A History of Chronobiological Concepts

  • Serge DaanEmail author
Part of the Protein Reviews book series (PRON, volume 12)


The perpetual alternation of night and day could not escape being noticed by the earliest humans. It must have marked to them the passage of time. Tilling their fertile soil, the early Sumerians needed precise knowledge of time. When should the wheat be sown, when be harvested? How many days to wait till the great floods in spring? How allocate their stores of grain such that daily rations would last till the new harvest? Scores of practical questions. The Sumerians went to their temples to seek the answers. Much more than the nomads’ opportunistic way of life, early agricultural civilisation relied on planning, on anticipation, on keeping track of time. There was a growing caste of those who assembled the information: the priests. They noticed the rigid patterns of annual change in the sun’s position. They started to observe the movements of other celestial bodies. They constructed their temples almost as astronomical observatories, with the major axes aligned to the stellar constellation on days of importance. The priests in Sumer were the first, but not the last in this respect. Most of the Mesopotamian temples, such as the Ziggurath in Babylon had a long East–West axis. In Egypt, temples were often oriented towards the direction where the sun rises on the longest day. Once per year, at dawn of the summer solstice, the first rays would illuminate the god-statue at the end of a narrow pillar gallery. Much later, the Incas in South-, the Anasazi in North America again dramatized special days in the annual cycle by the architecture and orientation of their places of worship. It was the place where priests engaged both in scientific observation and in religious duties. It also became the great storage room of past observations and events, of accumulating knowledge. The observation of stellar constellations as a means of measuring time became the first scientific activity in most early settlements, long before the cause of their movements was evident.


Circadian Rhythm Circadian Clock Clock Gene Optic Lobe Circadian System 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    De Mairan M (1729) Observation botanique. Hist. de l’Acad. Royal Sciences, Paris, p 1Google Scholar
  2. 2.
    Duhamel du Monceau HL (1758) La physique des arbres, vol 2. H.L.Guerin and L.F. Delatour, ParisGoogle Scholar
  3. 3.
    Pfeffer W (1875) Die Periodischen Bewegungen der Blattorgane. Wilhelm Engelmann, LeipzigGoogle Scholar
  4. 4.
    Stoppel R (1926) Die Schlafbewegungen der Blätter von Phaseolus multiflorus in Island zur Zeit der Mitternachtsonne. Planta 2:342–355Google Scholar
  5. 5.
    Brown FA (1970) Hypothesis of environmental timing of the clock. In: Brown FA, Hastings JW, Palmer JD (eds) The biological clock: two views. Academic Press, New York, pp 13–59Google Scholar
  6. 6.
    Hamner K, Finn J Jr, Sirohi G, Hoshizaki T, Carpenter B (1962) The biological clock at the South Pole. Nature 195:476–480Google Scholar
  7. 7.
    Sulzman FM, Ellman D, Fuller CA, Moore-Ede MC, Czeisler CA, Wassmer G (1984) Neurospora circadian rhythms in space: a reexamination of the endogenous-exogenous ­question. Science 225:232–234PubMedGoogle Scholar
  8. 8.
    Kiesel A (1894) Untersuchungen zur Physiologie des facettierten Auges. Sitzungsber Akad Wiss Wien 103: 97–139.Google Scholar
  9. 9.
    Simpson S, Galbraith JJ (1905) An investigation into the diurnal variation of the body ­temperature of nocturnal and other birds and a few mammals. J Physiol 33:225–238PubMedGoogle Scholar
  10. 10.
    Darwin CR, Darwin F (1880) The power of movement in plants. John Murray, LondonGoogle Scholar
  11. 11.
    Bünning E (1960) Opening address: biological clocks. Cold Spring Harb Symp Quant Biol 25:1–9Google Scholar
  12. 12.
    Enright J (1982) Sleep movements of leaves: in defense of Darwin’s interpretation. Oecologia (Berl.) 54:253–259Google Scholar
  13. 13.
    Pfeffer W (1915) Beiträge zur Kenntnis der Entstehung der Schlafbewegungen. Abh. ­math-phys. Klasse Königl. Sächs. Ges. Wiss 34:1–154Google Scholar
  14. 14.
    Bünning E, Chandrashekaran MK (1975) Pfeffer’s views on rhythms. Chronobiologia 2:160–167PubMedGoogle Scholar
  15. 15.
    Kleinhoonte A (1929) Über die durch das Licht regulierten autonomen Bewegungen der Canavalia-blätter. Arch Neerl Sci Exactes 5:1–110Google Scholar
  16. 16.
    Bünning E, Stern K (1930) Über die tagesperiodischen Bewegungen der Primärblätter von Phaseolus multiflorus. II. Die Bewegungen bei Thermo-konstanz. Ber Deutsche Bot Ges 48:227–252Google Scholar
  17. 17.
    Gamble FW, Keeble F (1900) Hippolyte varians: a study in colour-change. Q J Microsc Sci 43:589–698Google Scholar
  18. 18.
    Richter, CP (1922) A behavioristic study of the activity of the rat. Comparative Psychology Monographs 1:1–54Google Scholar
  19. 19.
    Pittendrigh CS (1960) Circadian rhythms and the circadian organization of living systems. Cold Spring Harb Symp Quant Biol 25:159–184PubMedGoogle Scholar
  20. 20.
    Halberg F (1959) Physiologic 24-hour periodicity in human beings and mice, the lighting regimen and daily routine. In: Withrow E (ed) Photoperiodism and related phenomena in plants and animals. AAAS, Washington, pp 803–878Google Scholar
  21. 21.
    Hufeland CW (1797) Die Kunst das menschliche Leben zu verlängern. Jena: Akademische BuchhandlungGoogle Scholar
  22. 22.
    Aschoff J, Wever R (1962) Spontanperiodik des Menschen bei Ausschluss aller Zeitgeber. Naturwissenschaften 49:337–342Google Scholar
  23. 23.
    Semon R (1904) Das Mneme als erhaltendes Prinzip im Wechsel des organischen Geschehens. W. Engelmann, LeipzigGoogle Scholar
  24. 24.
    Semon R (1905) Über die Erblichkeit der Tagesperiode. Biol Zent Bl 15:241–252Google Scholar
  25. 25.
    Aschoff J (1955) Tagesperiodik bei Mäusestämmen unter konstanten Umgebungsbedingungen. Pflügers Arch 262:51–59PubMedGoogle Scholar
  26. 26.
    Davis F, Mannion J (1988) Entrainment of hamster pup circadian rhythms by prenatal ­melatonin injections to the mother. Am J Physiol 255:R439–R448PubMedGoogle Scholar
  27. 27.
    Aschoff J, Meyer-Lohmann J (1954) Angeborene 24-Stunden-Periodik bei Kücken. Pflügers Arch 260:170–176PubMedGoogle Scholar
  28. 28.
    Sheeba V, Sharma VK, Chandrashekaran MK, Joshi A (1999) Persistence of eclosion rhythm in Drosophila melanogaster after 600 generations in an aperiodic environment. Naturwissenschaften 86:448–449PubMedGoogle Scholar
  29. 29.
    Wever R (1980) Circadian rhythms of finches under steadily changing light intensity: are selfsustaining circadian rhythms self-excitatory? J Comp Physiol 140:113–119Google Scholar
  30. 30.
    Beling I (1929) Über das Zeitgedächtnis der Bienen. Z Vgl Physiol 9:259–338Google Scholar
  31. 31.
    Santschi F (1913) A propos de l’orientation virtuelle chez les fourmis. Bull Soc Hist Nat Afr Nord 4–6: 231–235Google Scholar
  32. 32.
    Von Frisch K (1950) Die Sonne als Kompasz im Leben der Bienen. Experientia 6:210–221Google Scholar
  33. 33.
    Kramer G (1950) Weitere Analyse der Faktoren, welche die Zugaktivität des gekäfigten Vogels orientieren. Naturwissenschaften 37:377–378Google Scholar
  34. 34.
    Virey JJ (1814) Ephémerides de la vie humaine, ou recherches sur la révolution journaliere et la periodicité de ses phénomènes dans la santé et les malades. Sorbonne, ParisGoogle Scholar
  35. 35.
    Johnson MS (1939) Effect of continuous light on periodic spontaneous activity of ­white-footed mice (Peromyscus). J Exp Zool 82:315–328Google Scholar
  36. 36.
    Kalmus H (1940) Diurnal rhythms in the axolotl larva and in Drosophila. Nature 145:72–73Google Scholar
  37. 37.
    Pittendrigh CS (1954) On temperature independence of the clock system controlling ­emergence time in Drosophila. Proc Natl Acad Sci U S A 40:1018–1029PubMedGoogle Scholar
  38. 38.
    Hastings WJ, Sweeney BM (1957) On the mechanism of temperature independence in a ­biological clock. Proc Natl Acad Sci U S A 43:804–811PubMedGoogle Scholar
  39. 39.
    Pittendrigh CS, Caldarola PC (1973) General homeostasis of the frequency of circadian ­oscillations. Proc Nat Acad Sci U S A 70:2697–2701Google Scholar
  40. 40.
    Aschoff J (1960) Exogenous and endogenous components in circadian rhythms. Cold Spring Harb Symp Quant Biol 25:11–28PubMedGoogle Scholar
  41. 41.
    Aschoff J (1979) Circadian rhythms: influences of internal and external factors on the period measured in constant conditions. Z Tierpsychol 49:225–249PubMedGoogle Scholar
  42. 42.
    Pittendrigh CS, Daan S (1976) A functional analysis of circadian pacemakers in nocturnal rodents I. The stability and lability of spontaneous frequency. J Comp Physiol 106:223–252Google Scholar
  43. 43.
    Page TL, Block GD (1980) Circadian rhythmicity in cockroaches: effects of early ­post-embryonic development and ageing. Physiol Entomol 5:271–281Google Scholar
  44. 44.
    Daan S (2000) Colin Pittendrigh, Jürgen Aschoff, and the natural entrainment of circadian systems. J Biol Rhythms 15:195–207PubMedGoogle Scholar
  45. 45.
    Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci U S A 95:8660–8664PubMedGoogle Scholar
  46. 46.
    Pittendrigh C (1958) Perspectives in the study of biological clocks. In: Buzzati-Traverso AA (ed) Perspectives in marine biology. University of California Press, Berkeley, pp 239–268Google Scholar
  47. 47.
    Bennett M, Schatz MF, Rockwood H, Wiesenfeld H (2002) Huygens’s clocks. Proc Math Phys Eng Sci 458:563–579Google Scholar
  48. 48.
    DeCoursey PJ (1960) Phase control of activity in an rodent. Cold Spring Harb Symp Quant Biol 25:49–55PubMedGoogle Scholar
  49. 49.
    Wever R (1966) Ein mathematisches Modell für die circadiane Periodik. Z Angew Math Mech Sonderheft (GAMM-Tagung) 46:148–157Google Scholar
  50. 50.
    Pavlidis T (1973) Biological oscillators: their mathematical analysis. Academic Press, New YorkGoogle Scholar
  51. 51.
    Winfree AT (1970) Integrated view of resetting a circadian clock. J Theor Biol 28:327–374PubMedGoogle Scholar
  52. 52.
    Bruce VG (1960) Environmental entrainment of circadian rhythms. Cold Spring Harb Symp Quant Biol 25:29–48Google Scholar
  53. 53.
    Aschoff J (1954) Zeitgeber der tierischen Tagesperiodik. Naturwissenschaften 41:49–56Google Scholar
  54. 54.
    Aschoff J, Tokura H (1986) Circadian activity rhythms in squirrel monkeys: entrainment by temperature cycles. J Biol Rhythms 1:91–99PubMedGoogle Scholar
  55. 55.
    Hayden P, Lindberg RG (1969) Circadian rhythm in mammalian body temperature entrained by cyclic pressure changes. Science 164:1288–1289PubMedGoogle Scholar
  56. 56.
    Gwinner E (1966) Entrainment of a circadian rhythm in birds by species-specific song cycles (Aves, Fringillidae: Carduelis spinus, Serinus serinus). Experientia 22:1–3Google Scholar
  57. 57.
    Marimuthu G, Rajan S, Chandrashekaran MK (1981) Social entrainment of the circadian rhythm in the flight activity of the Microchiropteran bat Hipposideros speoris. Behav Ecol Sociobiol 8:147–150Google Scholar
  58. 58.
    Wever R (1970) Zur Zeitgeber-Stärke eines Licht-Dunkel-Wechsels für die circadiane ­periodik des Menschen. Pflügers Arch 321:133–142PubMedGoogle Scholar
  59. 59.
    Wever R (1979) The circadian system of man. Springer, BerlinGoogle Scholar
  60. 60.
    Roenneberg T, Kumar CJ, Merrow M (2007) The human circadian clock entrains to sun time. Curr Biol 17:R44–R45PubMedGoogle Scholar
  61. 61.
    Roenneberg T, Merrow M (1998) Molecular circadian oscillators: an alternative hypothesis. J Biol Rhythms 13:167–179PubMedGoogle Scholar
  62. 62.
    Roenneberg T, Merrow M (2001) Circadian systems: different levels of complexity. Philos Trans R Soc Lond B Biol Sci 356:1687–1696PubMedGoogle Scholar
  63. 63.
    DeCoursey P (1960) Daily light sensitivity rhythm in a rodent. Science 131:33–35Google Scholar
  64. 64.
    Hastings JW, Sweeney BM (1958) A persistent diurnal rhythm of luminiscence in Gonyaulax polyedra. Biol Bull 115:440–458Google Scholar
  65. 65.
    Johnson CH (1999) Forty years of PRCs – what have we learned? Chronobiol Int 16:711–743PubMedGoogle Scholar
  66. 66.
    Daan S, Lewy A (1984) Scheduled exposure to daylight: a potential strategy to reduce “jet lag” following transmeridian flights. Psychopharmacol Bull 20:566–568PubMedGoogle Scholar
  67. 67.
    Honma K, Honma S (1988) A human phase response curve for bright light pulses. Jpn J Psychiatry Neurol 42:167–168Google Scholar
  68. 68.
    Khalsa SBS, Jewett ME, Cajochen C, Czeisler CA (2003) A phase response curve to single bright light pulses in human subjects. J Physiol 549:945–952PubMedGoogle Scholar
  69. 69.
    Pittendrigh C (1974) Circadian oscillations in cells and the circadian organization of multicellular systems. In: Schmidt FO, Worden FG (eds) The neurosciences IIIrd study program. MIT Press, Cambridge, MA, pp 437–458Google Scholar
  70. 70.
    Pittendrigh CS, Daan S (1976) A functional analysis of circadian pacemakers in nocturnal rodents IV, Entrainment: pacemaker as clock. J Comp Physiol 106:291–331Google Scholar
  71. 71.
    Pittendrigh CS (1964) Entrainment of circadian oscillations by skeleton photoperiods. Science 144:565PubMedGoogle Scholar
  72. 72.
    Nelson DE, Takahashi JS (1999) Integration and saturation within the circadian photic entrainment pathway of hamsters. Am J Physiol 277:R1351–R1361PubMedGoogle Scholar
  73. 73.
    Comas M, Beersma DGM, Spoelstra K, Daan S (2007) Circadian response reduction in light and response restoration in darkness: a “skeleton” light pulse PRC study in mice (Mus ­musculus). J Biol Rhythms 22:432–444PubMedGoogle Scholar
  74. 74.
    Hut RA, Van Oort BEH, Daan S (1999) Natural entrainment without dawn and dusk: the case of the european ground squirrel (Spermophilus citellus). J Biol Rhythms 14:290–299PubMedGoogle Scholar
  75. 75.
    Pittendrigh CS, Bruce VG (1957) An oscillator model for biological clocks. In: Rudnick D (ed) Rhythmic and synthetic processes in growth. Princeton University Press, Princeton, pp 239–268Google Scholar
  76. 76.
    Harker JE (1960) Endocrine and nervous factors in insect circadian rhythms. Cold Spring Harb Symp Quant Biol 25:279–287PubMedGoogle Scholar
  77. 77.
    Page TL (1981) Neural and endocrine control of circadian rhythmicity in invertebrates. In: Aschoff J (ed) Handbook of behavioral neurobiology, vol 4. Plenum, New York, pp 145–172Google Scholar
  78. 78.
    Nishiitsutsuji-Uwo J, Pittendrigh CS (1968) Central nervous system control of circadian rhythmicity in the cockroach III. The optic lobes, locus of the driving oscillation? Z Vgl Physiol 58:14–46Google Scholar
  79. 79.
    Page T (1982) Transplantation of the cockroach circadian pacemaker. Science 216:73–75PubMedGoogle Scholar
  80. 80.
    Gaston S, Menaker M (1968) Pineal function: the biological clock in the sparrow? Science 160:1125–1127PubMedGoogle Scholar
  81. 81.
    Zimmerman NH, Menaker M (1979) Pineal-gland – Pacemaker within the circadian system of the house sparrow. Proc Natl Acad Sci U S A 76:999–1003PubMedGoogle Scholar
  82. 82.
    Simpson SM, Follett BK (1981) Pineal and hypothalamic pacemakers – their role in regulating circadian rhythmicity in Japanese quail. J Comp Physiol 144:381–389Google Scholar
  83. 83.
    Richter CP (1967) Sleep and activity: their relation to the 24-hour clock. Res Publ Assoc Nerv Ment Dis 45:8–27Google Scholar
  84. 84.
    Stephan FK, Zucker I (1972) Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Nat Acad Sci USA 69:1583–1586PubMedGoogle Scholar
  85. 85.
    Moore RY, Eichler VB (1972) Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in rat. Brain Res 42:201–206PubMedGoogle Scholar
  86. 86.
    Inouye S, Kawamura H (1979) Persistence of circadian rhythmicity in a mammalian hypothalamic “island” containing the suprachiasmatic nucleus. Proc Natl Acad Sci U S A 76:5962–5966PubMedGoogle Scholar
  87.  87.
    Ralph MR, Menaker M (1988) A mutation in the circadian system in golden hamsters. Science 241:1225–1227PubMedGoogle Scholar
  88.  88.
    Ralph MR, Foster RG, Davis FC, Menaker M (1990) Transplanted suprachiasmatic nucleus determines circadian period. Science 247:975–978PubMedGoogle Scholar
  89.  89.
    Block GD, Wallace SF (1982) Localization of a circadian pacemaker in the eye of a mollusk, Bulla. Science 217:155–157PubMedGoogle Scholar
  90.  90.
    Hendrickson AE, Wagoner N, Cowan WM (1972) An autoradiographic and electron ­microscopic study of retino-hypothalamic connections. Z Zellforsch Mikrosk Anat 135:1–26PubMedGoogle Scholar
  91.  91.
    Moore RY, Lenn NJ (1972) A retinohypothalamic projection in the rat. J Comp Neurol 146:1–14PubMedGoogle Scholar
  92.  92.
    Cloudsley-Thompson JL (1953) Studies on diurnal rhythms – III. Photoperiodism in the ­cockroach Periplaneta americana (L.). Ann Mag Nat Hist 6:705–712Google Scholar
  93.  93.
    Roberts SK (1965) Photoreception and entrainment of cockroach activity rhythms. Science 148:958–959PubMedGoogle Scholar
  94.  94.
    Nishiitsutsuji-Uwo J, Pittendrigh CS (1968) Central nervous system control of circadian rhythmicity in the cockroach II. The pathway of light signals that entrain the rhythm. Z Vgl Physiol 58:1–13Google Scholar
  95.  95.
    Truman JW (1971) Circadian rhythms and physiology with special reference to neuroendocrine processes in insects. In: Proceedings of the International Symposium on Circadian Rhymicity, Pudoc Press, Wageningen, pp 111–135Google Scholar
  96.  96.
    Menaker M (1968) Extraretinal light reception in the sparrow I. Entrainment of the biological clock. Proc Natl Acad Sci U S A 59:414–421PubMedGoogle Scholar
  97.  97.
    Underwood H (2001) Circadian organization in nonmammalian vertebrates. In: Takahashi JS, Turek FW, Moore RY (eds) Handbook of behavioral neurobiology, vol 12, Circadian clocks. Kluwer, New York, pp 111–140Google Scholar
  98.  98.
    Richter C (1967) Psychopathology of periodic behavior in animals and man. In: Zubin J, Hunt HF (eds) Comparative psychopathology. Grune & Stratton, New York, pp 205–227Google Scholar
  99.  99.
    Groos GA, Mason R (1980) The visual properties of rat and cat suprachiasmatic neurones. J Comp Physiol 135:349–356Google Scholar
  100. 100.
    Freedman MS, Lucas RJ, Soni B, von Schantz M, Munoz M, David-Gray Z, Foster R (1999) Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science 284:502–504PubMedGoogle Scholar
  101. 101.
    Provencio I, Rodriguez IR, Jiang GS, Hayes WP, Moreira EF, Rollag MD (2000) A novel human opsin in the inner retina. J Neurosci 20:600–605PubMedGoogle Scholar
  102. 102.
    Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070–1073PubMedGoogle Scholar
  103. 103.
    Lewy A, Newsome D (1983) Different types of melatonin circadian secretory rhythms in some blind subjects. J Clin Endocrinol Metab 56:1103–1107PubMedGoogle Scholar
  104. 103a.
    Lockley SW, Skene DJ, Arendt J, Tabandeh H, Bird AC, Defrance R (1999) Relationship between melatonin rhythms and visual loss in the blind J.clin. Endocrinol Metab 82:3763–3770PubMedGoogle Scholar
  105. 104.
    Menaker M, Binkley S (1981) Neural and endocrine control of circadian rhythms in the vertebrates. In: Aschoff J (ed) Handbook of behavioral neurobiology. Plenum, New York, pp 243–256Google Scholar
  106. 105.
    Tosini G, Menaker M (1996) Circadian rhythms in cultured mammalian retina. Science 272:419–421PubMedGoogle Scholar
  107. 106.
    Silver R, Lesauter J, Tresco PA, Lehman MN (1996) A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 382:810–813PubMedGoogle Scholar
  108. 107.
    Cannon WB (1929) Organization for physiological homeostasis. Physiol Rev 9:399–431Google Scholar
  109. 108.
    Bernard C (1878) Leçons sur les phénomènes de la vie communs aux animaux et aux ­végétaux. J.-B. Bailliere et fils, ParisGoogle Scholar
  110. 109.
    Mrosovsky N (1990) Rheostasis. The physiology of change. Oxford University Press, OxfordGoogle Scholar
  111. 110.
    Kleitman N (1963) Sleep and Wakefulness. Revised and enlarged edition. University of Chicago Press, ChicagoGoogle Scholar
  112. 111.
    Aserinsky E, Kleitman N (1953) Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. Science 118:273–274PubMedGoogle Scholar
  113. 112.
    Aschoff J (1965) Circadian rhythms in man – a self-sustained oscillator with an inherent frequency underlies human 24-hour periodicity. Science 148:1427–1432PubMedGoogle Scholar
  114. 113.
    Jouvet M, Mouret J, Chouvet G, Siffre M (1974) Toward a 48-hour day: experimental ­bicircadian rhythms in man. In: Schmitt F (ed) The neurosciences: third study program. MIT Press, Cambridge, MA, pp 491–497Google Scholar
  115. 114.
    Moore-Ede M (1983) The circadian timing system in mammals: two pacemakers preside over many secondary oscillators. Fed Proc 42:2802–2808PubMedGoogle Scholar
  116. 115.
    Eastman C (1982) The phase-shift model of spontaneous internal desynchronization in humans. In: Aschoff J, Daan S, Groos G (eds) Vertebrate circadian systems. Springer, ­Berlin-Heidelberg, pp 262–267Google Scholar
  117. 116.
    Borbély AA (1982) Circadian and sleep-dependent processes in sleep regulation. In: Aschoff J, Daan S, Groos GA (eds) Vertebrate circadian systems. Springer, Berlin-Heidelberg, pp 237–242Google Scholar
  118. 117.
    Zulley J, Wever RA (1982) Interaction between the sleep-wake cycle and the rhythm of rectal temperature. In: Aschoff J, Daan S, Groos GA (eds) Vertebrate circadian systems. Springer, Berlin-Heidelberg, pp 253–261Google Scholar
  119. 118.
    Borbély AA (1982) A two-process model of sleep regulation: I. Physiological basis and outline. Hum Neurobiol 1:195–204PubMedGoogle Scholar
  120. 119.
    Daan S, Beersma DGM (1983) Circadian gating of human sleep-wake cycles. In: Moore-Ede MC, Czeisler CA (eds) Mathematical models of the circadian sleep-wake cycle. Raven Press, New York, pp 129–158Google Scholar
  121. 120.
    Daan S, Beersma DGM, Borbély AA (1984) Timing of human sleep: recovery process gated by a circadian pacemaker. Am J Physiol 246:R161–R178PubMedGoogle Scholar
  122. 121.
    Dijk D-J, Duffy JF, Czeisler CA (1992) Circadian and sleep/wake dependent aspects of subjective alertness and cognitive performance. J Sleep Res 1:112–117PubMedGoogle Scholar
  123. 122.
    Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10:49–62PubMedGoogle Scholar
  124. 123.
    Bünning E (1935) Zur Kenntnis der erblichen Tagesperiodizitat bei den Primarblattern von Phaseolus multiflorus. Jahrb wiss Bot 81:411–418Google Scholar
  125. 124.
    Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A 68:2112–2116PubMedGoogle Scholar
  126. 125.
    Hardin PE, Hall JC, Rosbash M (1990) Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343:536–540PubMedGoogle Scholar
  127. 126.
    Feldman JF, Hoyle MN (1973) Isolation of circadian clock mutants of Neurospora crassa. Genetics 75:605–613PubMedGoogle Scholar
  128. 127.
    Lowrey PL, Shimomura K, Antoch MP, Yamazaki S, Zemenides PD, Ralph MR, Menaker M, Takahashi JS (2000) Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. Science 288:483–491PubMedGoogle Scholar
  129. 128.
    Hotz Vitaterna M, King D, Chang A, Kornhauser JM, Lowrey PL, McDonald JD, Dove WF, Pinto LH, Turek FW, Takahashi JS (1994) Mutagenesis and mapping of a mouse gene clock, essential for circadian behaviour. Science 264:719–725Google Scholar
  130. 129.
    Foster R, Kreitzman L (2004) Rhythms of life. The biological clocks that control the daily lives of every living thing. Profile Books Ltd., LondonGoogle Scholar
  131. 130.
    Toh KL, Jones CR, He Y, Eide EJ, Hinz WA, Virshup DM, Ptaçek LJ, Fu Y-H (2001) An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science 291:1040–1043PubMedGoogle Scholar
  132. 131.
    Nakajima M, Imai K, Ito H, Nishiwaki T, Murayama Y, Iwasaki H, Oyarna T, Kondo T (2005) Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308:414–415PubMedGoogle Scholar
  133. 132.
    Honma K, Honma S, Hiroshige T (1987) Activity rhythms in the circadian domain appear in suprachiasmatic nuclei lesioned rats given methamphetamine. Physiol Behav 40:767–774PubMedGoogle Scholar
  134. 133.
    Mohawk JA, Baer ML, Menaker M (2009) The methamphetamine-sensitive circadian oscillator does not employ canonical clock genes. Proc Natl Acad Sci U S A 106:3519–3524PubMedGoogle Scholar
  135. 134.
    Bünning E (1958) Das Weiterlaufen der “physiologischen Uhr” im Säugerdarm ohne zentrale Steuerung. Naturwissenschaften 45:68Google Scholar
  136. 135.
    Pittendrigh CS, Bruce V, Kaus P (1958) On the significance of transients in daily rhythms. Proc Natl Acad Sci U S A 44:965–973PubMedGoogle Scholar
  137. 136.
    Plautz JD, Kaneko M, Hall JC, Kay SA (1997) Independent photoreceptive circadian clocks throughout Drosophila. Science 278:1632–1635PubMedGoogle Scholar
  138. 137.
    Stephan F, Swann J, Sisk C (1979) Anticipation of 24-hr feeding schedules inrats with lesions of the suprachiasmatic nucleus. Behav Neural Biol 25:346–363PubMedGoogle Scholar
  139. 138.
    Stephan FK (2001) Food-entrainable oscillators in mammals. In: Takahashi JS, Turek FW, Moore RY (eds) Handbook of behavioral neurobiology, vol 12, Circadian clocks. Kluwer/Plenum, New York, pp 223–246Google Scholar
  140. 139.
    Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U (2000) Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 14:2950–2961PubMedGoogle Scholar
  141. 140.
    Stokkan K-A, Yamazaki S, Tei H, Sakaki Y, Menaker M (2001) Entrainment of the liver clock by feeding. Science 291:490–493PubMedGoogle Scholar
  142. 141.
    Schibler U (2009) The 2008 Pittendrigh/Aschoff lecture: peripheral phase coordination in the mammalian circadian timing system. J Biol Rhythms 24:3–15PubMedGoogle Scholar
  143. 142.
    Yoo SH, Yamazaki S, Lowrey PL, Shimomura K, Ko CH, Buhr ED, Siepka SM, Hong HK, Oh WJ, Yoo OJ, Menaker M, Takahashi JS (2004) PERIOD2:: LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci U S A 101:5339–5346PubMedGoogle Scholar
  144. 143.
    Roenneberg T, Morse D (1993) 2 Circadian oscillators in one cell. Nature 362:362–364Google Scholar
  145. 144.
    Roenneberg T, Aschoff J (1990) Annual rhythm of human-reproduction.1. Biology, Sociology, or Both. J Biol Rhythms 5:195–216PubMedGoogle Scholar
  146. 145.
    Garner WW, Allard HA (1920) Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. J Agric Res 18:553–606Google Scholar
  147. 146.
    Marcovitch S (1923) Plant lice and light exposure. Science 58:537–538PubMedGoogle Scholar
  148. 147.
    Rowan W (1926) On photoperiodism, reproductive periodicity and the annual migration of birds and certain fishes. Proc Boston Soc Nat Hist 38:147–189Google Scholar
  149. 148.
    Baker JR, Ransom JR (1932) Factors affecting the breeding of the field mouse (Microtus agrestis): 1. Light. Proc R Soc Lond B Biol Sci 110:313–322Google Scholar
  150. 149.
    Bünning E (1936) Die endonome Tagesrhythmik als Grundlage der photoperiodischen Reaktion. Ber Dtsch Bot Ges 54:590–607Google Scholar
  151. 150.
    Nanda KK, Hamner KC (1959) Photoperiodic cycles of different lengths in relation to flowering in Biloxi soybean. Planta 53:45–52Google Scholar
  152. 151.
    Follett BK, Mattocks PW, Farner DS (1974) Circadian function in the photoperiodic induction of gonadotrophin secretion in the white-crowned sparrow. Proc Natl Acad Sci U S A 71:1666–1669PubMedGoogle Scholar
  153. 152.
    Pittendrigh CS (1972) Circadian surfaces and the diversity of possible roles of circadian organization in photoperiodic induction. Proc Natl Acad Sci U S A 69:2734–2737PubMedGoogle Scholar
  154. 153.
    Saunders DS (1973) Thermoperiodic control of diapause in an insect: theory of internal coincidence. Science 181:358–360PubMedGoogle Scholar
  155. 154.
    Tyshchenko VM (1966) Two-oscillatory model of the physiological mechanism of the photoperiodic reaction of insects. Zh Obshch Biol 27:209–222PubMedGoogle Scholar
  156. 155.
    Pittendrigh CS, Daan S (1976) A functional analysis of circadian pacemakers in nocturnal rodents V. Pacemaker structure: a clock for all seasons. J Comp Physiol 106:333–355Google Scholar
  157. 156.
    Daan S, Berde C (1978) Two coupled oscillators: simulations of the circadian pacemaker in mammalian activity rhythms. J Theor Biol 70:297–313PubMedGoogle Scholar
  158. 157.
    Meijer JH, Daan S, Overkamp GJF, Hermann PM (1990) The 2-oscillator circadian system of tree shrews (Tupaia belangeri) and its response to light and dark pulses. J Biol Rhythms 5:1–16PubMedGoogle Scholar
  159. 158.
    de la Iglesia HO, Meyer J, Carpino A, Schwartz WJ (2000) Antiphase oscillation of the left and right suprachiasmatic nuclei. Science 290:799–801PubMedGoogle Scholar
  160. 159.
    Stoleru D, Peng Y, Agosto J, Rosbash M (2004) Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431:862–868PubMedGoogle Scholar
  161. 160.
    Grima B, Chelot E, Xia RH, Rouyer F (2004) Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431:869–873PubMedGoogle Scholar
  162. 161.
    Jagota A, de la Iglesia HO, Schwartz WJ (2000) Morning and Evening circadian oscillators in the suprachiasmatic nucleus in vitro. Nature 3:372–376Google Scholar
  163. 162.
    Sumová A, Travnicková Z, Peters R, Schwartz WJ, Illnerová H (1995) The rat suprachiasmatic nucleus is a clock for all seasons. Proc Natl Acad Sci U S A 92:7754–7758PubMedGoogle Scholar
  164. 163.
    Lerner AB, Case JD, Takahashi Y, Lee TH, Mori W (1958) Isolation of melatonin, the pineal gland factor that lightens melanocytes. J Am Chem Soc 80:2587Google Scholar
  165. 164.
    Czyba JC, Girod C, Durand N (1964) Sur l’ antagonisme épiphysohypophysaire et les ­variations saisonnieres de la spermatogenèse chez le hamster doré (Mesocricetus auratus). C R Soc Biol (Paris) 158:742–745Google Scholar
  166. 165.
    Moore RY, Heller A, Wurtman RJ, Axelrod J (1967) Visual pathway mediating pineal response to environmental light. Science 155:220–223PubMedGoogle Scholar
  167. 166.
    Reiter RJ (1978) Interaction of photoperiod, pineal and seasonal reproduction as exemplified by findings in the hamster. In: Reiter RJ (ed) Progress in reproductive biology, vol 4. Basel, S. Karger AG, pp 169–190Google Scholar
  168. 167.
    Carter DS, Goldman BD (1983) Antigonadal effects of timed melatonin infusion in pinealectomized male Djungarian hamsters (Phodopus sungorus sungorus): duration is the critical parameter. Endocrinology 113:1261–1267PubMedGoogle Scholar
  169. 168.
    Brandstätter R, Kumar V, Abraham U, Gwinner E (2000) Photoperiodic information acquired and stored in vivo is retained in vitro by a circadian oscillator, the avian pineal gland. Proc Natl Acad Sci U S A 97:12324–12328PubMedGoogle Scholar
  170. 169.
    Kolar J, Machackova I (2005) Melatonin in higher plants: occurrence and possible functions. J Pineal Res 39:333–341PubMedGoogle Scholar
  171. 170.
    Dubois R (1896) Étude sur le méchanisme de la thermogenèse et du sommeil chez les mammifères. Physiologie comparée de la Marmotte. Annales de l’ Université de Lyon 25:1–268Google Scholar
  172. 171.
    Marshall AJ (1951) The refractory period of testis rhythm in birds and its possible bearing on breeding and migration. Wilson Bull 63:238–261Google Scholar
  173. 172.
    Pengelley ET, Fisher KC (1957) Onset and cessation of hibernation under constant ­temperature and light in the golden-mantled ground squirrel (Citellus lateralis). Nature 180:1371–1372Google Scholar
  174. 173.
    Pengelley ET, Fisher KC (1963) The effect of temperature and photoperiod on the yearly hibernating behavior of captive golden-mantled ground squirrels (Citellus lateralis ­tescorum). Can J Zool 41:1103–1120Google Scholar
  175. 174.
    Blake GM (1959) Control of diapause by an “internal clock” in Anthrenus verbasci (L.) (Col. Dermestidae). Nature 183:126–127Google Scholar
  176. 175.
    Gwinner E (1968) Circannuale Periodik als Grundlage des jahreszeitlichen Funktionswandels bei Zugvögeln: Untersuchungen am Fitis (Phylloscopus trochilus) und am Waldlaubsänger (P. sibilatrix). J Ornithol 109:70–95Google Scholar
  177. 176.
    Gwinner E (1986) Circannual rhythms. Springer, BerlinGoogle Scholar
  178. 177.
    Fogden MPL (1972) The seasonality and population dynamics of equatorial forest birds in sarawak. Ibis 114:307–309Google Scholar
  179. 178.
    Chapin JP (1954) The calendar of wideawake fair. Auk 71:1–15Google Scholar
  180. 179.
    Gwinner E (1968) Artspezifische Muster der Zugunruhe bei Laubsängern und ihre mögliche Bedeutung für die Beendigung des Zuges im Winterquartier. Z Tierpsychol 25:843–853Google Scholar
  181. 180.
    Gwinner E, Wiltschko W (1980) Circannual changes in migratory orientation of the garden warbler, Sylvia borin. Behav Ecol Sociobiol 7:73–78Google Scholar
  182. 181.
    Gwinner E (1981) Circannuale Rhytmen bei Tieren und ihre photoperiodische Synchronisation. Naturwissenschaften 68:542–551PubMedGoogle Scholar
  183. 182.
    Zucker I (2001) Circannual rhythms. In: Takahashi JS, Turek FW, Moore RY (eds) Handbook of behavioural neurobiology, vol 12, Circadian clocks. Kluwer/Plenum, New York, pp 511–528Google Scholar
  184. 183.
    Lincoln GA, Clarke IJ, Hut RA, Hazlerigg DG (2006) Characterizing a mammalian circannual pacemaker. Science 314:1941–1944PubMedGoogle Scholar
  185. 184.
    Enright JT (1963) The tidal rhythm of activity of a sand-beach amphipod. Z Vgl Physiol 46:276–313Google Scholar
  186. 185.
    Neumann D (1966) Die Lunare Und Tägliche Schlupfperiodik Der Mücke Clunio - Steuerung Und Abstimmung Auf Die Gezeitenperiodik. Z Vgl Physiol 53:1–61Google Scholar
  187. 186.
    Enright JT (1972) A virtuoso isopod – circa-lunar rhythms and their tidal fine-structure. J Comp Physiol 77:141–161Google Scholar
  188. 187.
    Lloyd M, Dybas HS (1966) Periodical cicada problem. 2. Evolution. Evolution 20:466–505Google Scholar
  189. 188.
    Daan S, Slopsema S (1978) Short-term rhythms in foraging behavior of common vole, Microtus arvalis. J Comp Physiol 127:215–227Google Scholar
  190. 189.
    Gerkema MP, Groos GA, Daan S (1990) Differential elimination of circadian and ultradian rhythmicity by hypothalamic lesions in the common vole, Microtus arvalis. J Biol Rhythms 5:81–95PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Unit of ChronobiologyUniversity of GroningenGroningenThe Netherlands

Personalised recommendations