Summary
The avian pineal gland contains a circadian pacemaker that oscillates in vitro. Using a flow-through culture system it is possible to measure melatonin production from very small subsections of an individual gland. We have used this technique to attempt to localize the oscillators in the pineal. Progressive tissue reduction did not affect the rhythmicity of cultured pineals. Multiple pieces (up to eight) from a single pineal all were capable of circadian oscillation — establishing directly that a pineal gland contains at least eight oscillators. All pineal pieces were responsive to light, and single light pulses shifted the phase of the melatonin rhythm. Because pieces equivalent to less than one per cent of the whole gland were rhythmic and because the capacity for oscillation was distributed throughout the gland, an individual pineal appears to be composed of a population of circadian oscillators.
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References
Aschoff J, Wever R (1981) The circadian system of man. In: Aschoff J (ed) Handbook of behavioral neurobiology, vol 4, Biological rhythms. Plenum Press, New York, pp 311–331
Beattie CW, Glennie FH (1966) Some aspects of the vascularization and chemical histology of the pineal gland inGallus. Anat Anz 118:396–404
Binkley S, Muller G, Hernandez T (1981) Circadian rhythm in pineal N-acetyltransferase activity: phase shifting by light pulses (I). J Neurochem 37:798–800
Bischoff MB (1969) Photoreceptoral and secretory structures in the avian pineal organ. J Ultrastruct Res 28:16–26
Block GD, Page TL (1978) Circadian pacemakers in the nervous system. Annu Rev Neurosci 1:19–34
Block GD, Roberts MH (1981) Circadian pacemaker in theBursatella eye: properties of the rhythm and its effects on locomotor behavior. J Comp Physiol 142:403–410
Block GD, Wallace SF (1982) Localization of a circadian pacemaker in the eye of a mollusk,Bulla. Science 217:155–157
Boya J, Calvo J (1978) Post-hatching evolution of the pineal gland of the chicken. Acta Anat 101:1–9
Boya J, Zamarano L (1975) Ultrastructure study of the pineal glands of the chicken (Gallus gallus). Acta Anat 92:202–226
Cassone VM, Menaker M (1983) Sympathetic regulation of chicken pineal rhythms. Brain Res 272:311–317
Deguchi T (1979) A circadian oscillator in cultured cells of chicken pineal gland. Nature 282:94–96
Dodt E (1973) Parietal eye (pineal and parietal organs) of lower vertebrates. In: Jung R (ed) Handbook of sensory physiology, vol VII/3B. Springer, Berlin Heidelberg New York, pp 113–140
Eakin RM (1973) The third eye. University of California Press, Berkeley
Eskin A (1971) Some properties of the system controlling the circadian activity rhythm of sparrows. In: Menaker M (ed) Biochronometry. Natl Acad Sci, Washington DC, pp 55–78
Eskin A (1979) Circadian system of theAplysia eye: Properties of the pacemaker and mechanisms of its entrainment. Fed Proc 38:2573–2579
Eskin A, Harcombe E (1977) Eye ofNavanax: optic activity, circadian rhythm and morphology. Comp Biochem Physiol 57A:443–449
Hudson DJ, Lickey M (1980) Internal desynchronization between the identified circadian oscillators inAplysia. Brain Res 183:481–485
Jacklet JW (1969) Circadian rhythm of optic nerve impulses recorded in darkness from isolated eye ofAplysia. Science 164:562–563
Jacklet JW, Geronimo J (1971) Circadian rhythm: population of interacting neurons. Science 174:299–302
Kasal C, Perez-Polo R (1980) In vitro evidence of photoreception in the chick pineal gland and its interaction with the circadian clock controlling N-acetyltransferase (NAT). J Neurosci Res 5:579–585
Kasal C, Menaker M, Perez-Polo R (1979) Circadian clock in culture: N-acetyltransferase activity of chick pineal glands oscillates in vitro. Science 203:656–658
Koehler WK, Fleissner G (1978) Internal desynchronization of bilaterally organized circadian oscillators in the visual system of insects. Nature 274:708–710
Menaker M, Oksche A (1974) Avian pineal gland. In: Farner DS, King JR (eds) Avian biology, vol IV. Academic Press, New York, pp 79–118
Moore-Ede MC, Sulzman FM (1981) Internal temporal order. In: Aschoff J (ed) Handbook of behavioral neurobiology, vol. 4. Biological rhythms. Plenum Press, New York, pp 215–241
Page T (1982) Transplantation of the cockroach circadian pacemaker. Science 216:73–75
Pittendrigh CS (1974) Circadian oscillations in cells and the circadian organization of multicellular systems. In: Schmitt FO, Worden FG (eds) The Neurosciences Third Study Program. MIT Press, Cambridge, pp 437–458
Ralph CL, Pelham RW, MacBride SE, Reilly DP (1974) Persistent rhythms of pineal and serum melatonin in cockerels in continuous darkness. J Endocrinol 63:319–324
Rollag MD, Niswender GD (1976) Radioimmunoassay of serum concentration of melatonin in sheep exposed to different lighting regimes. Endocrinology 98:482–489
Strumwasser F (1974) Neuronal principles organizing periodic behaviors. In: Schmitt FO, Worden FG (eds) The Neuro-sciences Third Study Program. MIT Press, Cambridge, pp 459–478
Takahashi JS (1981) Neural and endocrine regulation of avian circadian systems. PhD dissertation, Dept Biology and Inst Neuroscience, Univ Oregon, Eugene
Takahashi JS, Menaker M (1982) Entrainment of the circadian system of the house sparrow: a population of oscillators in pinealectomized birds. J Comp Physiol 146:245–253
Takahashi JS, Menaker M (1984) Circadian rhythmicity: regulation in the time domain. In: Yamamoto KR, Goldberger RF (eds) Biological regulation and development, vol 3B. Plenum Press, New York, (in press)
Takahashi JS, Zatz M (1982) Regulation of circadian rhythmicity. Science 217:1104–1111
Takahashi JS, Hamm H, Menaker M (1980) Circadian rhythms of melatonin release from individual superfused chicken pineal glands in vitro. Proc Natl Acad Sci USA 77:2319–2322
Underwood H (1977) Circadian organization in lizards: the role of the pineal organ. Science 195:587–589
Wight PAL, MacKenzie GM (1971) The histochemistry of the pineal gland of the domestic fowl. J Anat 108:261–273
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Takahashi, J.S., Menaker, M. Multiple redundant circadian oscillators within the isolated avian pineal gland. J. Comp. Physiol. 154, 435–440 (1984). https://doi.org/10.1007/BF00605243
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DOI: https://doi.org/10.1007/BF00605243