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Neural elements of the pineal complex of the frog, rena esculenta, I: Centrally projecting neurons

Published online by Cambridge University Press:  02 June 2009

Peter Ekström  and
Hilmar Meissl
Peter Ekström
Affiliation:
Laboratory of Molecular Neuroanatomy, Department of Zoology, University of Lund, Lund, Sweden
Hilmar Meissl
Affiliation:
Max Planck Institute for Physiological and Clinical Research, Bad Nauheim, Federal Republic of Germany
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Abstract

The pineal complex of anuran &hibians is a directly photosensory organ, encompassing both an extracranial portion, the frontal organ, and an intracranial portion, the pineal organ proper. The projection neurons of the frontal organ respond differentially according to the wavelengths of the light stimuli. The pineal organ, on the other hand, functions mainly as a luminosity meter. Most of its centrally projecting neurons respond to all increases in ambient illumination with decreases in spontaneous firing of action potentials, although some neural units in the pineal organ may respond according to wavelength. This difference in responses to light stimulation may be reflected in the neural organization of the two parts of the pineal complex. In the present study, we have analyzed the morphology of the projection neurons of the frontal and pineal organs of the frog, Rana esculenta, by backfilling of the neurons with horseradish peroxidase through their cut axons. In the pineal organ, several types of centrally projecting neurons were observed: peripherally situated unipolar and multipolar neurons, the dendrites of which extend into a superficial axon plexus that surrounds the pineal epithelium; smaller unipolar, bipolar, or multipolar neurons situated close to the central pineal tract; and radially oriented bipolar neurons, with short dendritic processes oriented towards the lumen of the pineal organ. This latter type was strongly reminiscent of photoreceptor cells. The centrally projecting neurons of the frontal organ were multipolar, and situated in the ventral part of the organ. One photoreceptor-like bipolar neuron was observed in one frontal organ. The neurons of the frontal organ did not form a superficial plexus of neurites. This difference may relate to the different ratio of chromaticity/luminosity units in the frontal and pineal organs.

Keywords

Pineal complexProjection neuronsHorseradish peroxidaseRana esculenta (&hibia)
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 5 , May 1990 , pp. 389 - 397
Copyright
Copyright © Cambridge University Press 1990

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References

Abercrombie, M. (1946). Estimation of nuclear population from microtome sections. Anatomical Record 94, 239–247.CrossRefGoogle ScholarPubMed
Collin, J.-P.&;Oksche, A. (1981). Structural and functional relationships in the nonmammalian pineal organ. In The Pineal Gland, Vol.I. Anatomy and Biochemistry, ed. Reiter, R.J., pp. 27–67. Boca Raton, Florida: CRC Press, Inc.Google Scholar
Dodt, E. (1973). The parietal eye (pineal and parietal organs) of lower vertebrates. In Handbook of Sensory Physiology, Vol. VII/3B, ed. Jung, R., pp. 113–140. New York, Berlin, Heidelberg: Springer-Verlag.Google Scholar
Dodt, E.&;Heerd, E. (1962). Mode of action of pineal nerve fibers in frogs. Journal of Neurophysiology 25, 405–429.CrossRefGoogle ScholarPubMed
Dodt, E.&;Jacobson, M. (1963). Photosensitivity of a localized region of the frog diencephalon. Journal of Neurophysiology 26, 752–758.CrossRefGoogle ScholarPubMed
Dodt, E.&;Morita, Y. (1964). Purkinje-Verschiebung, absolute Schwelle und adaptives Verhalten einzelner Elemente der intrakranialen Anuren-Epiphyse. Vision Research 4, 413–421.CrossRefGoogle Scholar
Eakin, R.M. (1961). Photoreceptors in the &;hibian frontal organ. Proceedings of the National Academy of Sciences 47, 1084–1088.CrossRefGoogle ScholarPubMed
Eakin, R.M.&;Westfall, J.A. (1961). The development of photoreceptors in the Stirnorgan of the treefrog, Hyla regilla. Embryologia 6, 84–98.CrossRefGoogle Scholar
Ekström, P. (1984). Central neural connections of the pineal organ and retina in the teleost Gasterosteus aculeatus L. Journal of Comparative Neurology 226, 321–335.CrossRefGoogle ScholarPubMed
Ekström, P. (1985). Anterograde and retrograde filling of central neural systems with horseradish peroxidase under in vitro conditions. Journal of Neuroscience Methods 15, 21–35.CrossRefGoogle Scholar
Ekström, P. (1987). Photoreceptors and CSF-contacting neurons in the pineal organ of a teleost fish have direct axonal connections with the brain: an HRP–electron-microscopic study. Journal of Neuroscience 7, 987–995.CrossRefGoogle Scholar
Ekström, P.&;Korf, H.-W. (1985). Pineal neurons projecting to the brain of the rainbow trout, Salmo gairdneri Richardson (Teleostei). In vitro retrograde filling with horseradish peroxidase. Cell and Tissue Research 240, 693–700.CrossRefGoogle Scholar
Ekström, P.&;Korf, H.-W. (1986). Putative cholinergic elements in the photosensory pineal organ and retina of a teleost, Phoxinus phoxinus L. (Cyprinidae). Distribution of choline acetyltransferase immunoreactivity, acetylcholinesterase-positive elements, and pinealofugally projecting neurons. Cell and Tissue Research 246, 321–329.CrossRefGoogle ScholarPubMed
Ekström, P.&;Meissl, H. (1988). Intracellular staining of physiologically identified photoreceptor cells and hyperpolarizing interneurons in the teleost pineal organ. Neuroscience 25, 1061–1070.CrossRefGoogle ScholarPubMed
Ekström, P.&;Meissl, H. (1989). Signal processing in a simple vertebrate photoreceptor system: the teleost pineal organ. Physiologica Bohemoslovacica 38, 311–326.Google Scholar
Ekström, P., östholm, T., Meissl, H., Bruun, A., Richards, J.G.,&; Möhler, H. (1990). Neural elements in the pineal complex of the frog, Rana esculenta, II: GABA-immunoreactive neurons and FMRFamide-immunoreactive efferent axons. Visual Neuroscience 4, 399–412.CrossRefGoogle ScholarPubMed
Ekström, P.&;Van Veen, Th. (1983). Central connections of the pineal organ in the three-spined stickleback, Gasterosteus aculeatus L. (Teleostei). Cell and Tissue Research 232, 141–155.CrossRefGoogle ScholarPubMed
Ekström, P.&;Van, Veen Th. (1984). Pineal neural connections with the brain in two teleosts, the crucian carp and the European eel. Journal of Pineal Research 1, 245–261.CrossRefGoogle ScholarPubMed
Ekström, P., Foster, R.G., Korf, H.-W.&;Schalken, J.J. (1987). Antibodies against retinal photoreceptor-specific proteins reveal axonal projections from the photosensory pineal organ in teleosts. Journal of Comparative Neurology 265, 25–33.CrossRefGoogle ScholarPubMed
Eldred, W.D.&;Nolte, J. (1978). Pineal photoreceptors: evidence for a vertebrate visual pigment with two physiologically active states. Vision Research 18, 29–32.CrossRefGoogle ScholarPubMed
Elered, W.D.&;Nolte, J. (1981). Multiple classes of photoreceptors and neurons in the frontal organ of Rana pipiens. Journal of Comparative Neurology 203, 269–295.CrossRefGoogle Scholar
Glaser, R. (1958). Increase in locomotor activity following shielding of the parietal eye in night lizards. Science 128, 1577–1578.CrossRefGoogle ScholarPubMed
Hafeez, M.A.&;Zerihun, L. (1974). Studies on central projections of the pineal nerve tract in rainbow trout, Salmo gairdneri Richardson, using cobalt chloride iontophoresis. Cell and Tissue Research 154, 485–510.CrossRefGoogle ScholarPubMed
Hamasaki, D.I.&;Esserman, L. (1976). Neural activity of the frog's frontal organ during steady illumination. Journal of Comparative Physiology 109, 279–285.CrossRefGoogle Scholar
Holmgren, N. (1918). Zur Kenntnis der Parietalorgane von Rana temporaria. Arkiv för Zoologi 11/24, 1–13.Google Scholar
Kelly, D.E.&;Smith, S.W. (1964). Fine structure of the pineal organs of the adult frog, Rana pipiens. Journal of Cell Biology 22, 653–674.CrossRefGoogle ScholarPubMed
Kelly, D.E.&;van De Kamer, J.C. (1960). Cytological and histochemical investigations on the pineal organ of the adult frog (Rana esculenta). Zeitschrrft für Zellforschung 52, 618–639.CrossRefGoogle ScholarPubMed
Korf, H.-W., Oksche, A., Ekström, P., Gery, I., Zigler, J.S.&;Klein, D.C. (1986). Pinealocyte projections into the mammalian brain revealed with S-antigen antiserum. Science 231, 735–737.CrossRefGoogle ScholarPubMed
Mcfarland, W.N. (1986). Light in the sea—correlations with behaviors of fishes and invertebrates. American Zoologist 26, 389–401.CrossRefGoogle Scholar
Meissl, H.&;Dodt, E. (1981). Comparative physiology of pineal photoreceptor organs. In The Pineal Organ: Photobiology—Biochronometry—Endocrinology, eds, Oksche, A.&;Pévet, P., pp. 61–80. Amsterdam: Elsevier/North-Holland Biomedical Press.Google Scholar
Meissl, H.&;Donley, C.S. (1980). Change of threshold after light adaptation of the chromatic response of the frog's pineal organ. Vision Research 20, 379–383.CrossRefGoogle ScholarPubMed
Meissl, H.&;George, S. (1984). Electrophysiological studies on neuronal transmission in the frog's photosensory pineal organ. The effect of amino acids and biogenic amines. Vision Research 24, 1727–1734.CrossRefGoogle ScholarPubMed
Meissl, H.&;George, S. (1985). Effect of GABA and its antagonists, bicuculline and picrotoxin, on nerve cell discharges of the photosensory pineal organ of the frog, Rana esculenta. Brain Research 332, 39–46.CrossRefGoogle ScholarPubMed
Morita, Y. (1965). Extra- und intrazelluläre Ableitungen einzelner Elemente des lichtempfindlichen Zwischenhirns anurer &hibien. Pflügers Archiv für Gesamte Physiologie 286, 97–108.CrossRefGoogle Scholar
Morita, Y. (1969). Wellenlängen-Diskriminatoren im intrakranialen Pinealorgan von Rana catesbeyana. Experientia (Basel) 25, 1277.CrossRefGoogle Scholar
Morita, Y. (1971). Post-tetanic activity changes of the frog's neurosensory pineal end vesicle (Stirnorgan). Pflügers Archiv 328, 135–144.CrossRefGoogle ScholarPubMed
Morita, Y.&;Dodt, E. (1965). Nervous activity of the frog's epiphysis cerebri in relation to illumination. Experientia 21, 221–222.CrossRefGoogle ScholarPubMed
Oksche, A. (1952). Der Feinbau des Organon frontale bei Rana temporaria und seine funktionelle bedeutung. Morphologisches Jahrbuch 92, 123–167.Google Scholar
Oksche, A. (1955). Untersuchungen über die Nervenzellen und Nervenverbindungen des Stirnorgans, der Epiphyse und des Subcommissuralorgans bei anuren &hibien. Gegenbaurs Jahrbuch 95, 393–425.Google Scholar
Oksche, A.&;von Harnack, M. (1962). Elektronenmikroskopische Untersuchungen am Stirnorgan (Frontalorgan, Epiphysenendblase)von Rana temporaria und Rana esculenta. Naturwissenschaflen 49,429–430.CrossRefGoogle Scholar
Oksche, A.&;Vaupel-von Harnack, M. (1963). Elektronenmikroskopische Untersuchungen an der Epiphysis cerebri von Rana esculenta L. Zeitschrift für Zellforchung 59, 582–614.CrossRefGoogle Scholar
Oksche, A.&;Vaupel-von Harnack, M. (1965). Elektronenmikroskopische Untersuchungen an den Nervenbahnen des Pinealkomplexes von Rana esculenta L. Zeitschrift für Zellforschung 68, 389–426.CrossRefGoogle ScholarPubMed
Owman, Ch., Rüdeberg, C.&;Ueck, M. (1970). Fluoreszenzmikroskopischer Nachweis biogener Monoamine in der Epiphysis cerebri von Rana esculenta und Rana pipiens. Zeitschrift für Zellforschung 111, 550–558.CrossRefGoogle ScholarPubMed
Paul, E., Hartwig, H.-G.&;Oksche, A. (1971). Neurone und zentralnervöse Verbindungen des Pinealorgans der Anuren. Zeitschrift für Zellforschung 112, 466–493.CrossRefGoogle Scholar
Riech, F. (1925). Epiphyse und Paraphyse im Lebenscyclus der Anuren. Zeitschrift für Vergleichende Physiologie 2, 524–570.CrossRefGoogle Scholar
Vollrath, L. (1981). The Pineal Organ. Handbuch der Mikroskopischen Anatomie des Menschen, VI/7. Berlin, Heidelberg, New York: Springer-Verlag.Google Scholar
Wake, K., Ueck, M.&;Oksche, A. (1974). Acetylcholinesterase-containing nerve cells in the pineal complex and subcommissural area of the frogs, Rana ridibunda and Rana esculenla. Cell and Tissue Research 154, 423–442.CrossRefGoogle Scholar