Interactions between Sleep, Other Body Rhythms, Immune Responses, and Exercise

Canadian Journal of Applied Physiology

Volumn 22, Issue 2, 1997, Pages 95-116

  Shephard, Roy J ^a   Shek, Pang N ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Circadian rhythms; Cytokines; Hormones; Hypothalamus; Leukocytes; Melatonin

Indexed keywords

MELATONIN;

CIRCADIAN RHYTHM; ENDOCRINE GLAND; EXERCISE; HUMAN; HYPOTHALAMUS; IMMUNE SYSTEM; LEUKOCYTE; PHYSIOLOGY; REVIEW; SLEEP;

CIRCADIAN RHYTHM; ENDOCRINE GLANDS; EXERCISE; HUMANS; HYPOTHALAMUS; IMMUNE SYSTEM; LEUKOCYTES; MELATONIN; SLEEP;

EID: 0031112902     PISSN: 10667814     EISSN: None     Source Type: Journal    
DOI: 10.1139/h97-009     Document Type: Review

References (117)

1. Abo, T., Kawate, T., Itoh, K., and Kumagai, K. (1981). Studies on the bioperiodicity of the immune response: 1. Circadian rhythms of human T, B and K cell traffic in the peripheral blood. J. Immunol. 126: 1360-1363.
2. Ahnve, S, Theorell, T., Åkerstedt, T., Fröberg, J.E., and Halberg, F. (1981). Circadian variations in cardiovascular parameters during sleep deprivation. Eur. J. Appl. Physiol. 46: 9-19.
3. Angeli, A., Gatti, G., and Masera, R. (1994). Chronobiology of the hypothalamic-pituitary-adrenal and renin-angiotensin-aldosterone systems. In: Y. Touitou and E. Haus (Eds.), Biologic Rhythms in Clinical and Laboratory Medicine, pp. 292-314. Berlin: Springer Verlag.
4. Angeli, A., Gatti, G., Sartori, M.L., and Masera, R.G. (1992). Chronobiological aspects of the neuroendocrine-immune network. Regulation of human natural killer (NK) cell activity as a model. Chronobiologia 19: 93-110.
5. Baekeland, F., and Lasky, R. (1966). Exercise and sleep patterns in college athletes. Percept. Motor Skills 23: 1203-1207.
6. Barinaga, M. (1996). Researchers find the reset button for the fruit fly clock. Science 271: 1671-1672.
7. Bertouch, J.V., Roberts-Thomson, P.J., and Bradley, J. (1983). Diurnal variation of lymphocyte subsets identified by monoclonal antibodies. Br. Med. J. 286: 1171-1172.
8. Blomquist, C.H., and Holt, J.P. (1994). Chronobiology of the hypothalamic-pituitary-gonadal axis in men and women. In: Y. Touitou and E. Haus (Eds.), Biological Rhythms in Clinical and Laboratory Medicine, pp. 315-329. Berlin: Springer Verlag.
9. Brabant, G., Prank, K., and Schöfl, C. (1992). Pulsatile patterns in hormone secretion. Trends Endocrinol. Metab. 3: 183-190.
10. Bratescu, A., and Teoderescu, M. (1981). Circannual variations in the B cell/T cell ratio in normal human peripheral blood. J. Allergy Clin. Immunol. 68: 273-280.
11. Brosschot, J.F., Benschop, R.J., Godaert, G.L.R., Olff, M., de Smet, M., Heijnen, C.J., and Ballieux, R.E. (1994). Influence of life stress on immunological reactivity to mild psychological stress. Psychosom. Med. 56: 216-224.
12. Buguet, A., and Lonsdorfer, J. (1987). Sommeil et exercice physique chez l'homme. Sci. Sports 2: 193-202.
13. Buguet, A., Roussel, B., and Radomski, M.W. (1985). Sleep quality in adverse environments depends on individual stress reaction. In: W.P. Koella, E. Rüther, and H. Schulz (Eds.), Sleep '84, pp. 72-73. Stuttgart: Gustav Fischer Verlag.
14. Bunnell, D.E., Bevier, W., and Horvath, S.M. (1983a). Effects of exhaustive exercise on the sleep of men and women. Psychophysiol. 20: 50-58.
15. Bunnell, D.E., Bevier, W., and Horvath, S.M. (1983b). Nocturnal sleep, cardiovascular function and adrenal activity following maximal capacity exercise. Electroenceph. Clin. Neurophysiol. 56: 186-189.
16. Cannon, J.G. (1993). Exercise and resistance to infection. J. Appl. Physiol. 74: 973-981.
17. Canon, C., and Lévi, F. (1994). Immune system in relation to cancer. In: Y. Touitou and E. Haus (Eds.), Biological Rhythms in Clinical and Laboratory Medicine, pp. 635-647. Berlin: Springer Verlag.
18. Caradante, F., Angeli, A., Candiani, G.B., Crosignani, P.G., Dammacco, F., de Cecco, L., Marrama, P., Massobrio, M., and Martini, L. (1989). Rhythms in the ovulatory cycle: LH, FSH, estradiol and progesterone. Chronobiologia 16: 353-363.
19. Carrere, V., Dorfman, P., and Bastide, M. (1988). Evaluation of various factors influencing the action of mouse interferon on the chemiluminescence of mouse peritoneal macrophages. Ann. Rev. Chronopharm. 5: 9-12.
20. Cauter, E.V. (1990). Diurnal and ultradian rhythms in human endocrine function: A minireview. Horm. Res. 34: 45-53.
21. Clark, J.H., and Conlee, R.H. (1979). Muscle and liver glycogen content: Diurnal variation and endurance. J. Appl. Physiol. 47: 425-428.
22. Cohen, M.C., and Muller, J.E. (1994). Chronobiology of acute myocardial infarction. Lab. Med. 25: 494-500.
23. Dale, D.C., and Hammond, W.P. (1988). Cyclic neutropenia: A clinical review. Blood Rev. 2: 178-185.
24. Davies, C.T.M., and Sargeant, A. (1975). Circadian variation in physiological responses to exercise on a stationary cycle ergometer. Br. J. Industr. Med. 32: 110-114.
25. Dawson, D., Encel, N., and Lushington, K. (1995). Improving adaptation to simulated night shift: Timed exposure to bright light versus daytime melatonin administration. Sleep 18: 11-21.
26. Debry, G., Bleyer, R., and Reinberg, A. (1975). Circadian, circa annual and other rhythms in spontaneous nutrient and calorie intake of healthy four-year olds. Diabetes Metab. 1: 91-99.
27. Dhabhar, F.S., Miller, A.H., Stein, M., McEwen, B.S., and Spencer, R.L. (994). Diurnal and acute stress-induced changes in distribution of peripheral blood leukocyte subpopulations. Brain Behav. Immun. 8: 66-79.
28. Dinarello, C.A. (1984). Interleukin-1. Rev. Infect. Dis. 6: 51-95.
29. Ding, J.M., Chen, D., Weber, E.T., Faiman, L.E., Rea, M.A., and Gillette, M.U. (1994). Resetting the biological clock: Mediation of nocturnal circadian shifts by glutamate and NO. Science 266: 1713-1717.
30. Eskola, J., Frey, H., Molnar, G., and Soppi, E. (1976). Biological rhythm of cell-mediated immunity in man. Clin. Exp. Immunol. 26: 253-257.
31. Fernandes, G. (1994). Chronobiology of immune functions: Cellular and immune aspects. In: Y. Touitou and E, Haus (Eds.), Biologic Rhythms in Clinical and Laboratory Medicine, pp. 493-503. Berlin: Springer Verlag.
32. Fernandes, G., Halberg, F., Halberg, E., Miranda, M., Yunis, E.J., and Good, R.A. (1981). Murine circadian rhythm in natural cell-mediated cytotoxicity against lymphoma cells and chronoimmunology. In: C.A. Walker, K.F.A. Soliman, and C.M. Winget (Eds.), Chronopharmacology and Chronotherapeutics. Tallahassee, FL: A & M. University Foundation, pp. 233-245.
33. French, J. (1995). Circadian rhythms, jet lag and the athlete. In: Roy J. Shephard and J. Torg (Eds.), Current Therapy in Sports Medicine III, pp. 596-600. Philadelphia: Decker/ Mosby.
34. Fry, R.W., Grove, J.R., Morton, A.R., Zeroni, P.M., Gaudieri, S., and Keast, D. (1994). Psychological and immunological correlates of acute overtraining. Br. J. Sports Med. 28: 241-246.
35. Fry, R.W., Morton, A.R., Garcia-Webb, P., and Keast, D. (1991). Monitoring exercise stress by changes in metabolic and hormonal responses over a 24-hour period. Eur. J. Appl. Physiol. 63: 228-234.
36. Fujiwara, S., Shinkai, S., Kurokawa, Y., and Watanabe, T. (1992). The acute effects of experimental short-term evening and night shifts on human circadian rhythm: The oral temperature, heart rate, serum cortisol and urinary catecholamine levels. Int. Arch. Occup. Health 63: 409-418.
37. Gatti, G., Angeli, A., and Carignola, R. (1994). Chronobiology of endocrine-immune interactions. In: Y. Touitou and E. Haus (Eds.), Biologic Rhythms in Clinical and Laboratory Medicine, pp. 363-374. Berlin: Springer Verlag.
38. Gatti, G., Carignola, R., Masera, R., Sartori, M.L., Salvadori, A., Magro, E., and Angeli, A. (1989). Circadian-stage specified effects of melatonin on human natural killer (NK) cell activity: In vitro and in vivo studies. Ann. Rev. Chronopharm. 5: 25-28.
39. Gatti, G., Cavallo, R., Delponte, D., Masera, R., Carignola, R., Caradante, F., and Angeli, A. (1987). Circadian changes of human natural killer (NK) cells and their in vitro susceptibility to cortisol inhibition. Ann. Rev. Chronopharmacol. 3: 75-78.
40. Gatti, G., Cavallo, R., Sartori, M.L., Carignola, R., Masera, R., Delponte, D., Salvadori, A., and Angeli, A. (1988). Circadian variations of interferon-induced enhancement of natural killer (NK) cell activity. Cancer Detect. Prevent. 12: 431-438.
41. Gervais, P., Reinberg, A., Gervais, C., Smolensky, M., and DeFrance, O. (1977). Twenty four hour rhythm in the bronchial hyperactivity to house dust in asthmatics. J. Allergy Clin. Immunol. 59: 207-213.
42. Haus, E. (1994). Chronobiology of circulating blood cells and platelets. In: Y. Touitou and E. Haus (Eds.), Biological Rhythms in Clinical and Laboratory Medicine, pp. 504-526. Berlin: Springer Verlag.
43. Haus, E., and Touitou, Y. (1994). Principles of chronobiology. In: Y. Touitou and E. Haus (Eds.), Biological Rhythms in Clinical and Laboratory Medicine, pp. 6-34. Berlin: Springer Verlag.
44. Hayashi, O., and Kichuki, M. (1982). The effects of the light-dark cycle on humoral and cell-mediated immune response of mice. Chronobiologia 3: 291-300.
45. Hill, C.M., and Hill, D.W. (1991). Influence of time of day on responses to the profile of mood states [Abstract]. Percept. Mot. Skills 72: 434.
46. Hohagen, F., Timmer, J., Weyerbrook, A., Fritsch-Montero, R., Ganter, U., Krieger, S., Berger, M., and Bauer, J. (1993). Cytokine production during sleep and wakefulness and its relationship to cortisol in healthy humans. Neuropsychobiol. 28: 9-16.
47. Homo-Delarche, F. (1984). Gluco-corticoid receptors and steroid sensitivity in normal and neoplastic human lymphoid tissue: A review. Cancer Res. 44: 431-437.
48. Horne, J.A. (1988). Why We Sleep. Oxford: Oxford University Press.
49. Horne, J.A., and Reid, A.J. (1985). Night-time sleep EEG changes following body heating in a warm bath. Electroenceph. Clin. Neurophysiol. 60: 154-157.
50. Horne, J.A., and Staff, L.H.E. (1983). Exercise and sleep: Body-heating effects. Sleep 6: 36-46.
51. Indiveri, F., Pierri, I., Rogna, S., Poggi, P., Montaldo, P., Romano, R., Pende, A., Morgano, A., Barabino, A., and Ferrone, S. (1985). Circadian variations of autologous mixed lymphocyte reactions and endogenous cortisol. J. Immunol. Methods 82: 17-24.
52. Inouye, S.T., and Kawamura, H. (1982). Characteristics of a circadian pacemaker in the suprachiasmatic nucleus. J. Comp. Physiol. 146: 153-160.
53. Johnson, R.F., Morin, L.P., and Moore, R.Y. (1988). Retinohypothalamic projections in the hamster and rat, demonstrated using choleratoxin. Brain Res. 462: 301-312.
54. Kern, W., Perras, B., Wodick, R., Fehm, H.L., and Born, J. (1995). Hormonal secretion during nighttime sleep indicating stress of daytime exercise. J. Appl. Physiol. 79: 1461-1468.
55. Kim, Y., Pallansch, M., Caradente, F., Reissman, G., Halberg, E., and Halberg, F. (1980). Circadian and circannual aspects of the complement cascade. Chronobiologia 7: 189-204.
56. Kreiger, D.T. (1979). Endocrine Rhythms. New York: Raven Press.
57. Kronauer, R.E., Czeisler, C.A., Pilato, S.F., Moore-Ede, M.C., and Weitzman, E.D. (1982). Mathematical model of the human circadian system with two interacting oscillators. Am. J. Physiol. 242: R3-R17.
58. Krueger, J.M. (1985). Muramyl peptides and interleukin-1 as promoters of slow-wave sleep. In: S. Inoué and A.A. Borbély (Eds.), Endogenous Sleep Substances and Sleep Regulation, pp. 181-192. Tokyo: Japan Scientific Societies Press.
59. Krueger, J.M., Dinarello, C.A., Shoham, S., Davenne, D., Walter, J., Kubillus, S. (1987). Interferon-alpha2 enhances slow wave sleep in rabbits. Int. J. Immunopharmacol. 9: 23-30.
60. Kusaka, Y., Kondou, H., and Morimoto, K. (1992). Healthy lifestyles are associated with higher natural killer cell activity. Prev. Med. 21: 602-615.
61. Laerum, O.D. (1995). Hematopoiesis occurs in rhythms. Exp. Hematol. 23: 1145-1147.
62. Lévi, F., Canon, C., Touitou, Y., Reinberg, A., and Math, G. (1988). Seasonal modulation of the circadian time structure of circulating T and natural killer lymphocyte subsets from healthy subjects. J. Clin. Invest. 81: 407-413.
63. Lévi, F., and Halberg, F. (1982). Circaseptan (about 7-day) bioperiodicity-spontaneous and reactive- and the search for pacemakers. Ric. Clin. Lab. 12: 323-370.
64. Maestroni, G.J.M., and Conti, A. (1990). The pineal-endogenous opioid system-immune network: Mechanism and significance. 4th International Workshop on Neuroimmunomodulators, Florence, May 23-26, 1990, Abstr. 347.
65. Marcocchi, N., Musse, J.P., Kohler, F., Michaud, C., Michel, F., Schwertz, A., Drouin, P., and Méjean, L. (1987). Une expérience d'enquete nutritionnelle informatisée à la foire de Nancy [Experience of a computer survey at the Nancy fair]. Cah. Nutr. Diet. 22: 185-195.
66. Martin, B.J. (1986). Sleep deprivation and exercise. Exerc. Sport Sci. Rev. 14: 213-230.
67. Masera, R.G., Carignola, R., Staurenghi, A.H., Sartori, M.L., Lazzero, A., Griot, G., and Angeli, A. (1994). Altered circadian rhythms of natural killer (NK) cell activity in patients with auto-immune rheumatic diseases. Chronobiologia 21: 127-132.
68. Matsumara, H., Goh, Y., Ueno, R., Sakai, T., and Hayaishi, O. (1988). Awaking effect of PGE2 microinjected into the preoptic area of rats. Brain Res. 444: 265-272.
69. Mauer, A.M. (1965). Diurnal variation of proliferative activity in the human bone marrow. Blood 26: 1-7.
70. Méjean, L., Kolopp, M., and Drouin, P. (1994). Chronobiology, nutrition and diabetes mellitus. In: Y. Touitou and E. Haus (Eds.), Biological Rhythms in Clinical and Laboratory Medicine, pp. 375-385. Berlin: Springer Verlag.
71. Moldofsky, H., Lue, F.A., Eisen, J., Keyston, E., and Gorczynski, R.M. (1986). The relationship of interleukin-1 and immune functions to sleep in humans. Psychosom. Med. 48: 309-318.
72. Montelpare, W.J., Plyley, M.J., and Shephard, R.J. (1992). Evaluating the influence of sleep deprivation upon circadian rhythms of exercise metabolism. Can. J. Sports Sci. 17: 94-97.
73. Montmayeur, A., Buguet, A., Sollin, H., and Lacour, J.R. (1994). Exercise and sleep in four African sportsmen living in the Sahel. Int. J. Sports Med. 15: 42-45.
74. Morley, A., King-Smith, E.A., and Stohlman, F. (1970). The oscillatory nature of hemopoiesis. In: F. Stohlman (ed.), Symposium on Hemopoietic Cellular Proliferation, pp. 3-14. New York: Grune & Stratton.
75. Nakachi, K., and Imai, K. (1992). Environmental and physiological influences on human natural killer cell activity in relation to good health practices. Jpn. J. Cancer Res. 83: 798-805.
76. Neumann, K. (1996). Flying through jetlag: Too much ado about melatonin. Travel Med. Internat. 14: 53-58.
77. Nicolau, G.Y., and Haus, E. (1994). Chronobiology of the hypothalamic-pituitary-thyroid axis. In: Y. Touitou and E. Haus (Eds.), Biological Rhythms in Clinical and Laboratory Medicine, pp. 330-347. Berlin: Springer Verlag.
78. Nicolau, G.Y., Haus, E., Popesku, M., Sackett-Lundeen, L., and Petrescu, E. (1991). Circadian, weekly and seasonal variation in cardiac mortality, blood pressure and catecholamine excretion. Chronobiol. Internat. 8: 149-159.
79. Nieman, D.C., Ahle, J.C., Henson, D.A., Warren, B.J., Suttles, J., Davis, J.M., Buckley, K.S., Simandle, S., Butterworth, D.E., Fagoaga, O.R., and Nehlsen-Cannarella, S.L. (1995). Indomethacin does not alter natural killer cell response to 2.5 h of running. J. Appl. Physiol. 79: 748-755.
80. Pangerl, A., Ramien, J., and Haen, E. (1986). The number of beta-adrenoreceptor sites on intact human lymphocytes depends on time of day, season, and on sex. Ann. Rev. Chronopharmacol. 3: 331-334.
81. Petrovsky, N., McNair, P., and Harrison, L.C. (1994). Circadian rhythmicity of interferon-gamma production in antigen-stimulated whole blood. Chronobiologia 21: 293-300.
82. Plyley, M.J., Davis, G., Shephard, R.J., and Goode, R.C. (1984). Sleep deprivation and cardiorespiratory function-influence of intermittent exercise. Eur. J. Appl. Physiol. 56: 338-344.
83. Pollak, M.H. (1994). Heart rate reactivity to laboratory tasks and in two daily life settings. Psychosom. Med. 56: 271-276.
84. Putkonen, P.T.S., Elomaa, E., and Kotilainen, P.V. (1973). Increase in delta (3 + 4) sleep after heat stress in sauna. Scand. J. Lab. Clin. Invest. 31(Suppl. 130): 19.
85. Radomski, M.W., Hart, L.E.M., Goodman, J.M., and Plyley, M.L. (1992). Aerobic fitness and hormonal responses to prolonged sleep deprivation and sustained mental work. Aviat. Space Environ. Med. 63: 101-106.
86. Rebar, R.W., and Yen, S.S.C. (1979). Endocrine rhythms in gonadotrophins and ovarian steroids. In: D.T. Kreiger (Ed.), Endocrine Rhythms, pp. 259-298. New York: Raven Press.
87. Reilly, T. (1990). Human circadian rhythms and exercise. Crit. Rev. Biomed. Eng. 18: 165-180.
88. Reilly, T., and Brooks, G.A. (1982). Circadian constancy in work stress indices and physiological capacity [Abstract]. Ergonomics 25: 329-330.
89. Reilly, T., and Hales, A.J. (1988). Effects of partial sleep deprivation on performance measures in females. In: E.D. Mega (Ed.), Contemporary Ergonomics, pp. 509-514. London: Taylor and Francis.
90. Reinberg, A., Schuller, E., Clench, J., and Smolensky, M.H. (1980). Circadian and circaannual rhythms of leukocytes, proteins and immunoglobulins. In: M.H. Smolensky, A. Reinberg, and J.P. McGovern. (Eds.), Recent Advances in the Chronobiology of Allergy and Immunology, pp. 251-259. Oxford: Pergamon Press.
91. Reinberg, A., and Smolensky, M. (1983). Biological Rhythms and Medicine: Cellular, Metabolic, Physiopathologic and Pharmacologic Aspects. Berlin: Springer Verlag.
92. Reinberg, A., Z. Zagulla-Mally, J. Ghata, and F. Hallberg. (1969). Circadian reactivity rhythms of human skin to house dust, penicillin and histamine. J. Allergy 44: 292-298.
93. Reiter, R.J. (1994). Melatonin: Multifaceted messenger to the masses. Lab. Med. 25: 438-443.
94. Reiter, R.J., Poeggeler, B., Tan, D.-X., Chen, L.D., Manchester, L.C., and Guerrero, J.M.. (1993). Antioxidant capacity of melatonin: A novel function not requiring a receptor. Neurendocrinol. Lett. 15: 103-116.
95. Ritchie, A.W.S., Oswald, I., Miclem, H.S., Boyd, J.E., Elton, R.A., Jazwinska, E., and James, K. (1983). Circadian variations of lymphocyte subpopulations: A study with monoclonal antibodies. Br. Med. J. 286: 1773-1775.
96. Rodgers, C.D., Paterson, D.H., Cunningham, D.A., Noble, E.G., Pettigrew, F.P., Myles, W.S., and Taylor, A.W. (1995). Sleep deprivation: Effects on work capacity, self-paced walking, contractile properties and perceived exertion. Sleep 18: 30-38.
97. Rutenfranz, J., Ottmann, W., Neidhart, B., and Brockmann, W. (1988). Comparison of two analytical procedures for the determination of free urinary catecholamines under the demands of shiftwork experiments. Int. Arch. Occup. Environ. Health 61: 89-93.
98. Shapiro, C.M., Bortz, R., Mitchell, D., Bartell, P., and Jooste, P. (1981). Slow-wave sleep: A recovery period after exercise. Science 214: 1252-1254.
99. Shek, P.N., and Sabiston, B.H. (1983). Neuroendocrine regulation of immune processes: Change in circulating corticosterone levels induced by the primary antibody response in mice. Int. J. Immunopharmac. 5: 23-33.
100. Shephard, R.J. (1984). Sleep. biorhythms and human performance. Sports Med. 1: 11-37.
101. Shephard, R.J. (1997). Physical Activity and Immune Function. Carmel, IN: Cooper.
102. Shifrine, M., Taylor, N., Rosenblatt, L.S., and Wilson, F. (1980). Seasonal variation in cell-mediated immunity of clinically normal dogs. Exp. Hematol. 8: 318-326.
103. Stephenson, L.A., Kolka, M.A., Francesconi, R., and Gonzalez, R.R. (1989). Circadian variations in plasma renin activity, catecholamines and aldosterone during exercise in women. Eur. J. Appl. Physiol. 58: 756-764.
104. Sutton, J.R., Jurkowski, J.E., Keane, P., Walker, W.H.C., Jones, N.L., and Toews, C.J. (1980). Plasma catecholamine, insulin, glucose and lactate responses to exercise in relation to the menstrual cycle [Abstract]. Med. Sci. Sports Exerc. 12: 83.
105. Takahashi, J.S. (1993). Circadian clocks à la CREM. Nature 365: 299-300.
106. Takahashi, J.S., and Hoffman, M. (1995). Molecular biological clocks. Am. Scient. 83: 158-165.
107. Taylor, S.R., Rogers, G.G., and Driver, H.S. (1994). Training taper decreases slow-wave sleep in competitive female swimmers. J. Sleep Res. 3(Suppl. 1): 250.
108. Torsvall, L., Åkerstedt, T., and Lindbeck, G. (1984). Effect on sleep stages and EEG power density of different degrees of exercise in fit subjects. Electroenceph. Clin. Neurophysiol. 57: 347-353.
109. Trine, M.R., and Morgan, W.P. (1995). Influence of time of day on psychological responses to exercise: A review. Sports Med. 20: 328-337.
110. Veldhuis, J.D., King, J.C., Urban, R.J., Rogol, A.D., Evans, W.S., Kolp, L.A., and Johnson. M.L. (1987). Operating characteristics of the male hypothalamo-pituitary gonadal axis pulsatile release of testosterone and follicular stimulating hormone and their temporal coupling with luteinizing hormone. J. Clin. Endocrinol. Metab. 65: 929-941.
111. Veldhuis, J.D., and Johnson, M.L. (1986). Cluster analysis: a simple and robust algorhythm for endocrine pulse detection. Am. J. Physiol. 250: E486-E496.
112. Veldhuis, J.D., Johnson, M.L., Iranmanesh, A., and Lizarralde, G. (1994). Rhythmic and non-rhythmic modes of anterior pituitary hormone release in man. In: Y. Touitou and E. Haus (Eds.), Biological Rhythms in Clinical and Laboratory Medicine, pp. 277-291. Berlin: Springer Verlag.
113. Weibel, L., Spiegel, K., Follenius, M., Ehrhart, J., and Brandenberger, G. (1996). Internal dissociation of the circadian markers of the cortisol rhythm in night workers. Am. J. Physiol. 270: E608-E613.
114. Whichelow, M.J., Sturge, R.A., Keen, H., Jarrett, R.J., Stimmler, L., and Grainger, S. (1974). Diurnal variation in response to intravenous glucose. Br. Med. J. 1: 488-491.
115. Winget, C.M., Soliman, M.R.I., Holley, D.C., and Meylor, J.S. (1994). Chronobiology of physical performance and sports medicine. In: Y. Touitou and E. Haus (Eds.), Biological Rhythms in Clinical and Laboratory Medicine, pp. 230-242. Berlin: Springer Verlag.
116. 170 and maximal oxygen intake. J. Hum. Ergol. 10: 213-219.
117. Zimmet, P.Z., Wall, J.R., Rome, L., Stimmler, L., and Jarrett, R.J. (1974). Diurnal variation in glucose tolerance: Associated changes in plasma insulin, growth hormone and non-esterified fatty acid. Br. Med. J. 1: 485-488.