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The nucleus lateralis tuberis system of the gobiid fish Gillichthys mirabilis

II. Innervation of the pituitary

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Summary

The innervation of the pituitary gland of the teleost fish Gillichthys mirabilis was studied with light and electron microscopy in order to determine its nature and distribution. Two types of neurosecretory fibers (“A” and “B”) are present in the adenohypophysis. Type “A” fibers containing elementary neurosecretory granules, 1,500–1,600 Å in diameter, perforate the basement membrane in the neurointermediate lobe and make synaptoid contacts with MSH cells. Type “B” fibers containing large granulated vesicles (LGV), 900–1,000 Å in diameter, perforate the basement membrane in all lobes of the pituitary gland and terminate in direct contact with the several adenohypophysial cell types. At the electron-microscope level, LGV from type “B” fibers show a positive reaction to zinc iodide-osmium tetroxide (ZIO) impregnation. Reserpine treatment resulted in a depletion of their dense cores if osmium tetroxide was used as the only fixative, whereas double fixation with aldehydes and osmium tetroxide did not reveal appreciable changes. Yellow-to-green fluorescent fibers were detected in the pituitary gland after the Falck-Hillarp technique at sites corresponding approximately to the location of type “B” fibers, strongly suggesting the monoaminergic nature of the latter. After hypophysectomy, medial and lateral neurons of the nucleus lateralis tuberis (NLT) undergo retrograde degeneration. This finding, together with the morphological and cytochemical similarities of the LGV in NLT neurons and those in the type “B” fibers, suggests that the fibers originate from certain NLT neurosecretory neurons.

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References

  • Bargmann, W.: Zwischenhirn-Hypophysensystem von Fischen. Z. Zellforsch. 38, 275–298 (1953).

    Google Scholar 

  • —: Das neurosekretorische Zwischenhirn-Hypophysensystem und seine synaptischen Verknüpfungen. J. Neuro-Viscer. Relat., Suppl. 9, 64–77 (1969).

    Google Scholar 

  • —, Knoop, A.: Über die morphologischen Beziehungen des neurosekretorischen Zwischenhirnsystems zum Zwischenlappen der Hypophyse (Licht- und elektronenmikroskopische Untersuchungen). Z. Zellforsch. 52, 256–277 (1960).

    Google Scholar 

  • Billenstien, D. C.: Neurosecretory material from the nucleus lateralis tuberis in the hypophysis of the Eastern trout Salvelinus fontinalis. Z. Zellforsch. 59, 507–512 (1963).

    Google Scholar 

  • Bloom, F. E., Aghajanian, G. K.: Fine structure and cytochemical analysis of the staining of synaptic junctions with phosphotungstic acid. J. Ultrastruct. Res. 22, 361–375 (1968).

    Google Scholar 

  • Charlton, H. H.: Comparative studies on the nucleus preopticus pars magnocellularis and the nucleus lateralis in fishes. J. comp. Neurol. 54, 237–275 (1932).

    Google Scholar 

  • Chen, I. L., Yates, R. D., Duncan, D.: The effects of reserpine and hypoxia on the aminestoring granules of the hamster carotid body. J. Cell Biol. 42, 804–816 (1969).

    Google Scholar 

  • Corrodi, H., Hillarp, N.-Å., Jonsson, G.: Fluorescence methods for the histochemical demonstration of monoamines. 3. Sodium borohydride reduction of the fluorescent compounds as a specific test. J. Histochem. Cytochem. 12, 582–586 (1964).

    Google Scholar 

  • Dahlström, A., Fuxe, K.: Monoamines and the pituitary gland. Acta endocr. (Kbh.) 51, 301–314 (1966).

    Google Scholar 

  • Dharmamba, M., Nishioka, R. S.: Response of “prolactin secreting” cells of Tilapia mossambica to environmental salinity. Gen. comp. Endocr. 10, 409–420 (1968).

    Google Scholar 

  • Diepen, R.: Über das Hypophysen-Hypothalamussystem bei Knochenfischen. Anat. Anz. 110, 111–122 (1954).

    Google Scholar 

  • Duncan, D., Yates, R. D.: Ultrastructure of the carotid body of the cat as revealed by various fixatives and the use of reserpine. Anat. Rec. 157, 667–682 (1967).

    Google Scholar 

  • Falck, B.: Observations on the possibilities of the cellular localization of monoamines by fluorescent method. Acta physiol. scand. 56, Suppl. 197, 1–25 (1962).

    Google Scholar 

  • Follenius, E.: Bases structurales et ultrastructurales des corrélations hypothalamo-hypophysaires chez quelques espèces de Poissons Téléostéens. Ann. Sci. Nat. Zool. 7, 1–150 (1965a).

    Google Scholar 

  • —: Bases structurales et ultrastructurales des corrélations diencéphalo-hypophysaires chez les Sélaciens et les Téléostéens. Arch. Anat. micr. Morph. exp. 54, 195–216 (1965b).

    Google Scholar 

  • —: Innervation adrénergique de la méta-adénohypophyse de l'Epinoche (Gasterosteus aculeatus L.). Mise en évidence par radioautographie au microscope électronique. C. R. Acad. Sci. (Paris) 267, 1208–1211 (1968).

    Google Scholar 

  • Golding, D. W., Baskin, D. G., Bern, H. A.: The infracerebral gland —A possible neuroendocrine complex in Nereis. J. Morph. 124, 187–216 (1968).

    Google Scholar 

  • Hayashida, T., Lagios, M. D.: Fish growth hormone: biological, immunochemical and ultrastructural study of sturgeon and paddlefish pituitaries. Gen. comp. Endocr. 13, 403–411 (1969).

    Google Scholar 

  • Honma, S., Honma, Y.: Histochemical demonstration of monoamines in the hypothalamus of the lampreys and ice-goby. Bull. Japan Soc. Sci. Fisheries 36, 125–134 (1970).

    Google Scholar 

  • Ishii, S.: Association of luteinizing hormone-releasing factor with granules separated from equine hypophyseal stalk. Endocrinology 86, 207–216 (1970).

    Google Scholar 

  • Iturriza, F. C.: Electron microscopic studies of the pars intermedia of the pituitary of the toad, Bufo arenarum. Gen. comp. Endocr. 4, 492–502 (1964).

    Google Scholar 

  • Jaim-Etcheverry, G., Zieher, L. M.: Electron microscopy cytochemistry of 5-hydroxytryptamine (5-HT) in the beta cells of guinea pig endocrine pancreas. Endocrinology 83, 917–923 (1968a)

    Google Scholar 

  • Jaim-Etcheverry, G., Zieher, L. M.: Cytochemical localization of monoamine stores in sheep thyroid gland at the electron microscopic level. Experientia (Basel) 24, 593–595 (1968b).

    Google Scholar 

  • —: Cytochemistry of 5-hydroxytryptamine at the electron microscope level. II. Localization in the autonomic nerves of the rat pineal gland. Z. Zellforsch. 86, 393–400 (1968c).

    Google Scholar 

  • Jørgensen, C. G., Rosenkilde, P., Wingstrand, K. G.: Regeneration of the neural lobe of the pituitary gland of the toad, Bufo bufo (L.). In: Bertil Hanström—Zoological papers in honor of his 65th birthday (K. G. Wingstrand, ed.), p. 184–195. Zoological Institute, Lund, Sweden (1956).

    Google Scholar 

  • Kamberi, I. A., McCann, S. M.: Effect of biogenic amines, FSH-releasing factor (FRF) and other substances on the release of FSH by pituitaries incubated in vitro. Endocrinology 85, 815–824 (1969).

    Google Scholar 

  • Karnovsky, M. J.: A formaldehyde-glutaraldehyde fixative for use in electron microscopy. J. Cell Biol. 27, 137 A (1965).

    Google Scholar 

  • Knowles, F. G. W.: Evidence for a dual control, by neurosecretion, of hormone synthesis and release in the pituitary of the dogfish, Scylliorhinus stellaris. Phil. Trans. B 249, 435–456 (1965).

    Google Scholar 

  • —, Bern, H. A.: The function of neurosecretion in endocrine regulation. Nature (Lond.) 210, 271–272 (1966).

    Google Scholar 

  • —, Vollrath, L.: Neurosecretory innervations of the pituitary of the eels Anguilla and Conger. I. The structure and ultrastructure of the neurointermediate lobe under normal and experimental conditions. Phil. Trans. B 250, 311–327 (1966a).

    Google Scholar 

  • —: Neurosecretory innervations of the pituitary of the eels Anguilla and Conger. II. The structure and innervation of the pars distalis at different stages of the life cycle. Phil. Trans. B 250, 329–342 (1966b).

    Google Scholar 

  • —, Nishioka, R. S.: Dual neurosecretory innervation of the adenohypophysis of Hippocampus, the sea horse. Nature (Lond.) 214, 309 (1967).

    Google Scholar 

  • Kobayashi, H., Ishii, S., Gorbman, A.: The hypothalamic neurosecretory apparatus and the pituitary gland of a teleost, Lepidogobius lepidus. Gunma J. med. Sci. 8, 301–321 (1959).

    Google Scholar 

  • Lagios, M. D.: Tetrapod-like organization of the pituitary gland of the polypteriformid fishes, Calamoichthys calabaricus and Polypterus palmas. Gen. comp. Endocr. 11, 300–315 (1968).

    Google Scholar 

  • - The median eminence of the bowfin, Amia calva. Gen. comp. Endocr. (in press) (1970).

  • Legg, P. G.: The fine structure and innervation of the beta and delta cells in the islet of Langerhans of the cat. Z. Zellforsch. 80, 307–321 (1967).

    Google Scholar 

  • Murakami, M., Nakayama, Y., Hashimoto, J.: Elektronenmikroskopische Untersuchungen über das Verhalten des supraoptico-hypophysären Systems in der hypophysektomierten Ratte. Endokrinologie 54, 300–315 (1969).

    Google Scholar 

  • Nakai, Y., Gorbman, A.: Evidence for a double innervated secretory unit in the anuran pars intermedia. II. Electron microscopic studies. Gen. comp. Endocr. 13, 108–116 (1969).

    Google Scholar 

  • Nishioka, R. S., Bern, H. A.: Ultrastructural study of the innervation of the pituitary of the teleost Tilapia mossambica. Amer. Zoologist 7, 714 (1967).

    Google Scholar 

  • —, Golding, D. W.: Innervation of the cephalopod optic gland. In: Neuroendocrinology (W. Bargmann and B. Scharrer, eds.). München: Bergmann 1970 (in press).

    Google Scholar 

  • Normann, T. C.: The neurosecretory system of the adult Calliphora erythrocephala. I. The fine structure of the corpus cardiacum with some observations on adjacent organs. Z. Zellforsch. 67, 461–501 (1965).

    Google Scholar 

  • Oshima, K., Gorbman, A.: Evidence for a doubly innervated secretory unit in the anuran pars intermedia. I. Electrophysiologic studies. Gen. comp. Endocr. 13, 98–107 (1969).

    Google Scholar 

  • Pellegrino de Iraldi, A., De Robertis, E.: Action of reserpine on submieroscopic morphology of the pineal gland. Experientia (Basel) 17, 122–123 (1961).

    Google Scholar 

  • —, Guedet, R.: Action of reserpine on the osmium tetroxide zinc iodide reactive site of synaptic vesicles in the pineal gland. Z. Zellforsch. 91, 178–185 (1968).

    Google Scholar 

  • Robertson, D. R.: The ultimobranchial body in Rana pipiens. III. Sympathetic innervation of the secretory parenchyma. Z. Zellforsch. 78, 328–340 (1967).

    Google Scholar 

  • Rodríguez, E. M.: Fixation of the central nervous system by perfusion of the cerebral ventricles with a threefold aldehyde mixture. Brain Res. 15, 395–412 (1969).

    Google Scholar 

  • Samuelsson, B., Fernholm, B., Fridberg, G.: Light microscopic studies on the nucleus lateralis tuberis and the pituitary of the roach, Leuciscus rutilis, with reference to the nucleuspituitary relationship. Acta zool. 49, 141–153 (1968).

    Google Scholar 

  • Sathyanesan, A. G.: The reorganization of the hypophysial stalk following hypophysectomy in the teleost Porichthys notatus Girard. Z. Zellforsch. 67, 734–739 (1965).

    Google Scholar 

  • Scharrer, B.: Histophysiological studies on the corpus allatum of Leucophaea moderae. IV. Ultrastructure during normal activity. Z. Zellforsch. 62, 125–148 (1964).

    Google Scholar 

  • Schneider, H. P. G., McCann, S. M.: Possible role of dopamine as transmitter to promote discharge of LH-releasing factor. Endocrinology 85, 121–132 (1969).

    Google Scholar 

  • Stutinsky, F.: La neurosécrétion chez l'Anguille normale et hypophysectomisée. Z. Zellforsch. 39, 276–297 (1953).

    Google Scholar 

  • Urano, A.: Distribution of monoamine oxidase in the hypothalamo-hypophysial region of the teleosts, Anguilla japonica and Oryzias latipes. Z. Zellforsch. (in press) (1970).

  • Vollrath, L.: Über die neurosekretorische Innervation der Adenohypophyse von Teleostiern, insbesondere von Hippocampus cuda und Tinca tinca. Z. Zellforsch. 78, 234–260 (1967).

    Google Scholar 

  • Wingstrand, K. G.: Attempts at a comparison between the neurohypophysial region in fishes and tetrapods, with particular regard to amphibians. In: Comparative endocrinology (A. Gorbman, ed.), p. 393–403. New York: Wiley 1959.

    Google Scholar 

  • Zambrano, D.: The nucleus lateralis tuberis (NLT) system of the gobiid fish Gillichthys mirabilis. I. Ultrastructural and histochemical characterization of the nucleus. Z. Zellforsch. 110, 9–26 (1970a).

    Google Scholar 

  • - The nucleus lateralis tuberis (NLT) system of the gobiid fish Gillichthys mirabilis. III. Functional modifications (in preparation) (1970b).

  • - Nishioka, R. S., Bern, H. A.: Comparison of the innervation of the pituitary of two teleost euryhaline fishes, Gillichthys mirabilis and Tilapia mossambica, with special reference to the origin and nature of type “B” fibers. Mem. Soc. Endocrinol. v. 19 (in press) (1970).

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Authors and Affiliations

  1. Department of Zoology and its Cancer Research Genetics Laboratory, University of California, 94720, Berkeley, USA

    David Zambrano

  2. Facultad de Medicina Paraguay 2155, 2∘ Piso, Instituto de Anatomía Generaly Embriología, Buenos Aires, Argentina

    David Zambrano

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  1. David Zambrano
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Associated Investigator, Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina. Recipient of National Institutes of Health International Fellowship 1-F05-TW1330.—I am indebted to Professor Howard A. Bern and Mr. Richard S. Nishioka for their valuable advice and critical reading of the manuscript. Thanks are also due Mr. W. Craig Clarke who performed the hypophysectomies, Mrs. Emily Reid who prepared the graphs and Mr. John Underhill who did the photographic work. This study was aided by NSF grant GB 6424 to Professor Bern.

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Zambrano, D. The nucleus lateralis tuberis system of the gobiid fish Gillichthys mirabilis . Z. Zellforsch. 110, 496–516 (1970). https://doi.org/10.1007/BF00330101

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