic suprachiasmatic nucleus adrenal (cortex) pathway. Eur. J. Neurosci. 1999, 11:1535-1544.
13. Cailotto C., La Fleur S.E., Van Heijningen C., Wortel J., Kalsbeek A., Feenstra M., Pevet P., Buijs R.M. The suprachiasmatic nucleus controls the daily variation of plasma glucose via the autonomic output to the liver: Are the clock genes involved?. Eur. J. Neurosci. 2005, 22:2531-2540.
14. Cailotto C., Lei J., van der Vliet J., van Heijningen C., van Eden C.G., Kalsbeek A., Pevet P., Buijs R.M. Effects of nocturnal light on (clock) gene expression in peripheral organs: A role for the autonomic innervation of the liver. PLoS ONE 2009, 4:e5650.
15. Cailotto C., van Heijningen C., van der Vliet J., van der Plasse G., Habold C., Kalsbeek A., Pevet P., Buijs R.M. Daily rhythms in metabolic liver enzymes and plasma glucose require a balance in the autonomic output to the liver. Endocrinology 2008, 149:1914-1925.
16. Cheng M.Y., Bullock C.M., Li C., Lee A.G., Bermak J.C., Belluzzi J., Weaver D.R., Leslie F.M., Zhou Q.Y. Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 2002, 417:405-410.
17. Cuesta M., Clesse D., Pevet P., Challet E. From daily behavior to hormonal and neurotransmitters rhythms: Comparison between diurnal and nocturnal rat species. Horm. Behav. 2009, 55:338-347.
18. Dallman M.F., Strack A.M., Akana S.F., Bradbury M.J., Hanson E.S., Scribner K.A., Smith M. Feast and Famine-Critical role of glucocorticoids with insulin in daily energy flow. Front. Neuroendocrinol. 1993, 14:303-347.
19. Dardente H., Menet J.S., Challet E., Tournier B.B., Pévet P., Masson-Pévet M. Daily and circadian expression of neuropeptides in the suprachiasmatic nuclei of nocturnal and diurnal rodents. Mol. Brain Res. 2004, 124:143-151.
20. de la Iglesia H.O., Meyer J., Carpino A., Schwartz W.J. Antiphase oscillation of the left and right suprachiasmatic nuclei. Science 2000, 290:799-801.
21. de la Iglesia H.O., Meyer J., Schwartz W.J. Lateralization of circadian pacemaker output: Activation of left-and right-sided luteinizing hormone-releasing hormone neurons involves a neural rather than a humoral pathway. J. Neurosci. 2003, 23:7412-7414.
22. Durgan D.J., Young M.E. The cardiomyocyte circadian clock: Emerging roles in health and disease. Circ. Res. 2010, 106:647-658.
23. Evans C., Chalmers J., Capewell S., Redpath A., Finlayson A., Boyd J., Pell J., McMurray J., Macintyre K., Graham L. "I don't like Mondays"-Day of the week of coronary heart disease deaths in Scotland: Study of routinely collected data. BMJ 2000, 320:218-219.
24. Goncharuk V.D., van Heerikhuize J.J., Dai J.P., Swaab D.F., Buijs R.M. Neuropeptide changes in the suprachiasmatic nucleus in primary hypertension indicate functional impairment of the biological clock. J. Comp. Neurol. 2001, 431:320-330.
25. Goncharuk V.D., Van Heerikhuize J., Swaab D.F., Buijs R.M. Paraventricular nucleus of the human hypothalamus in primary hypertension: Activation of corticotropin- releasing hormone neurons. J. Comp. Neurol. 2002, 443:321-331.
26. Guo H., Brewer J.M., Lehman M.N., Bittman E.L. Suprachiasmatic regulation of circadian rhythms of gene expression in hamster peripheral organs: Effects of transplanting the pacemaker. J. Neurosci. 2006, 26:6406-6412.
27. Hahm S.H., Eiden L.E. Five discrete cis-active domains direct cell type-specific transcription of the vasoactive intestinal peptide (VIP) gene. J. Biol. Chem. 1998, 273:17086-17094.
28. Hastings M. Circadian rhythms: Peering into the molecular clockwork. J. Neuroendocrinol. 1995, 7:331-340.
29. Hatcher N.G., Atkins N., Annangudi S.P., Forbes A.J., Kelleher N.L., Gillette M.U., Sweedler J.V. Mass spectrometry-based discovery of circadian peptides. Proc. Natl. Acad. Sci. U.S.A 2008, 105:12527-12532.
30. Hendrickson A.E., Wagoner N., Cowan W.M. An autoradiographic and electron microscopic study of retino-hypothalamic connections. Z. Zellforsch. 1972, 135:1-26.
31. Hermes M.L.H.J., Ruijter J.M., Klop A., Buijs R.M., Renaud L.P. Vasopressin increases GABAergic inhibition of rat hypothalamic paraventricular nucleus neurons in vitro. J. Neurophysiol. 2000, 83:705-711.
32. Janszky I., Ljung R. Shifts to and from daylight saving time and incidence of myocardial infarction. N. Engl. J. Med. 2008, 359:1966-1968.
33. Jasper M.S., Engeland W.C. Splanchnic neural activity modulates ultradian and circadian rhythms in adrenocortical secretion in awake rats. Neuroendocrinology 1994, 59:97-109.
34. Jin X.W., Shearman L.P., Weaver D.R., Zylka M.J., De Vries G.J., Reppert S.M. A molecular mechanism regulating rhythmic output from the suprachiasmatic circadian clock. Cell 1999, 96:57-68.
35. Joëls M., Urban I.J.A. The effect of microiontophoretically applied vasopressin and oxytocin on single neurones in the septum and dorsal hippocampus of the rat. Neurosci. Lett. 1982, 33:79-84.
36. Jolin T., Montes A. Daily rhythm of plasma glucose and insulin levels in rats. Horm. Res. 1973, 4:153-156.
37. Kalsbeek A., Buijs R.M. Output pathways of the mammalian suprachiasmatic nucleus: Coding circadian time by transmitter selection and specific targeting. Cell Tissue Res. 2002, 309:109-118.
38. Kalsbeek A., Buijs R.M., Van Heerikhuize J.J., Arts M. Van Der Woude TP: Vasopressin-containing neurons of the suprachiasmatic nuclei inhibit corticosterone release. Brain Res. 1992, 580:62-67.
39. Kalsbeek A., Fliers E., Hofman M.A., Swaab D.F., Buijs R.M. Vasopressin and the output of the hypothalamic biological clock. J. Neurogenet. 2010, 22:362-372.
40. Kalsbeek A., Foppen E., Schalij I., Van Heijningen C., van der Vliet J., Fliers E., Buijs R.M. Circadian control of the daily plasma glucose rhythm: An interplay of GABA and glutamate. PLoS ONE 2008, 3:e3194.
41. Kalsbeek A., La Fleur S.E., Van Heijningen C., Buijs R.M. Suprachiasmatic GABAergic inputs to the paraventricular nucleus control plasma glucose concentrations in the rat via sympathetic innervation of the liver. J. Neurosci. 2004, 24:7604-7613.
42. Kalsbeek A., Van Der Vliet J., Buijs R.M. Decrease of endogenous vasopressin release necessary for expression of the circadian rise in plasma corticosterone: A reverse microdialysis study. J. Neurogenet. 1996, 8:299-307.
43. Kalsbeek A., Van Heerikhuize J.J., Wortel J., Buijs R.M. A diurnal rhythm of stimulatory input to the hypothalamo-pituitary-adrenal system as revealed by timed intrahypothalamic administration of the vasopressin V1 antagonist. J. Neurosci. 1996, 16:5555-5565.
44. Kalsbeek A., Verhagen L.A., Schalij I., Foppen E., Saboureau M., Bothorel B., Buijs R.M., Pevet P. Opposite actions of hypothalamic vasopressin on circadian corticosterone rhythm in nocturnal versus diurnal species. Eur. J. Neurosci. 2008, 27:818-827.
45. Kita Y., Shiozawa N., Jin W.H., Majewski R.R., Besharse J.C., Greene A.S., Jacob H.J. Implications of circadian gene expression in kidney, liver and the effects of fasting on pharmacogenomic studies. Pharmacogenetics 2002, 12:55-65.
46. Kloner R.A., Poole W.K., Perritt R.L. When throughout the year is coronary death most likely to occur? A 12-year population-based analysis of more than 220,000 cases. Circulation 1999, 100:1630-1634.
47. Kow L.M., Pfaff D.W. Vasopressin excites ventromedial hypothalamic glucose-responsive neurons in vitro. Physiol. Behav. 1986, 37:153-158.
48. Kramer A., Yang F.C., Snodgrass P., Li X.D., Scammell T.E., Davis F.C., Weitz C.J. Regulation of daily locomotor activity and sleep by hypothalamic EGF receptor signaling. Science 2001, 294:2511-2515.
49. Kraves S., Weitz C.J. A role for cardiotrophin-like cytokine in the circadian control of mammalian locomotor activity. Nat. Neurosci. 2006, 9:212-219.
50. La Fleur S.E., Kalsbeek A., Wortel J., Buijs R.M. An SCN generated rhythm in basal glucose levels. J. Neurogenet. 1999, 11:643-652.
51. La Fleur S.E., Kalsbeek A., Wortel J., Fekkes M.L., Buijs R.M. A daily rhythm in glucose tolerance. A role for the suprachiasmatic nucleus. Diabetes 2001, 50:1237-1243.
52. Lehman M.N., Silver R., Gladstone W.R., Kahn R.M., Gibson M., Bittman E.L. Circadian rhythmicity restored by neural transplant. Immunocytochemcical characterization of the graft and its integration with the host brain. J. Neurosci. 1987, 7:1626-1638.
53. Meyer-Bernstein E.L., Jetton A.E., Matsumoto S.I., Markuns J.F., Lehman M.N., Bittman E.L. Effects of suprachiasmatic transplants on circadian rhythms of neuroendocrine function in golden hamsters. Endocrinology 1999, 140:207-218.
54. Moore R.Y. Neural control of the pineal gland. Behav. Brain Res. 1996, 73:125-130.
55. Moore R.Y., Eichler V.B. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res. 1972, 42:201-206.
56. Moore R.Y., Lenn N.J. A retinohypothalamic projection in the rat. J. Comp. Neurol. 1972, 146:1-9.
57. Mul J.D., Yi C.X., van den Berg S.A., Ruiter M., Toonen P.W., van der Elst M.C., Voshol P.J., Ellenbroek B.A., Kalsbeek A., la Fleur S.E., Cuppen E. Pmch expression during early development is critical for normal energy homeostasis. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E477-E488.
58. Nonogaki K. New insights into sympathetic regulation of glucose and fat metabolism. Diabetologia 2000, 43:533-549.
59. Oishi K., Miyazaki K., Kadota K., Kikuno R., Nagase T., Atsumi G., Ohkura N., Azama T., Mesaki M., Yukimasa S., Kobayashi H., Iitaka C., Umehara T., Horikoshi M., Kudo T., Shimizu Y., Yano M., Monden M., Machida K., Matsuda J., Horie S., Todo T., Ishida N. Genome-wide expression analysis of mouse liver reveals CLOCK-regulated circadian output genes. J. Biol. Chem. 2003, 278:41519-41527.
60. Perreau-Lenz S., Pévet P., Buijs R.M., Kalsbeek A. The biological clock: The bodyguard of temporal homeostasis. Chronobiol. Int. 2004, 21:1-25.
61. Peters R.V., Zoeller R.T., Hennessey A.C., Stopa E.G., Anderson G., Albers H.E. The control of circadian rhythms and the levels of vasoactive intestinal peptide messenger RNA in the suprachiasmatic nucleus are altered in spontaneously hypertensive rats. Brain Res. 1994, 639:217-227.
62. Puschel G.P. Control of hepatocyte metabolism by sympathetic and parasympathetic hepatic nerves. Anat. Rec. 2004, 280A:854.
63. Ralph M.R., Foster R.G., Davis F.C., Menaker M. Transplanted suprachiasmatic nucleus determines circadian period. Science 1990, 247:975-978.
64. Rimmele U., Meier F., Lange T., Born J. Suppressing the morning rise in cortisol impairs free recall. Learn. Mem. 2010, 17:186-190.
65. Scheer F.A., Van Montfrans G.A., van Someren E.J., Mairuhu G., Buijs R.M. Daily nighttime melatonin reduces blood pressure in male patients with essential hypertension. Hypertension 2004, 43:192-197.
66. Shea S.A., Hilton M.F., Orlova C., Ayers R.T., Mantzoros C.S. Independent circadian and sleep/wake regulation of adipokines and glucose in humans. J. Clin. Endocrinol. Metab. 2005, 90:2537-2544.
67. Shimazu T. Neuronal regulation of hepatic glucose metabolism in mammals. Diabetes Metab. Rev. 1987, 3:185-206.
68. Shiuchi T., Haque M.S., Okamoto S., Inoue T., Kageyama H., Lee S., Toda C., Suzuki A., Bachman E.S., Kim Y.B., Sakurai T., Yanagisawa M., Shioda S., Imoto K., Minokoshi Y. Hypothalamic orexin stimulates feeding-associated glucose utilization in skeletal muscle via sympathetic nervous system. Cell Metab. 2009, 10:466-480.
69. Silver R., Lesauter J., Tresco P.A., Lehman M. A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 1996, 382:810-813.
70. Stephan F.K., Zucker I. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc. Natl. Acad. Sci. U.S.A. 1972, 69:1583-1586.
71. Sujino M., Masumoto K., Yamaguchi S., van der Horst G.T.J., Okamura H., Inouye S.I.T. Suprachiasmatic nucleus grafts restore circadian behavioral rhythms of genetically arrhythmic mice. Curr. Biol. 2003, 13:664-668.
72. Takahashi J.S. Circadian clock genes are ticking. Science 1992, 258:238-240.
73. Takahashi J.S., Hong H.K., Ko C.H., McDearmon E.L. The genetics of mammalian circadian order and disorder: Implications for physiology and disease. Nat. Rev. Genet. 2008, 9:764-775.
74. Takeda N., Maemura K. Cardiovascular disease, chronopharmacotherapy, and the molecular clock. Adv. Drug Deliv. Rev. 2010, 62:956-966.
75. Teclemariam-Mesbah R., Ter Horst G.J., Postema F., Wortel J., Buijs R.M. Anatomical demonstration of the suprachiasmatic nucleus-Pineal pathway. J. Comp. Neurol. 1999, 406:171-182.
76. Tsujino N., Sakurai T. Orexin/hypocretin: A neuropeptide at the interface of sleep, energy homeostasis, and reward system. Pharmacol. Rev. 2009, 61:162-176.
77. Van Cauter E., Polonsky K.S., Scheen A.J. Roles of circadian rhythmicity and sleep in human glucose regulation. Endocr. Rev. 1997, 18:716-738.
78. van den Hoek A.M., van Heijningen C., Schroder-van der Elst J.P., Ouwens D.M., Havekes L.M., Romijn J.A., Kalsbeek A., Pijl H. Intracerebroventricular administration of neuropeptide Y induces hepatic insulin resistance via sympathetic innervation. Diabetes 2008, 57:2304-2310.
79. Van den Top M., Nolan M.F., Lee K., Richardson P.J., Buijs R.M., Davies C., Spanswick D. Orexins induce increased excitability and synchronisation of rat sympathetic preganglionic neurones. J. Physiol. 2003, 548:809-821.
80. Vogelbaum M.A., Menaker M. Temporal chimeras produced by hypothalamic transplants. J. Neurosci. 1992, 12:3619-3627.
81. Vrang N., Larsen P.J., MaeC6;ller M., Mikkelsen J.D. Topographical organization of the rat suprachiasmatic-paraventricular projection. J. Comp. Neurol. 1995, 353:585-603.
82. Vrang N., Larsen P.J., Mikkelsen J.D. Direct projection from the suprachiasmatic nucleus to hypophysiotrophic corticotropin-releasing factor immunoreactive cells in the paraventricular nucleus of the hypothalamus demonstrated by means of Phaseolus vulgaris-leucoagglutinin tract tracing. Brain Res. 1995, 684:61-69.
83. Vrang N., Mikkelsen J.D., Larsen P.J. Direct link from the suprachiasmatic nucleus to hypothalamic neurons projecting to the spinal cord: A combined tracing study using cholera toxin subunit B and Phaseolus vulgaris-leucoagglutinin. Brain Res. Bull. 1997, 44:671-680.
84. Watts A.G., Swanson L.W. Efferent projections of the suprachiasmatic nucleus: II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat. J. Comp. Neurol. 1987, 258:230-252.
85. Watts A.G., Swanson L.W., Sanchez-Watts G. Efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat. J. Comp. Neurol. 1987, 258:204-229.
86. Weaver D.R. The suprachiasmatic nucleus: A 25-year retrospective. J. Biol. Rhythm. 1998, 13:100-112.
87. Yi C.X., Serlie M.J., Ackermans M.T., Foppen E., Buijs R.M., Sauerwein H.P., Fliers E., Kalsbeek A. A major role for perifornical orexin neurons in the control of glucose metabolism in rats. Diabetes 2009, 58:1998-2005.