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Melatonin modulates the neural activity in the photosensory pineal organ of the trout: Evidence for endocrine-neuronal interactions

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Summary

Hormonal and neural signals transmitted from the pineal organ to the brain in cold-blooded vertebrates presumably convert information about the ambient illumination into signals which may be used to mediate photoperiodic and circadian responses. The possible intrapineal function of melatonin was investigated by recording intra- and extracellularly from photoreceptors and second-order neurons in the isolated superfused pineal organ of the trout (Salmo gairdneri). Melatonin added through the perfusion bath to the explanted pineal organ caused a dose-related and reversible inhibition of ganglion cells of the luminance type whereas the hormone did not significantly affect the membrane potential of photoreceptors and their light-evoked response. The observed effects seem to be independent from photoperiod and adaptation conditions. These results suggest that melatonin provides a feedforward signal to intrapineal neurons regulating the neural output of the organ.

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References

  • Besharse JC, Dunis DA (1983) Methoxyindoles and photoreceptor metabolism: activation of rod shedding. Science 219:1341–1343

    Google Scholar 

  • Besharse JC, Iuvone DM (1983) Circadian clocks in Xenopus eye controlling retinal serotonin N-acetyltransferase. Nature 305:133–135

    Google Scholar 

  • Birks EK, Ewing RD (1986) Seasonal changes in pineal melatonin content and hydroxyindole-O-methyltransferase activity in juvenile chinook salmon, Oncorhynchus tshawytscha. Gen Comp Endocrinol 64:91–98

    Google Scholar 

  • Cahill GM, Besharse JC (1989) Retinal melatonin is metabolized within the eye of Xenopus laevis. Proc Natl Acad Sci 86:1098–1102

    Google Scholar 

  • Cassone VM, Roberts MH, Moore RY (1987) Effects of melatonin on 2-deoxy-[1-14C]glucose uptake within rat suprachiasmatic nucleus. Am J Physiol 255:R332-R337

    Google Scholar 

  • Chéze G, Ali MA (1976) Rôle de l'épiphyse dans la migration du pigment épithélial rétinien chez quelques Téléostéens. Can J Zool 54:475–481

    Google Scholar 

  • Dodt E (1963) Photosensitivity of the pineal organ in the teleost, Salmo irideus (Gibbons). Experientia 19:642

    Google Scholar 

  • Dodt E (1973) The parietal eye (pineal and parietal organs) of lower vertebrates. In: Jung R (ed) Central Visual Information (Handbook of sensory physiol vol VII/3B). Springer, Berlin Heidelberg New York, pp 113–140

    Google Scholar 

  • Dodt E, Heerd E (1962) Mode of action of pineal nerve fibers in frogs. J Neurophysiol 26:752–758

    Google Scholar 

  • Dubocovich ML (1983) Melatonin is a potent modulator of dopamine release in the retina. Nature 306:782–784

    Google Scholar 

  • Dubocovich ML (1985) Characterization of a retinal melatonin receptor. J Pharmacol Exp Ther 234:395–401

    Google Scholar 

  • Dubocovich ML (1988) Role of melatonin in retina. In: Osborne NN, Chader GJ (eds) Progr Retinal Res Vol. 8, Pergamon Press, Oxford, pp 129–151

    Google Scholar 

  • Eakin RE, Westfall JA (1960) Further observations on the fine structure of the parietal eye of lizards. J Biophys Biochem Cytol 8:483–499

    Google Scholar 

  • Ekström P (1984) Central connections of the pineal organ in the three spined stickleback, Gasterosteus aculeatus L. (Teleostei). Cell Tissue Res 232:141–155

    Google 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-electronmicroscopic study. J Neurosci 7:987–995

    Google Scholar 

  • Ekström P, Meissl H (1988) Intracellular staining of physiologically identified photoreceptor cells and hyperpolarizing interneurons in the teleost pineal organ. Neurosci 25:1061–1070

    Google Scholar 

  • Ekström P, Veen Th van (1984) Pineal neural connections with the brain in two teleosts, the crucian carp and the European eel. J Pineal Res 1:245–261

    Google Scholar 

  • Falcon J, Meissl H (1981) The photosensory function of the pineal organ of the pike (Esox lucius L.): correlation between structure and function. J Comp Physiol 144:127–137

    Google Scholar 

  • Falcón J, Geffard M, Juillard MT, Delaage M, Collin JP (1981) Melatonin-like immunoreactivity in photoreceptor cells: a study in the teleost pineal organ and the concept of photoneuroendocrine cells. Biol Cell 42:65–68

    Google Scholar 

  • Falcon J, Guerlotté JF, Voisin P, Collin JP (1987) Rhythmic melatonin biosynthesis in a photoreceptive pineal organ: a study in the pike. Neuroendocrinol 45:479–486

    Google Scholar 

  • Falcón J, Brun-Marmillon J, Claustrat B, Collin JP (1989) Regulation of melatonin secretion in a photoreceptive pineal organ: an in vitro study in the pike. J Neurosci 9:1943–1950

    Google Scholar 

  • Foà A, Menaker M (1988) Contribution of pineal and retinae to the circadian rhythms of circulating melatonin in pigeons. J Comp Physiol A 164:25–30

    Google Scholar 

  • Gern WA, Greenhouse SS (1988) Examination of in vitro melatonin secretion from superfused trout (Salmo gairdneri) pineal organs maintained under diel illumination or continuous darkness. Gen Comp Endocrinol 71:163–174

    Google Scholar 

  • Gern WA, Ralph LL (1979) Melatonin synthesis by the retina. Science 204:183–184

    Google Scholar 

  • Goudie CA, Davies KB, Simco BA (1983) Influence of the eyes and pineal gland on locomotor activity patterns of channel catfish Ictalurus punctatus. Physiol Zool 56:10–17

    Google Scholar 

  • Joss JMP (1977) Hydroxyindole-O-methyltransferase (HIOMT) activity and the uptake of 3H-melatonin in the lamprey, Geotria australis Gray. Gen Comp Endocrinol 31:270–275

    Google Scholar 

  • Mason R, Brooks A (1988) The electrophysiological effects of melatonin and a putative melatonin antagonist (N-acetyl-tryptamine) on rat suprachiasmatic neurones in vitro. Neurosci Lett 95:296–301

    Google Scholar 

  • McNulty JA (1986) Uptake and mechanism of indole compounds by the goldfish pineal organ. Gen Comp Endocrinol 61:179–186

    Google Scholar 

  • Meissl H (1986) Photoneurophysiology of pinealocytes. In: O'Brien PJ, Klein DC (eds) Pineal and retinal relationships. Academic Press, New York, pp 33–45

    Google Scholar 

  • Meissl H, Dodt E (1981) Comparative physiology of pineal photo-receptors. In: Oksche A, Pevet P (eds) The pineal organ: photobiology-biochronometry-endocrinology. Elsevier, New York, 61–80

    Google Scholar 

  • Meissl H, Ekström P (1988 a) Photoreceptor responses to light in the isolated pineal organ of the trout, Salmo gairdneri. Neurosci 25:1071–1076

    Google Scholar 

  • Meissl H, Ekström P (1988 b) Dark and light adaptation of pineal photoreceptors. Vision Res 28:49–56

    Google Scholar 

  • Meissl H, Ekström P (1991) GABAergic modulation of the neural activity of ganglion cells in the photosensory pineal organ of the trout. In: Arendt J, Pevet P (eds), Advances in pineal research, vol. 5. J Libbeys, London (in press)

    Google Scholar 

  • Meissl H, Nakamura T, Thiele G (1986) Neural response mechanisms in the photoreceptive pineal organ of goldfish. Comp Biochem Physiol 84A:467–473

    Google Scholar 

  • Miller RF, Frumkes TE, Slaughter MM, Dacheux RF (1981) Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina. I. Receptors, horizontal cells, bipolars, and G-cells. J Neurophysiol 45:743–763

    Google Scholar 

  • Morita Y (1966) Entladungsmuster pinealer Neurone der Regen-bogenforelle (Salmo irideus) bei Belichtung des Zwischenhirns. Pflügers Arch 289:155–167

    Google Scholar 

  • Morita Y, Samejima M, Uchida K (1987) Pineal role in circadian locomotor rhythm and cellular basis of photic entrainment. In: Trentini GP, De Gaetani C, Pevet P (eds) Fundamentals and clinics in pineal research. Raven Press, New York, pp 161–164

    Google Scholar 

  • Nakamura T, Thiele G, Meissl H (1986) Intracellular responses from the photosensitive pineal organ of the teleost Phoxinus phoxinus. J Comp Physiol A 159:325–330

    Google Scholar 

  • Nicol RA (1978) Physiological studies on amino acids and peptides as prospective transmitters in the CNS. In: Lipton MA, DiMaschio A, Killam KF (eds) Psychopharmacology: a generation of progress. New York, Raven Press, pp 103–118

    Google Scholar 

  • Niles LP, Wong YW, Mishra RK, Brown GM (1979) Melatonin receptors in brain. Eur J Pharmacol 55:219–220

    Google Scholar 

  • Ogino N, Matsumura M, Shirakawa H, Tsukahara I (1983) Phagocytic activity of cultured retinal pigment epithelial cells from chick embryo: inhibition by melatonin and cyclic AMP, and its reversal by taurine and cyclic GMP. Ophthalmic Res 15:72–89

    Google Scholar 

  • Oksche A, Kirschstein H (1967) Die Ultrastruktur der Sinneszellen im Pinealorgan von Phoxinus laevis L. Z Zellforsch 78:151–166

    Google Scholar 

  • Pazo JH (1979) Effects of melatonin on spontaneous and evoked neuronal activity in the mesencephalic reticular formation. Brain Res Bull 4:725–730

    Google Scholar 

  • Pierce ME, Besharse JC (1985) Circadian regulation of retinomotor movements. I. Interaction of melatonin and dopamine in the control of cone length. J Gen Physiol 86:671–689

    Google Scholar 

  • Pu GA, Dowling JE (1981) Anatomical and physiological characteristics of pineal photoreceptor cell in the larval lamprey, Petromyzon marinus. J Neurophysiol 46:1018–1038

    Google Scholar 

  • Reiter RJ (1986) The pineal gland: an important link to the environment. News Physiol Sci 1:202–205

    Google Scholar 

  • Semm P, Vollrath L (1982) Alterations in the spontaneous activity of cells in the guinea pig pineal gland and visual system produced by pineal indoles. J Neural Transm 53:265–275

    Google Scholar 

  • Semm P, Vollrath L (1984) Electrical responses of homing pigeon and guinea pig Purkinje cells to pineal indoleamines applied by microiontophoresis. J Comp Physiol A 154:675–681

    Google Scholar 

  • Stehle J, Vaneček J, Vollrath L (1989) Effects of melatonin on spontaneous electrical activity of neurons in rat suprachiasmatic nuclei: an in vitro iontophoretic study. J Neural Transm 78:173–177

    Google Scholar 

  • Tabata M, Tamura T, Niwa H (1975) Origin of the slow potential in the pineal organ of the rainbow trout. Vision Res 15:737–740

    Google Scholar 

  • Underwood H (1989) The pineal and melatonin: Regulators of circadian function in lower vertebrates. Experientia 45:914–922

    Google Scholar 

  • Vacas MI, Cardinali DP (1980) Binding sites for melatonin in bovine pineal gland. Hormone Res 13:121–131

    Google Scholar 

  • Vollrath L (1981) The pineal organ. Handbuch der Mikroskopischen Anatomie des Menschen, Vol VI/7. Springer, Berlin

    Google Scholar 

  • Wiechmann AF, Bok D, Horwitz J (1985) Localization of hydroxy-indole-O-methyltransferase in the mammalian pineal gland and retina. Invest Ophthalmol Visual Sci 26:253–265

    Google Scholar 

  • Wiechmann AF, Bok D, Horiwtz J (1986) Melatonin binding in the frog retina: autoradiographic and biochemical analysis. Invest Ophthalmol Visual Sci 27:153–163

    Google Scholar 

  • Wiechmann AF, Yang XL, Wu SL, Hollyfield JG (1988) Melatonin enhances horizontal cell sensitivity in salamander retina. Brain Res 453:377–380

    Google Scholar 

  • Wu SM (1986) Effects of gamma-aminobutyric acid on cones and bipolar cells of the tiger salamander retina. Brain Res 365:70–77

    Google Scholar 

  • Zeise ML, Semm P (1985) Melatonin lowers excitability of guinea pig hippocampal neurons in vitro. J Comp Physiol A 157:23–29

    Google Scholar 

  • Zisapel N (1988) Melatonin receptors revisited. J Neural Transm 73:1–5

    Google Scholar 

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Author notes

  1. M. Tabata

    Present address: Max-Planck-Institut für Physiologische und Klinische Forschung, W.G. Kerckhoff-Institut, Parkstr. 1, W-6350, Bad Nauheim, Federal Republic of Germany

  2. C. Martin

    Present address: Laboratoire de Biologie Cellulaire, 40 Avenue du Recteur Pineau, F-86022, Poitiers, France

Authors and Affiliations

  1. Max-Planck-Institut für Physiologische und Klinische Forschung, W.G. Kerckhoff-Institut, Parkstr. 1, W-6350, Bad Nauheim, Federal Republic of Germany

    H. Meissl & C. Martin

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Laboratory of Fish Biology, School of Agriculture, Nagoya University, Chikusa, Nagoya 464 Japan

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Meissl, H., Martin, C. & Tabata, M. Melatonin modulates the neural activity in the photosensory pineal organ of the trout: Evidence for endocrine-neuronal interactions. J Comp Physiol A 167, 641–648 (1990). https://doi.org/10.1007/BF00192657

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