Fluoreszenzmikroskopische und elektronenmikroskopische Untersuchungen am Pinealorgan verschiedener Vogelarten

Article

Zusammenfassung

Mit der Fluoreszenzmethode von Falck-Hillarp lassen sich Artunterschiede im Innervationsmodus der Vogelepiphyse nachweisen. Bei Passer domesticus, Carduelis chloris, Pica pica, Corvus frugilegus und Gallus domesticus treten fluoreszierende adrenerge Nervenfasern nur perivaskulär, bei Anas platyrhynchos und Excalfactoria chinensis sowohl perivaskulär als auch im Parenchym, bei Columba livia lediglich vereinzelt im Parenchym auf. Die Fluoreszenzintensität des Epiphysenparenchyms von Passer domesticus und Columba livia, die nach mikrospektrographischen Messungen auf Serotonin beruht, schwankt stark von Fanggruppe zu Fanggruppe; die großen Unterschiede sind durch tagesrhythmische Schwankungen allein nicht erklärbar. In permanenter Dunkelheit nimmt die Serotoninfluoreszenz der Taubenepiphyse beträchtlich zu. Serotonin wird auch von den aminergen Nervenfasern der Vogelepiphyse gespeichert; seine Abgabe in die Blutbahn und deren physiologische Bedeutung werden diskutiert.

Die in das Lumen der Vogelepiphyse hineinragenden, von modifizierten Zilien der Pinealozyten ausgehenden Membranwirbel zeigen mit der Osmierung nach Eakin, Brandenburger, Kopsch, Kolatschev gleichartige Partikel (Durchmesser 50 Å) wie die regulär gebauten Außenglieder der retinalen und pinealen Photorezeptoren. Diese Befunde werden mit elektrophysiologischen, biochemischen und verhaltensphysiologischen Ergebnissen verglichen.

Fluorescence and electron microscope investigations of the avian pineal organ

Summary

The adrenergic innervation and the parenchymal 5-HT in the pineal organ of different avian species were investigated with the method of Falck-Hillarp. The fluorophores were identified microspectrographically. An entirely perivascular localization of adrenergic nerve fibres was observed in the pineal organs of Passer domesticus, Carduelis chloris, Pica pica, Corvus frugilegus and Gallus domesticus. The pineal organs of Anas platyrhynchos and Excalfactoria chinensis showed both perivascular and parenchymal innervation. Perivascular fibres were absent from the pineal organ of Columba livia, and only a few fine fluorescent fibres appeared in its parenchyma after pretreatment with l-dopa. The intensity of the 5-HT fluorescence of the parenchyma cells showed a high individual variability. These differences apparently do not reflect a circadian 5-HT-rhythm. Continuous darkness increased the intensity of the 5-HT-fluorescence in the pineal organ of Columba livia. 5-HT was also demonstrated within the perivascular autonomic nerve fibres of the avian pineal organ. It is probable that 5-HT is released from the pineal parenchyma into the circulation.

After prolonged osmium tetroxide treatment according to Eakin, Brandenburger, Kopsch, Kolatschev, the membrane whorls that are formed by the cilia of avian pinealocytes showed osmiophilic particles 50 Å in diameter. Similar particles have been observed in the regular outer segments of retinal and pineal photoreceptor cells of lower vertebrates. The above morphological results are discussed in view of electrophysiological, biochemical and behavioural observations.

Key words

Avian pineal organ 5-HT Adrenergic innervation Light-dependent functions 

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Literatur

  1. Altner, H.: Persönliche Mitteilung.Google Scholar
  2. Axelrod, J., Wurtman, R.J., Winget, Ch. M.: Melatonin synthesis in the hen pineal gland and its control by light. Nature (Lond.) 201, 1134 (1964).Google Scholar
  3. Azmitia, E.C., Algeri, S., Costa, E.: In vivo conversion of 3H-L-tryptophan into 3H-serotonin in brain areas of adrenalectomized rats. Science 169, 201–203 (1970).Google Scholar
  4. Banerjee, U., Burks, T.D., Feldberg, W., Goodrich, C.A.: Temperature responses and other effects of 5-hydroxytryptophan and 5-hydroxytryptamine when acting from the liquor space in unanaesthetized rabbits. Brit. J. Pharmacol. 38, 688–701 (1970).Google Scholar
  5. Benoit, J.: The role of the eye and of the hypothalamus in the photostimulation of gonads in the duck. Ann. N. Y. Acad. Sci. 117, 204–217 (1964).Google Scholar
  6. Bern, H.A.: Comparison of the innervation of the pituitary of two eurohyaline teleost fishes, Gillichthys mirabilis and Tilapia mossambica, with special reference to the origin and nature of type “B” fibers. In: Subcellular organization and function in endocrine tissues (eds. H. Heller u. K. Lederis). Memoirs of the Society for Endocrinol. vol. 19, p. 817–822. Cambridge: University Press 1971.Google Scholar
  7. Bertler, A., Falck, B., Owman, Ch.: Cellular localization of 5-hydroxytryptamine in the rat pineal organ. Kungl. Fysiogr. Sällsk. Lund Förh. 33, 13–16 (1963).Google Scholar
  8. Bertler, A., Falck, B., Owman, Ch.: Studies on 5-hydroxytryptamine stores in pineal gland of rat. Acta physiol. scand. 63, Suppl. 239, 1–18 (1964).Google Scholar
  9. Binkley, S., Kluth, E., Menaker, M.: Pineal function in sparrows: circadian rhythms and body temperature. Science 174, 311–314 (1971).Google Scholar
  10. Bischoff, M.B.: Photoreceptoral and secretory structures in the avian pineal organ. J. Ultrastruct. Res. 28, 16–26 (1969).Google Scholar
  11. Björklund, A., Ehinger, B., Falck, B.: A method for differentiating dopamine from noradrenaline in tissue sections by microspectrofluorometry. J. Histochem. Cytochem. 16, 263–270 (1968).Google Scholar
  12. Björklund, A., Falck, B., Owman, Ch.: Fluorescence microscopic and microspectrofluorometric techniques for the cellular localization and characterization of biogenic amines. In: Methods of investigative and diagnostic endocrinology (ed. J. Kopin). North Holland Publ. Company 1972.Google Scholar
  13. Björklund, A., Falck, B., Stenevi, U.: On the possible existence of a new intraneuronal monoamine in the spinal cord of the rat. J. Pharmacol. exp. Ther. 175, 525–532 (1970).Google Scholar
  14. Böttger, W.V., Böttger, E.M., Ueck, M.: Autoradiographischer und quantitativer Nachweis von Vitamin A in der Epiphysis cerebri von Rana esculenta im Licht-Dunkelversuch. (In Vorbereitung.)Google Scholar
  15. Bruinvels, J.: Effect of noradrenaline, dopamine and 5-hydroxytryptamine on body temperature in the rat after intracisternal administration. Neuropharmacol. 9, 277–282 (1970).Google Scholar
  16. Collin, J.-P.: Contribution à l'étude de l'organe pinéal. De l'épiphyse sensorielle à la glande pinéale: Modalités de transformation et implications fonctionelles. Ann. Stat. Biol. de Besse-en-Chandesse, Suppl. 1, 1–359 (1969a).Google Scholar
  17. Collin, J.-P.: Distinction et rapports entre les pédicules basaux des photorécepteurs rudimentaires sécrétoires et les afférences nerveuses monoaminergiques de l'épiphyse d'Oiseau. Recherches chez le poussin de Passereau (Pica pica L.). C. R. Soc. Biol. (Paris) 163, 1137 (1969b).Google Scholar
  18. Collin, J.-P., Meiniel, A., Vernerey, S.: L'organe pinéal. Études combinées ultrastructurales, cytochimiques (monoamines) et expérimentales, chez Testudo mauritanica. Grains denses des cellules de la lignée «sensorielle» chez les vertébrés. Arch. Anat. micr. Morph. exp. 60, 269–304 (1971).Google Scholar
  19. Eakin, R.M., Brandenburger, J.L.: Osmic staining of amphibian and gastropod photoreceptors. J. Ultrastruct. Res. 30, 619–641 (1970).Google Scholar
  20. Falck, B., Owman, Ch.: A detailed methodological description of the fluorescence method for the cellular demonstration of biogenic monoamines. Acta Univ. Lund., Sectio II, 7, 1–23 (1965).Google Scholar
  21. Feldstein, A., Chang, F.H., Kucharski, J.M.: Tryptophol, 5-hydroxytryptophol and 5-methyl-tryptophol induced sleep in mice. Life Sci. 9, 323–329 (1970).Google Scholar
  22. Fenwick, J.C.: Brain serotonin and swimming activity in the goldfish, Carassius auratus. Comp. Biochem. Physiol. 32, 803–806 (1970).Google Scholar
  23. Friend, D.S.: Cytochemical staining of multivesicular body and Golgi vesicles. J. Cell Biol. 41, 269–279 (1969).Google Scholar
  24. Friend, D.S., Murray, M.J.: Osmium impregnation of the Golgi apparatus. Amer. J. Anat. 117, 135–150 (1965).Google Scholar
  25. Fujie, E.: Ultrastructure of the pineal body of the domestic chicken, with special reference of the changes induced by altered photoperiods. Arch. histol. jap. 29, 271–302 (1968).Google Scholar
  26. Fuxe, K., Hökfelt, T., Jonsson, G., Ungerstedt, U.: Fluorescence microscopy in neuroanatomy. In: Contemporary research in neuroanatomy (ed. W.J.H. Nauta and S.O.E. Ebbesson), p. 275–314. Berlin-Heidelberg-New York: Springer 1970.Google Scholar
  27. Gaston, S., Menaker, M.: Pineal function: the biological clock in the sparrow? Science 7, 1125–1127 (1968).Google Scholar
  28. Gessa, G.L., Tagliamonte, A., Tagliamonte, P., Brodie, B.: Essential role of testosterone in the sexual stimulation induced by p-chlorophenylalanine in male animals. Nature (Lond.) 227, 616–617 (1970).Google Scholar
  29. Hafeez, M.A., Quay, W.B.: Histochemical and experimental studies of 5-hydroxytryptamine in pineal organs of teleosts (Salmo gairdneri and Atherinopsis californiensis). Gen. comp. Endocr. 13, 211–217 (1969).Google Scholar
  30. Hamasaki, D.I.: Persönliche Mitteilung. In: Oksche, A., Kirschstein, H.: Z. Zellforsch. 102, 214–241 (1969).Google Scholar
  31. Hedlund, L.: Sympathetic innervation of the avian pineal body. Anat. Rec. 166, 406 (1970).Google Scholar
  32. Hedlund, L., Nalbandov, A.V.: Innervation of the avian pineal body. Amer. Zool. 9, 1090 (1969).Google Scholar
  33. Hedlund, L., Ralph, C.L., Chepho, J., Lynch, H.J.: A diurnal serotonin cycle in the pineal body of Japanese quail: photoperiod phasing and the effect of superior cervical ganglionectomy. Gen. comp. Endocr. 16, 52–58 (1971).Google Scholar
  34. Kamberi, I.A., Mical, R.S., Porter, J.C.: Effect of anterior pituitary perfusion and intraventricular injection of catecholamines and indolamines on LH release. Endocrinology 87, 1–12 (1970).Google Scholar
  35. Kappers, J. Ariëns: The development, topographical relations and innervation of the epiphysis cerebri in the albino rat. Z. Zellforsch. 52, 163–215 (1960).Google Scholar
  36. Kappers, J. Ariëns: The mammalian pineal organ. J. Neuro-Visc. Rel., Suppl. IX, 140–184 (1969).Google Scholar
  37. Krass, M.E., La Bella, F.S., Shin, S.H., Minnich, J.: Biochemical features on the pineal compared with other endocrine and nervous tissues. In: Subcellular organization and function in endocrine tissues (eds. H. Heller u. K. Lederis). Memoirs of the Society for Endocrinol. vol. 19, p. 49–76. Cambridge: University Press 1971.Google Scholar
  38. Lauber, J.K., Boyd, J.E., Axelrod, J.: Enzymatic synthesis of melatonin in the avian pineal body; extraretinal responses to light. Science 161, 489–490 (1968).Google Scholar
  39. Möllmann, H., Niemeyer, D.H., Alfes, H., Knoche, H.: Mikrospektrofluorometrische Unterschungen der biogenen Amine im Glomus caroticum des Kaninchens nach Reserpinund PCPA-Application. Z. Zellforsch. 126, 104–115 (1972).Google Scholar
  40. Morita, Y.: Absence of electrical activity of the pigeon's pineal organ in response to light. Experientia (Basel) 22, 402 (1966).Google Scholar
  41. Norberg, K.-A.: Transmitter histochemistry of the sympathetic adrenergic nervous system. Brain Res. 5, 125–170 (1967).Google Scholar
  42. Oksche, A.: Zur Frage extraretinaler Photorezeptoren im Pinealorgan der Vögel. Arch. Anat. (Strasbourg) 51, 497–507 (1968).Google Scholar
  43. Oksche, A., Kirschstein, H.: Elektronenmikroskopische Untersuchungen am Pinealorgan von Passer domesticus. Z. Zellforsch. 102, 214–241 (1969).Google Scholar
  44. Oksche, A., Kirschstein, H., Kobayashi, H., Farner, D.S.: Electron microscopic and experimental studies of the pineal organ in the white-crowned sparrow, Zonotrichia leucophrys gambelii. Z. Zellforsch. 124, 247–274 (1972).Google Scholar
  45. Oksche, A., Morita, Y., Vaupel-von Harnack, M.: Zur Feinstruktur und Funktion des Pinealorgans der Taube (Columba livia). Z. Zellforsch. 102, 1–30 (1969).Google Scholar
  46. Oksche, A., Ueck, M., Rüdeberg, C.: Comparative ultrastructural studies of sensory and secretory elements in pineal organs. In: Subcellular organization and function in endocrine tissues (eds. H. Heller and K. Lederis). Memoirs of the Society for Endocrinol. vol. 19, p. 7–25. Cambridge: University Press 1971.Google Scholar
  47. Oksche, A., Vaupel-von Harnack, M.: Elektronenmikroskopische Untersuchungen zur Frage der Sinneszellen im Pinealorgan der Vögel. Z. Zellforsch. 69, 41–60 (1966).Google Scholar
  48. Owman, Ch.: New aspects of the mammalian pineal gland, p. 1–40. Lund: Håkan Ohlssons Boktryckerij 1964a.Google Scholar
  49. Owman, Ch.: Sympathetic nerves probably storing two different types of monoamine in the rat pineal gland. Int. J. Neuropharmacol. 2, 105–112 (1964b).Google Scholar
  50. Owman, Ch.: Localization of neuronal and parenchymal monoamines under normal and experimental conditions in the mammalian pineal gland. Progr. Brain Res. 10, 423–453 (1965).Google Scholar
  51. Owman, Ch., Rüdeberg, C.: Light, fluorescence, and electron microscopic studies on the pineal organ of the pike, Esox lucius L., with special regard to 5-hydroxytryptamine. Z. Zellforsch. 107, 522–550 (1970).Google Scholar
  52. Owman, Ch., Rüdeberg, C., Ueck, M.: Fluoreszenzmikroskopischer Nachweis biogener Monoamine in der Epiphysis cerebri von Rana esculenta und Rana pipiens. Z. Zellforsch. 111, 550–558 (1970).Google Scholar
  53. Owman, Ch., Rüdeberg, C., Ueck, M.: Unveröffentlichte Befunde.Google Scholar
  54. Quay, W.B.: Rhythmic and light-induced changes in levels of pineal 5-hydroxyindoles in the pigeon (Columba livia). Gen. comp. Endocr. 6, 371–377 (1966).Google Scholar
  55. Quay, W.B.: Endocrine effects of the mammalian pineal. Amer. Zool. 10, 237–246 (1970).Google Scholar
  56. Quay, W.B., Kappers, J. Ariëns, Jongkind, J.F.: Innervation and fluorescence histochemistry of monoamines in the pineal organ of a snake (Natrix natrix). J. Neuro-Visc. Rel. 31, 11–25 (1968).Google Scholar
  57. Quay, W.B., Renzoni, A., Eakin, R.M.: Pineal ultrastructure in Melopsittacus undulatus with particular regard to cell types and functions. Riv. Biol. 61, 371–393 (1968).Google Scholar
  58. Ralph, C.L.: Structure and alleged functions of avian pineals. Amer. Zool. 10, 217–235 (1970).Google Scholar
  59. Ralph, C.L., Dawson, D.C.: Failure of the pineal body of two species of birds (Coturnix coturnix japonica and Passer domesticus) to show electrical responses to illumination. Experientia (Basel) 24, 147–148 (1968).Google Scholar
  60. Rosner, J.M., Declercq de Pérez Bedéz, G., Cardinali, D.P.: Direct effect of light on duck pineal explants. Life Sci. 10, 1065–1069 (1971).Google Scholar
  61. Rüdeberg, C.: A rapid method for staining thin sections of Vestopal W-embedded tissue for light microscopy. Experientia (Basel) 23, 792 (1967).Google Scholar
  62. Stammer, A.: Untersuchungen über die Struktur und die Innervation der Epiphyse bei Vögeln. Acta Biol., Nova Ser., Acta Univ. Szeged. 7, 65–75 (1961).Google Scholar
  63. Stammer, A.: Light and electron microscopic investigations on the pineal organ of pigeon. Abstr. of Vth. Confer. of Europ. Compar. Endocrinologists. 154, Utrecht 1969.Google Scholar
  64. Stern, H.: Serotonin and its effects on the pituitary-adrenal axis in depression. Chicago Med. School Quart. 29, 24–30 (1970).Google Scholar
  65. Ueck, M.: Granulierte marklose Nervenfasern in der Epiphysenregion von Anuren. Z. Zellforsch. 90, 389–402 (1968).Google Scholar
  66. Ueck, M.: Zur Ultrastruktur der Epiphysis cerebri der Vögel. Zool. Anz., Suppl. 33, Verh. Zool. Ges. 509–518 (1969).Google Scholar
  67. Ueck, M.: Weitere Untersuchungen zur Feinstruktur und Innervation des Pinealorgans von Passer domesticus L. Z. Zellforsch. 105, 276–302 (1970).Google Scholar
  68. Ueck, M.: Strukturbesonderheiten der Anurenepiphyse nach prolongierter Osmierung und Anwendung der Acetylcholinesterase-Reaktion. Z. Zellforsch. 112, 526–541 (1971).Google Scholar
  69. Ueck, M.: Kobayashi, H.: Vergleichende Untersuchungen über acetylcholinesterase-haltige Neurone im Pinealorgan der Vögel. Z. Zellforsch. 129, 140–160 (1972).Google Scholar
  70. Wartenberg, H., Baumgarten, H.G.: Untersuchungen zur fluoreszenz- und elektronen-mikroskopischen Darstellung von 5-Hydroxytryptamin (5-HT) im Pineal-Organ von Lacerta viridis und L. muralis. Z. Anat. Entwickl.-Gesch. 128, 185–210 (1969).Google Scholar
  71. Wurtman, R.J., Axelrod, J., Fischer, J.E.: Melatonin synthesis in the pineal gland: effect of light mediated by the sympathetic nervous systems. Science 143, 1328–1330 (1964).Google Scholar
  72. Wurtman, R.J., Axelrod, J., Kelly, D.E.: The pineal. New York and London: Academic Press 1968.Google Scholar
  73. Zimmermann, H.: Ultrastrukturelle und cytochemische Untersuchungen am Saccus vasculosus von Knochenfischen unter besonderer Berücksichtigung der Innervation. Z. Zellforsch. 126, 240–260 (1972).Google Scholar

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© Springer-Verlag 1973

Authors and Affiliations

  • M. Ueck
    • 1
  1. 1.Anatomisches Institut der Universität GießenGermany

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