Skip to main content
Log in

Innervation of the male genital tract and kidney in the amphibia, Xenopus laevis daudin, Rana temporaria L., and Bufo bufo L.

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The innervation of the male genital tract and kidney in three anuran species was studied by the fluorescence histochemical method of Falck-Hillarp for the demonstration of monoamines whose identity was secured by thin-layer chromatography, and by electron microscopy including administration of 5- or 6-hydroxydopamine (5- and 6-OHDA). The genital tract comprises testis, intra- and extratesticular and intrarenal seminal efferent ducts, Bidder's canal, renal dorsal transverse ducts, and ureter. In addition-depending on the species studied-renal corpuscles and the various portions of uriniferous tubules may be involved in sperm transport.

  1. 1.

    Adrenaline is the main transmitter in nerves supplying the male genital tract and kidney. Only in Xenopus is it possible to demonstrate the presence of noradrenaline, which was confirmed in the Chromatographic analysis. No obvious changes are observed with regard to the distribution, amount, and fluorescence intensity of adrenergic fibers and their susceptibility towards 5- and 6-OHDA when comparing animals killed in late autumn and winter, or in late spring, respectively. Non-adrenergic nerve fibers have not been observed.

  2. 2.

    The adrenergic innervation in the testis is only scarce and confined to blood vessels. Neuro-endocrine contacts on Leydig cells are not established. The gonadal ducts and the specific (i.e. non-vascular) intratesticular smooth muscle cells in Xenopus are not innervated.

  3. 3.

    Apart from the uriniferous tubules (see below), only the ureter receives an adrenergic innervation which, however, is scarce even around the time of spermiation. Bundles of nonterminal and terminal axons are seen running contiguous to the superficial bundles of smooth muscle or smooth muscle-like cells. Neuromuscular relationships comprise synapses at distances of 2000–5000 Å, but no close contacts. In the seminal vesicle of Rana the same mode of apposition of adrenergic terminals to muscle cells is observed. In addition, a direct innervation of the epithelium is seen in a few instances.

  4. 4.

    In the kidney the renal arteries, afferent arterioles, and the main branches of the portal veins are supplied by a dense plexus of adrenergic nerves. Small groups of intensely fluorescent cells are found in the walls of the renal portal veins and veins proper. The density of the arteriolar plexus is more pronounced in Rana and Bufo than in Xenopus. In Rana and Bufo the arteriolar innervation comprises terminals at “ordinary” smooth musculature with membrane-to-membrane appositions, as well as contacts at a distance of 800 to 4000n Å on juxtaglomerular epitheloid cells. In Xenopus the latter have not been identified with certainty. Adrenergic nerves, running dorsal to the row of glomeruli and ventral to the muscular branches of the portal vein, may reflect a tubular innervation because, in that region, muscular vessels do not exist. Terminals partly or completely devoid of the Schwann cell sheath approach the tubular basal lamina with a distance down to 200 Å. An innervation related to a particular portion of the nephron is not observed; however, the connecting tubules and dorsal transverse ducts are also supplied by adrenergic nerve terminals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Angelakos, E. T., Glassman, P. M., Millard, R. W., King, M.: Regional distribution and subcellular localization of catecholamines in the frog heart. Comp. Biochem. Physiol. 15, 313–324 (1965)

    Google Scholar 

  • Axelsson, S., Björklund, A., Falck, B., Lindvall, O., Svensson, L.-Å.: Glyoxylic acid condensation: A new fluorescence method for the histochemical demonstration of biogenic monoamines. Acta physiol. scand. 87, 57–62 (1973)

    Google Scholar 

  • Axelsson, S., Björklund, A., Sciler, N.: Identification of the para-isomer of tyramine in rat brain. Life Sci. 13, 1411–1419 (1973)

    Google Scholar 

  • Azuma, T., Binia, A., Visscher, M. B.: Adrenergic mechanisms in the bull-frog and turtle. Amer. J. Physiol. 209, 1287–1294 (1965)

    Google Scholar 

  • Barajas, L.: The innervation of the juxtaglomerular apparatus: An electron microscopic study of the glomerular arterioles. Lab. Invest. 13, 916–929(1964)

    Google Scholar 

  • Barajas, L., Müller, J.: The innervation of the juxtaglomerular apparatus and surrounding tubules: A quantitative analysis by serial section electron microscopy. J. Ultrastruct. Res. 43, 107–132 (1973)

    Google Scholar 

  • Bargmann, W., Knoop, A., Schiebler, T. H.: Histologische, zytochemische und elektronenmikroskopische Untersuchungen am Nephron (mit Berücksichtigung der Mitochondrien). Z. Zellforsch. 42, 386–422 (1955)

    Google Scholar 

  • Bargmann, W., Welsch, U.: Über Kanälchenzellen und dunkle Zellen im Nephron von Anuren. Z. Zellforsch. 134, 193–204 (1972)

    Google Scholar 

  • Baumgarten, H. G., Falck, B., Holstein, A.-F., Owman, Ch., Owman, T.: Adrenergic innervation of the human testis, epididymis, ductus deferens, and prostate: A fluorescence microscopic and fluorimetric study. Z. Zellforsch. 90, 81–95 (1968)

    Google Scholar 

  • Baumgarten, H. G., Holstein, A. F.: Catecholaminhaltige Nervenfasern im Hoden des Menschen. Z. Zellforsch. 79, 389–395 (1967)

    Google Scholar 

  • Baumgarten, H. G., Holstein, A. F.: Adrenerge Innervation im Hoden und Nebenhoden vom Schwan (Cygnus olor). Z. Zellforsch. 91, 402–410 (1968)

    Google Scholar 

  • Baumgarten, H. G., Holstein, A. F.: Noradrenerge Nervenfasern im Hoden von Mammalian und anderen Vertebraten. J. neurovisc. Rel., Suppl. 10, 563–572 (1971)

    Google Scholar 

  • Baumgarten, H. G., Holstein, A. F., Rosengren, E.: Arrangement, ultrastructure, and adrenergic innervation of smooth musculature of the ductuli efferentes, ductus epididymidis and ductus deferens of man. Z. Zellforsch. 120, 37–79 (1971)

    Google Scholar 

  • Bell, Ch.: An electrophysiological study of the effects of atropine and physostygmine on transmission to the guinea-pig vas deferens. J. Physiol. (Lond.) 189, 31–42 (1967)

    Google Scholar 

  • Bellocci, M., Picardi, R., de Martino, C.: The juxtaglomerular apparatus in the mesonephros of newt (Triturus cristatus). A morphology study. Z. Zellforsch. 144, 203–219 (1971)

    Google Scholar 

  • Belt, W. D., Cavazos, L. F.: Personal communication. Quoted after Hudson, N.: The nerves of the testis, epididymis and scrotum. In: The testis (ed. by A. D. Johnson, W. R. Gomes, and N. L. Vandemark), vol. I, p. 47–99. New York and London: Academic Press 1970

    Google Scholar 

  • Bennet, T., Burnstock, G., Cobb, J. L. S., Malmfors, T.: An ultrastructural and histochemical study of the short term effects of 6-hydroxydopamine on adrenergic nerves in the domestic fowl. Brit. J. Pharmacol. 38, 802–809 (1970)

    Google Scholar 

  • Björklund, A., Falck, B., Owman, Ch.: Fluorescence microscopic and microspectrofluorometric techniques for the cellular localization and characterization of biogenic amines. In: S. A. Berson (ed.), Methods of investigative and diagnostic endocrinology, vol.1: J. E. Rall and I. J. Kopin (eds.), The thyroid and biogenic amines, p. 318–368. Amsterdam: North-Holland Publ. Co. 1972

    Google Scholar 

  • Björklund, A., Lindvall, O., Svensson, L.-Å.: Mechanisms of fluorophore formation in the histochemical glyoxylic acid method for monoamines. Histochemie 32, 113–131 (1972)

    Google Scholar 

  • Brodie, B. B., Bogdanski, D. F., Bonomi, L.: Formation, storage and metabolism of serotonin (5-hydroxytryptamine) and catecholamines in lower vertebrates. In: Comparative neurochemistry, p. 367–377, ed. by D. Richter. Oxford: Pergamon Press 1964

    Google Scholar 

  • Burgers, A. C. J., Boschman, T. A. C., van de Kamer, J. C.: Excitement darkening and the effect of adrenaline on the melanophores of Xenopus laevis. Acta endocr. (Kbh.) 14, 72–82 (1953)

    Google Scholar 

  • Burnstock, G.: Evolution of the autonomic innervation of visceral and cardiovascular system in vertebrates. Pharmacol. Rev. 21, 247–324 (1969)

    Google Scholar 

  • Burnstock, G.: Structure of smooth muscle and its innervation. In: Smooth Muscle, ed. by E. Bülbring, A. F. Bradin, A. W. Jones, and T. Tomita. London: Edward Arnold (Publisher) Ltd. 1970

    Google Scholar 

  • Burnstock, G.: Purinergic nerves. Pharmacol. Rev. 24, 509–581 (1972)

    Google Scholar 

  • Burnstock, G., Robinson, P. M.: Localization of catecholamines and acetyl cholinesterase in autonomic nerves. Circulat. Res. 21, Suppl. 3, 43–55 (1967)

    Google Scholar 

  • Chiba, T.: Electron microscopic and histochemical studies on the synaptic vesicles in mouse vas deferens and atrium after 5-hydroxydopamine administration. Anat. Rec. 176, 35–48 (1973)

    Google Scholar 

  • Dayan, A. D.: Variation between species in the innervation of intratesticular blood vessels. Experientia (Basel) 26, 1359–1360 (1970)

    Google Scholar 

  • Disselhorst, R.: Der Harnleiter der Wirbeltiere. Anatomische Hefte (Merkel and Bonnet), vol. 4, 1894. Quoted after Gaupp (1904)

  • Dixon, J. S., Goslin, J. A.: Histochemical and electron microscopic observations on the innervation of the upper segment of the mammalian ureter. J. Anat. (Lond.) 110, 57–66 (1971)

    Google Scholar 

  • Doležel, S.: Histochemische Untersuchung der Niereninnervation mittels der Reaktion auf Cholinesterasen. Z. mikr.-anat. Forsch. 63, 599–608 (1958)

    Google Scholar 

  • Doležel, S.: Monoaminergic innervation of the arteries and veins of the kidney observed using fluorescence reaction. Folia morph. (Praha) 14, 168–174 (1966)

    Google Scholar 

  • Donoso, A. O., Segura, E. T.: Seasonal variations of plasma adrenaline and noradrenaline in toads. Gen. comp. Endocr. 5, 440–443 (1965)

    Google Scholar 

  • Dongen, W. J. van, Heijden, C. A. van der: The demonstration of renal juxtaglomerular granules and the evolution of the index of granulation in the toad, Bufo bufo. Z. Zellforsch. 94, 40–45 (1969)

    Google Scholar 

  • Ehinger, B., Falck, B., Sporrong, B.: Possible axo-axonal synapses between peripheral adrenergic and cholinergic nerve terminals. Z. Zellforsch. 107, 508–521 (1970)

    Google Scholar 

  • El-Badawi, A., Schenk, E. A.: The distribution of cholinergic and adrenergic nerves in the mammalian epididymis. A comparative histochemical study. Amer. J. Anat. 121, 1–14 (1967)

    Google Scholar 

  • Euler, U. S. von: Noradrenaline. Springfield, Illinois: Ch. C. Thomas 1956

    Google Scholar 

  • Falck, B., Hillarp, N.-Å., Thieme, G., Torp, A.: Fluorescence of catecholamines and related compounds condensed with formaldehyde. J. Histochem. Cytochem. 10, 348–354 (1962)

    Google Scholar 

  • Falck, B., Häggendal, J., Owman, Ch.: The localization of adrenaline in adrenergic nerves in the frog. Quart. J. exp. Physiol. 48, 253–257 (1963)

    Google Scholar 

  • Falck, B., Owman, Ch.: A detailed methodological description of the fluorescence method for the cellular demonstration of biogenic monoamines. Acta Univ. Lund II, 7, 1–23 (1965)

    Google Scholar 

  • Falck, B., Owman, Ch., Sjöstrand, N. O.: Peripherally located adrenergic nerves innervating the vas deferens and the seminal vesicle of the guinea-pig. Experientia (Basel) 21, 98–100 (1965)

    Google Scholar 

  • Fillenz, M.: Fine structure of noradrenaline storage vesicles in nerve terminals of the rat vas deferens. Phil. Trans. B 261, 319–323 (1971)

    Google Scholar 

  • Furness, J. B., Campbell, G. R., Gillard, S. M., Malmfors, T., Cobb, J. U. S., Burnstock, G.: Cellular studies of sympathetic denervation produced by 6-hydroxydopamine in the vas deferens. J. Pharmacol. exp. Ther. 174, 111–122 (1970)

    Google Scholar 

  • Fuxe, K., Hökfelt, T., Jonsson, G., Ungerstedt, U.: Fluorescence microscopy in neuroanatomy. In: S. J. Nauta and S. O. E. Ebbesson (eds.), Contemporary research methods in neuroanatomy, p. 275–314. Berlin-Heidelberg-New York: Springer 1970

    Google Scholar 

  • Ganong, W. F.: Sympathetic effect on renin secretion: Mechanism and physiological role. In: Control of renin secretion, ed. by T. A. Assaykeen, p. 17. New York: Plenum Press 1972

    Google Scholar 

  • Gaupp, E.: Anatomie des Frosches. III. Lehre von den Eingeweiden, dem Integument und den Sinnesorganen. Apparatus urogenitalis, p. 223–365 Braunschweig 1904

  • Geffen, L. B., Livett, B. G.: Synaptic vesicles in sympathetic neurons. Physiol. Rev. 51, 98–157 (1971)

    Google Scholar 

  • Gill, J. R., Jr.: In: Frontiers in neuroendocrinology — 1969, p. 289. London and New York: Oxford Univ. Press 1969. Quoted after Barajas and Müller (1973)

    Google Scholar 

  • Gillard, S. M., Read, J. B.: Fluorescent histochemical studies on the effects of 6-hydroxydopamine on adrenaline-containing nerves in the toad. Z. Zellforsch. 118, 493–511 (1971)

    Google Scholar 

  • Gosling, J. A.: Observations on the distribution of intrarenal nervous tissue. Anat. Rec. 163, 81–88 (1969)

    Google Scholar 

  • Gosling, J. A., Dixon, J. S.: The effect of 6-hydroxydopamine on nerves in the rat upper urinary tract. J. Cell Sci. 10, 197–209 (1972)

    Google Scholar 

  • Gresik, E. W.: Fine structural evidence for the presence of nerve terminals in the testis of the teleost, Oryzias latipes. Gen. comp. Endocr. 21, 210–213 (1973)

    Google Scholar 

  • Haase, E.: Histochemische und elektronenmikroskopische Untersuchungen über die Innervation des Hodens vom Bergfink (Fringilla montifringilla). Verh. Dtsch. Zool. Ges. 66. Jahresvers. Stuttgart: Gustav Fischer 1973

    Google Scholar 

  • Hirt, A.: Zur Innervation der Niere und Nebenniere des Frosches. Z. Anat. Entwickl. Gesch. 91, 5/6 (1930)

    Google Scholar 

  • Hökfelt, T.: The effect of reserpine on the intraneuronal vesicles of the rat vas deferens. Experientia (Basel) 22, 56 (1966)

    Google Scholar 

  • Hökfelt, T.: Electron microscopic studies on peripheral and central monoamine neurons. In: Aspects of Neuroendocrinology, ed. by W. Bargmann and B. Scharrer, p. 87–94. Berlin Heidelberg-New York: Spirnger 1971

    Google Scholar 

  • Hökfelt, T., Jonsson, G., Sachs, Ch.: Fine structure and fluorescence morphology of adrenergic nerves after 6-hydroxydopamine in vivo and in vitro. Z. Zellforsch. 131, 529–543 (1972)

    Google Scholar 

  • Holzbauer, M., Sharman, D. F.: The distribution of catecholamines in vertebrates. In: Handbook of experimental pharmacology, vol. 33 (ed. by H. Blaschko and E. Muscholl), p. 110–185. Berlin-Heidelberg-New York: Springer 1972

    Google Scholar 

  • Jonas, L., Spannhof, L.: Elektronenmikroskopischer Nachweis von Mucoproteiden in den Flaschenzellen der Urniere von Xenopus laevis Daudin mittels Phosphorwolframsäurefärbung. Acta histochem. (Jena) 41, 185–192 (1971)

    Google Scholar 

  • Lamers, A. P. M., Dongen, W. J. van: The morphology of the juxtaglomerular apparatus in Bufo bufo. Some light- and electronmicroscopic observations. Gen. comp. Endocr. 18, 602 (1972)

    Google Scholar 

  • Lane, B. P., Rhodin, J. A. G.: Cellular interrelationships and electrical activity in two types of smooth muscle. J. Ultrastruct. Res. 10, 470–488(1964)

    Google Scholar 

  • Lange, W.: Personal communication (1974)

  • Ljunggren, L.: Studies on seasonal activity in pigeons with aspects on the role of biogenic monoamines in the endocrine organs. Thesis. CWK Gleerup, Lund (1969)

    Google Scholar 

  • Ljungqvist, A., Wågermark, J.: The adrenergic innervation of intrarenal glomerular and extra-glomerular circulatory routes. Nephron (Basel) 7, 218–229 (1970)

    Google Scholar 

  • Malmfors, T., Sachs, Ch.: Degeneration of adrenergic nerves produced by 6-hydroxydopamine. Europ. J. Pharmacol. 3, 89–92 (1968)

    Google Scholar 

  • McKenna, O. C., Angelakos, E. T.: Adrenergic innervation of the canine kidney. Circulat. Res. 22, 345–354 (1968a)

    Google Scholar 

  • McKenna, O. C., Angelakos, E. T.: Acetylcholinesterase containing nerve fibers in the canine kidney. Circulat. Res. 23, 645–651 (1968b)

    Google Scholar 

  • Merrillees, N. C. R., Burnstock, G., Holman, M. E.: Correlation of fine structure and physiology of the innervation of smooth muscle in the guinea-pig vas deferens. J. Cell Biol. 19, 529–550 (1963)

    Google Scholar 

  • Möllendorff, W. von: Der Exkretionsapparat. In: Handbuch der mikroskopischen Anatomie des Menschen, vol. VII/1, ed. by W. v. Möllendorff. Berlin: Springer 1930

    Google Scholar 

  • Müller, J., Barajas, L.: Electron microscopic and histochemical evidence for a tubular innervation in the renal cortex of the monkey. J. Ultrastruct. Res. 41, 533–549 (1972)

    Google Scholar 

  • Munkacsi, I.: Distribution of the interrenal monoaminergic nerves in the kidneys of the desert rat (Dipodomys merriami) and the white rat (Rattus norvegicus). Acta anat. (Basel) 73, 56–68 (1969)

    Google Scholar 

  • Newstead, J. D.: Filaments in renal parenchymal and interstitial cells. J. Ultrastruct. Res. 34, 316–328 (1971)

    Google Scholar 

  • Norberg, K. A.: Transmitter histochemistry of the sympathetic adrenergic nervous system. Brain Res. 5, 125–170 (1967)

    Google Scholar 

  • Norberg, K. A., Risley, P. L., Ungerstedt, U.: Adrenergic innervation of the male reproductive ducts in some mammals. I. The distribution of adrenergic nerves. Z. Zellforsch. 76, 278–286 (1967)

    Google Scholar 

  • Norvell, J. E.: A histochemical study of the adrenergic and cholinergic innervation of the mammalian kidney. Anat. Res. 163, 236 (1969)

    Google Scholar 

  • Norvell, J. E., Weitsen, H. A., Sheppek, G. G.: The intrinsic innervation of human renal homotransplants. Transplantation 9, 168–176 (1970)

    Google Scholar 

  • Notley, R. G.: The innervation of the upper ureter in man and in the rat: An ultrastructural study. J. Anat. (Lond.) 105, 393–402 (1969)

    Google Scholar 

  • Ohgushi, N., Mohri, K., Sato, M., Onsumi, K., Tsunekawa, K.: Histochemical demonstration of adrenergic fibers in the renal tubules of dog. Experientia (Basel) 26, 401 (1970)

    Google Scholar 

  • Owman, Ch., Sjöstrand, N. O.: Short adrenergic neurons and catecholamine-containing cells in vas deferns and accessory male genital glands of different mammals. Z. Zellforsch. 66, 300–320 (1965)

    Google Scholar 

  • Pease, D. C.: Myoid feature of renal corpuscles and tubules. J. Ultrastruct. Res. 23, 304–320 (1968)

    Google Scholar 

  • Richards, J. G., Tranzer, J. P.: Electron microscopic localization of 5-hydroxydopamine, a “false” adrenergic neurotransmitter, in the autonomic nerve endings of the rat pineal gland. Experientia (Basel) 25, 53–54 (1969)

    Google Scholar 

  • Richardson, K. C.: The fine structure of autonomic nerve endings in smooth muscle of the rat vas deferens. J. Anat. (Lond.) 96, 427–442 (1967)

    Google Scholar 

  • Richardson, K. C., Jarret, L., Finke, E. H.: Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol. 35, 313–323 (1960)

    Google Scholar 

  • Robinson, P. M.: A cholinergic component of the innervation of the guinea-pig vas deferens: The fine structural localization of cholinesterase. J. Cell Biol. 41, 462–476 (1969)

    Google Scholar 

  • Ross, M. H., Reith, E. J.: Myoid elements in the mammalian nephron and their relationship to other specializations in the basal part of kidney tubule cells. Amer. J. Anat. 129, 399–416 (1970)

    Google Scholar 

  • Rostgaard, J., Kristensen, B. I., Nielsen, C. E.: Electron microscopy of filaments in the basal part of rat kidney tubule cells, and their in situ interaction with heavy meromyosin. Z. Zellforsch. 132, 497–521 (1972)

    Google Scholar 

  • Segura, E. T., Biscardi, A. M., Apelbaum, J.: Seasonal variations of brain epinephrine, norepinephrine and 5-hydroxytryptamine associated with changes in the EEG of the toad, Bufo arenarum Hensel. Comp. Biochem. Physiol. 22, 843–850 (1967)

    Google Scholar 

  • Silverman, A.-J., Barajas, L.: Effect of reserpine on the juxtaglomerular granular cells and renal nerves. Lab. Invest. 30, 723–731 (1974)

    Google Scholar 

  • Sjöstrand, N. O.: The adrenergic innervation of the vas deferens and the accessory male genital glands. Acta physiol. scand. 65, Suppl. 257, 1–82 (1965)

    Google Scholar 

  • Sjöstrand, N. O.: Noradrenaline-containing cells in the epididymis and vas deferens of the tortoise Testudo hermanni. Acta zool. (Stockh.) 50, 271–275 (1969)

    Google Scholar 

  • Sokabe, H., Ogawa, M.: Comparative studies of the juxtaglomerular apparatus. Int. Rev. Cytol. 27, 271–327 (1974)

    Google Scholar 

  • Spanner, R.: Untersuchungen über die Nerven der Niere von Rana agilis und Anguis fragilis mit der Methylenblaufärbung. Verh. Anat. Ges. 1928, Erg.-Bd. zu Bd. 66, pp. 88–93

    Google Scholar 

  • Spannhof, L., Jonas, L.: Elektronenmikroskopische Untersuchungen zur Genese und Sekretbildung in den Flaschenzellen der Urniere vom Krallenfrosch. Z. Zellforsch. 95, 134–142 (1969)

    Google Scholar 

  • Taxi, J.: Contribution a l'étude des connexions des neurones moteurs du système nerveux autonome. Naturelles Zool. 12e sér. 7, 413–674 (1965)

    Google Scholar 

  • Tingari, M. D., Lake, P. E.: The intrinsic innervation of the reproductive tract of the male fowl (Gallus domesticus). A histochemical and fine structural study. J. Anat. (Lond.) 112, 257–271 (1972)

    Google Scholar 

  • Tranzer, J. P., Thoenen, H.: Ultramorphologische Veränderungen der synaptischen Nervenendigungen der Katze nach Vorbehandlung mit 5- und 6-Hydroxy-Dopamin. Naunyn-Schmiedebergs Arch. Pharmak. exp. Path. 257, 343–344 (1967)

    Google Scholar 

  • Tranzer, J. P., Thoenen, H.: An electron microscopic study of selective, acute degeneration of sympathetic nerve terminals after administration of 6-hydroxydopamine. Experientia (Basel) 24, 155–156 (1968)

    Google Scholar 

  • Unsicker, K.: Innervation of the testicular interstitial tissue in reptiles. Z. Zellforsch. 146, 123–138 (1973)

    Google Scholar 

  • Unsicker, K.: Fine structure of the male genital tract and kidney in the amphibia Xenopus laevis Daudin, Rana temporaria L., and Bufo bufo L. under normal and experimental conditions. I. Testicular interstitial tissue and seminal efferent ducts. Cell Tiss. Res. 158, 215–240 (1975a)

    Google Scholar 

  • Unsicker, K.: Fine structure of the male genital tract and kidney in the amphibia Xenopus laevis Daudin, Rana temporaria, and Bufo bufo L. under normal and experimental conditions. II. Kidney and ureter (ductus deferens). In preparation (1975b)

  • Unsicker, K., Krisch, B.: Kontraktile Filamente im Nephron. Dtsch. med. Wschr. 100, 116–119 (1975)

    Google Scholar 

  • Wågermark, J., Ungerstedt, U., Ljungqvist, A.: Sympathetic innervation of the juxtaglomerular cells of the kidney. Circulat. Res. 22, 149–153 (1968)

    Google Scholar 

  • Waleewa, Ch. G.: Vergleichend-anatomische Untersuchungen über die Mikromorphologie des Nervenapparates der Niere. I. Mitteilung: Zur Morphologie des Nervenapparates der Niere bei Amphibien. Anat. Anz. 108, 20–25 (1960)

    Google Scholar 

  • Weitsen, H. A., Norvell, J. E.: Cholinergic innervation of the autotransplanted canine kidney. Circulat. Res. 25, 535–541 (1969)

    Google Scholar 

  • Williams, T.: Cytology of nervous tissue, p. 12. London: Taylor and Francis 1961

    Google Scholar 

  • Yamagishi, S., Azuma, T.: Innervation of renal blood vessels of the toad. Jap. J. Physiol. 13, 399–412 (1963)

    Google Scholar 

  • Yamauchi, A., Burnstock, G.: Post-natal development of the innervation of the mouse vas deferens. A fine structural study. J. Anat. (Lond.) 104, 17–32 (1969)

    Google Scholar 

  • Zimmermann, H. D.: Elektronenmikroskopische Befunde zur Innervation des Nephron nach Untersuchungen an der fetalen Nachniere des Menschen. Z. Zellforsch. 129, 65–75 (1972)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This work was supported by grants from Deutsche Forschungsgemeinschaft (Un 34/2) and the Swedish Medical Research Council. The skilful and invaluable technical assistance of Mrs. K. Jacob, Mrs. R. Sprang, and Mrs. K. Fogelström is gratefully acknowledged.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Unsicker, K., Axelsson, S., Owman, C. et al. Innervation of the male genital tract and kidney in the amphibia, Xenopus laevis daudin, Rana temporaria L., and Bufo bufo L.. Cell Tissue Res. 160, 453–484 (1975). https://doi.org/10.1007/BF00225764

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00225764

Key words

Navigation