Summary
The central catecholamine innervation of the pituitary neural lobe and pars intermedia of the rat have been identified ultrastructurally and their organization has been investigated in a combined fluorescence histochemical and electron microscopical study. The dopamine analogues, 5-hydroxydopamine and 6-hydroxydopamine, were used to “label” the catecholamine terminals, and to enable the direct correlation between the fluorescence microscopical and the electron microscopical pictures.
The fibre type that was identified as catecholamine-containing was ultrastructurally chiefly characterized by dense-cored vesicles, 500–1200 Å in diameter, intermingled with varying numbers of small empty vesicles. 5-hydroxydopamine was selectively accumulated in these fibres and caused an increased electron density of the granular vesicles as well as of some small normally agranular vesicles, and systemically administered 6-hydroxydopamine caused a selective degeneration of these fibres, most prominently within the neural lobe. The dopaminergic terminals of the neural lobe showed frequent close contacts (80–120 Å), without real membrane thickenings, to neurosecretory axons and to pituicyte processes. It is suggested that these close contacts might signify a direct dopaminergic influence on the neurosecretory axons and/or on the pituicyte processes. The identified central catecholamine fibres were also found to make common synapse-like contacts on the pars intermedia cells, whereas the innervation by neurosecretory fibres was very rare. This suggests that the direct central nervous control of the rat pars intermedia is exerted by the catecholamine neurons. A very special feature of the catecholamine fibres in the pituitary is the occurrence of peculiar, large dopamine-filled droplet-like swellings. Electron microscopically, such large axonal swellings (more than 2 μ in diameter) were found to contain, in addition to the characteristic vesicles and organelles, strongly osmiophilic lamellated membrane complexes resembling myelin bodies and multivesicular bodies encircling disintegrated vesicles, suggesting that these “droplet fibres” represent dilated stumps of spontaneously degenerating dopaminergic axons. It is suggested that the dopaminergic neural lobe fibres are undergoing continuous reorganization through degeneration—regeneration cycles, a phenomenon previously suggested for the neurosecretory axons of the neural lobe.
Similar content being viewed by others
References
Aghajanian, G. K., Bloom, F.: Electron microscopic autoradiography of rat hypothalamus after intraventricular H3-norepinephrine. Science 153, 308–310 (1966).
Andén, N.-E., Dahlström, A., Fuxe, K., Larsson, K., Olson, L., Ungerstedt, U.: Ascending monoamine neurons to the telencephalon and diencephalon. Acta physiol. scand. 67, 313–326 (1966).
Bargmann, W., Lindner, E., Andres, K. H.: Über Synapsen an endokrinen Epithelzellen und die Definition sekretorischer Neurone. Untersuchungen am Zwischenlappen der Katzenhypophyse. Z. Zellforsch. 77, 282–298 (1967).
Baumgarten, H.-G., Braak, H., Wartenberg, H.: Demonstration of dense core vesicles by means of pyrogallol derivatives in noradrenaline containing neurones from the organon vasculosum hypothalami of Lacerta. Z. Zellforsch. 95, 396–404 (1969).
— Falck, B., Wartenberg, H.: Adrenergic neurones in the spinal cord of the pike (Esox lucius) and their relation to the caudal neurosecretory system. Z. Zellforsch. 107, 479–498 (1970a).
Baumgarten, H. G., Holstein, A. F., Owman, Ch.: Auerbach's plexus of mammals and man: Electron microscopic identification of three different types of neuronal processes in myenteric ganglia of the large intestine from rhesus monkeys, guinea-pigs and man. Z. Zellforsch. 106, 376–397 (1970b).
Belenky, M. A., Konstantinova, M. S., Polenov, A. L.: On neurosecretory and adrenergic fibers in the intermediate lobe of the hypophysis in albino mice. Gen. comp. Endocr. 15, 185–197 (1970).
Bertler, Å., Carlsson, A., Rosengren, E.: A method for the fluorimetric determinations of adrenaline and noradrenaline in tissues. Acta physiol. scand. 44, 273–292 (1958a).
— Waldeck, B.: A method for the fluorimetric determinations of adrenaline, norrenaline, and dopamine in tissues. Kungl. Fysiogr. Sällsk. Lund Förh. 28, 121–123 (1958b).
Björklund, A.: Monoamine-containing fibres in the neurointermediate lobe of the pig and rat. Z. Zellforsch. 89, 573–589 (1968).
— Ehinger, B., Falck, B.: A method for differentiating dopamine from noradrenaline in tissue sections by microspectrofluorometry. J. Histochem. Cytochem. 16, 262–270 (1968).
— Falck, B.: An improvement of the histochemical fluorescence method for monoamines. Observations on varying extractability of fluorophores in different nerve fibres. J. Histochem. Cytochem. 16, 717–720 (1968).
— Pituitary monoamines of the cat with special reference to the presence of an unidentified monoamine-like substance in the adenohypophysis Z. Zellforsch. 93, 254–264 (1969).
— Hromek, F., Owman, Ch., West, K. A.: Identification and terminal distribution of the tubero-hypophyseal monoamine fibre systems in the rat by means of stereotaxic and microspectrofluorimetric techniques. Brain Res. 17, 1–23 (1970).
Björklund, A., Falck, B., Owman, Ch.: Fluorescence microscopic and microspectrofluorometric techniques for the cellular localization and characterization of biogenic amines. In: Methods in investigative and diagnostic endocrinology (ed. I. Kopin). Amsterdam: North Holland Publ. (in press), (1972).
— Rosengren, E.: Monoamines in the pituitary gland of the pig. Life Sci. 6, 2103–2110 (1967).
— Stenevi, U.: Classification of monoamine neurones in the rat mesencephalon: Distribution of a new monoamine neurone system. Brain Res. 32, 269–285 (1971).
Bloom, F. E., Algeri, S., Groppetti, A., Revuelta, A., Costa, E.: Lesions of central norepinephrine terminals with 6-OH-dopamine: Biochemistry and fine structure. Science 166, 1284–1286 (1969).
Breese, G. R., Traylor, T. D.: Effect of 6-hydroxydopamine on brain norepinephrine and dopamine: Evidence for selective degeneration of catecholamine neurons. J. Pharmacol. exp. Ther. 174, 413–420 (1970).
Cameron, E., Foster, C. L.: Some light- and electron microscopical observations on the pars intermedia of the pituitary gland of the rabbit. J. Endocr. 49, 479–485 (1971).
Cannata, M. A., Tramezzani, J. H.: The neural lobe of the neurohypophysis of the rat: Several types of nerve endings. Experientia (Basel) 25, 1281–1282 (1969).
— Neurohypophysis of the Wedell seal: an electron microscopic study. J. Anat. (Lond.) 108, 185–195 (1971).
Champlain, J. de: Degeneration and regrowth of adrenergic nerve fibers in the rat peripheral tissues after 6-hydroxydopamine. Canad. J. Phys. Pharm. 49, 345–360 (1971).
Dahlström, A.: The effects of drugs on axonal transport of amine storage granules. In: New aspects of storage and release mechanisms of catecholamines (ed. H. J. Schumann, G. Kronberg), p. 20–36. Berlin-Heidelberg-New York: Springer 1970.
— Fuxe, K.: Monoamines and the pituitary gland. Acta endocr. 51, 301–314 (1966).
— Häggendal, J.: Axonal transport of amine storage granules in sympathetic adrenergic neurons. In: Biochemistry of simple neuronal models (eds. E. Costa and E. Giacobini), p. 65–93. New York: Raven Press 1970.
Daniel, A. R., Lederis, K.: Effects of ether anesthesia and haemorrhage on hormone storage and ultrastructure of the rat neurohypophysis. J. Endocr. 34, 91–104 (1966).
Da Prada, M., Pletscher, A.: Isolated 5-hydroxytryptamine organelles of rabbit blood platelets: Physiological properties and drug-induced changes. Brit. J. Pharmacol. 34, 591–597 (1968).
Dellmann, H.-D., Rodríguez, E. M.: Herring bodies; an electron microscopic study of local degeneration and regeneration of neurosecretory axons. Z. Zellforsch. 111, 293–315 (1970).
Ehinger, B., Falck, B.: Fluorescence microscopical demonstration of 5-hydroxydopamine in adrenergic nerves. Histochemie 18, 1–7 (1969).
Enemar, A., Falck, B.: On the presence of adrenergic nerves in the Pars intermedia of the frog, Rana temporaria. Gen. comp. Endocr. 5, 577–583 (1965).
Falck, B., Owman, Ch.: A detailed methodological description of the fluorescence methods for the cellular demonstration of biogenic monoamines. Acta Univ. Lund II, 7, 1–23 (1965).
Green, J. D.: Microanatomical aspects of the formation of neurohypophysial hormones and neurosecretion. In: The pituitary gland (eds. G. W. Harris and B. T. Donovan), vol. 3, p. 240–268. Berkeley-Los Angeles: University of California Press 1966.
Hamberger, B.: Reserpine-resistent uptake of catecholamines in isolated tissues of the rat. M. D. Thesis, Stockholm 1967.
Hartmann, J. F.: Electron microscopy of the neurohypophysis in normal and histamine treated rats. Z. Zellforsch. 48, 291–308 (1958).
Hökfelt, T.: In vitro studies on central and peripheral monoamine neurons at the ultrastructural level. Z. Zellforsch. 91, 1–74 (1968).
Howe, A., Maxwell, D. S.: Electron microscopy of the pars intermedia of the pituitary gland in the rat. Gen. comp. Endocr. 11, 169–185 (1968).
Iturriza, F. C.: The secretion of intermedin in autotransplants of pars intermedia growing in the anterior chamber of intact and sympathectomized eyes of the toad. Neuroendocrinology 2, 11–18 (1967).
Iturriza, F. C.: Further evidence for the blocking effect of catecholamines on the secretion of melanocyte-stimulating hormone in toads. Gen. comp. Endocr. 12, 417–426 (1969).
Kapeller, K., Mayor, D.: Accumulation of noradrenaline in constricted sympathetic nerves as studied by fluorescence and electron microscopy. Proc. roy. Soc. B 167, 282–292 (1967).
Knowles, F., Vollrath, L.: A functional relationship between neurosecretory fibres and pituicytes in the eel. Nature (Lond.) 208, 1343 (1965).
— Neurosecretory innervation of the pituitary of the eels Anguilla and Conger. Phil. Trans. Roy. Soc. B 250, 311–342 (1966).
Kobayashi, Y., Hirano, T., Oota, Y.: Electron microscopic and pharmacological studies on the median eminence and pars nervosa. Arch. Anat. micr. Morph. exp. 54, 277–294 (1965).
Kurosumi, K., Matsuzawa, T., Shibasaki, S.: Electron microscope studies on the fine structures of the pars nervosa and pars intermedia, and their morphological interrelation in the normal rat hypophysis. Gen. comp. Endocr. 1, 433–452 (1961).
Lederis, K.: An electron microscopical study of the human neurohypophysis. Z. Zellforsch. 65, 847–868 (1965).
Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).
Monroe, B. G.: A comparative study of the ultrastructure of the median eminence, infundibular stem and neural lobe of the hypophysis of the rat. Z. Zellforsch. 76, 405–432 (1967).
Nakai, Y.: Electron microscopic observations on synapse-like contacts between pituicytes and different types of nerve fibers in the anuran pars nervosa. Z. Zellforsch. 110, 27–39 (1970).
Palay, S. L.: The fine structure of the neurohypophysis. In: Ultrastructure and cellular chemistry of neural tissue (ed. H. Waelsch), p. 31–49. New York: Harper (Hoeber) 1957.
Piezzi, R. S., Larin, F., Wurtman, R. J.: Serotonin, 5-hydroxyindoleacetic acid (5-HIAA), and monoamine oxidase in bovine median eminence and pituitary gland. Endocrinology 86, 1460–1462 (1970).
Reynolds, E. S.: The use of lead citrat at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 210–213 (1963).
Richards, J. G., Tranzer, J. P.: The ultrastructural localization of amine storage sites in the central nervous system with the aid of a specific marker, 5-hydroxydopamine. Brain Res. 17, 463–469 (1970).
Smoller, C. G.: Ultrastructural studies on the developing neurophysis of the pacific tree-frog, Hyla regilla. Gen. comp. Endocr. 7, 44–73 (1966).
Thoenen, H., Tranzer, J. P.: Chemical sympathectomy by selective destruction of adrenergic nerve endings with 6-hydroxydopamine. Naunyn-Schmiedebergs Arch. Pharmak. exp. Path. 261, 271–288 (1968).
Tranzer, J. P., Thoenen, H.: Ultramorphologische Veränderungen der sympathischen Nervenendigungen der Katze nach Vorbehandlung mit 5- und 6-Hydroxy-Dopamin. Naunyn-Schmiedebergs Arch. Pharmak. exp. Path. 257, 343–344 (1967a).
— Electronmicroscopic localization of 5-hydroxydopamine (3, 4, 5-trihydroxy-phenylethylamine), a new “false” sympathetic transmitter. Experientia (Basel) 23, 743–745 (1967b).
— An electron microscopic study of selective, acute degeneration of sympathetic nerve terminals after administration of 6-hydroxydopamine. Experientia (Basel) 24, 155–156 (1968).
— Snipes, R. L., Richards, J. G.: Recent development on the ultrastructural aspect of adrenergic nerve endings in various experimental conditions. In: Mechanisms of synaptic transmission (eds. K. Akert and P. G. Waser). Progr. Brain Res. 31, 33–46 (1969).
Ungerstedt, U.: 6-Hydroxydopamine induced degeneration of central monoamine neurons. Europ. J. Pharmacol. 5, 107–110 (1968).
— Histochemical studies on the effects of intracerebral and intraventricular injections of 6-hydroxydopamine on monoamine neurons in the rat brain. In: 6-Hydroxydopamine and catecholamine neurons (eds. T. Malmfors and H. Thoenen), p. 101–127. North-Holland Amsterdam-London 1971.
Uretsky, N. J., Iversen, I. L.: Effects of 6-hydroxydopamine on catecholamine containing neurones in the brain. J. Neurochem. 17, 269–278 (1970).
Vincent, D. S., Anand Kumar, T. C.: Electron microscopic study on the pars intermedia of the ferret. Z. Zellforsch. 99, 185–197 (1969).
Wittkowski, W.: Kapillaren und perikapilläre Räume im Hypothalamo-Hypophysen-System und ihre Beziehungen zum Nervengewebe. Z. Zellforsch. 81, 344–360 (1967).
— Nervenfasern mit ultrastrukturell verschiedenen Elementargranula im Hypophysenhinterlappen des Rhesusaffen. Z. Zellforsch. 107, 499–507 (1970).
Ziegler, B.: Licht- und elektronenmikroskopische Untersuchungen an Pars intermedia und Neurohypophyse der Ratte. Z. Zellforsch. 59, 486–506 (1963).
Author information
Authors and Affiliations
Additional information
Supported by the Deutsche Forschungsgemeinschaft.
Supported by Svenska Livförsäkringsbolags Nämnd för Medicinsk Forskning, by The Medical Faculty, University of Lund and by the Ford Foundation.
Rights and permissions
About this article
Cite this article
Baumgarten, H.G., Björklund, A., Holstein, A.F. et al. Organization and ultrastructural identification of the catecholamine nerve terminals in the neural lobe and pars intermedia of the rat pituitary. Z.Zellforsch 126, 483–517 (1972). https://doi.org/10.1007/BF00306908
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00306908