Summary
In the tortoise Testudo graeca, the lizards Lacerta dugesi and Lacerta pityusensis, and the snake Natrix natrix, the innervation of the testicular interstitial tissue was studied by light and electron microscopy, the acetylcholinesterase (ache) technique, the Falck-Hillarp method for the detection of catecholamines, and the application of 6-hydroxydopamine. The intertubular spaces of the reptilian testes studied contain adrenergic nerve fibers the amount and distribution of which varies considerably both in various species and in various stages of the reproduction cycle. Nerve fibers do not enter the seminiferous epithelium. Fluorescence microscopy of the lizard testis reveals catecholaminergic varicosities which are mainly arranged around blood vessels, but do not show obvious connexions to Leydig cells. Ache-positive fibers are equally distributed in lizard testes surrounding each seminiferous tubule. In Natrix natrix ache-positive fibers are irregularly spread among groups of tubules, without showing a definite relation to Leydig cells either. By electron microscopy bundles of unmyelinated axons and axon terminals can be more easily detected in the testes of immature animals than in adult. Terminals of nerve fibers containing small (400–500 Å in diameter) and large (800–1400 Å) dense-cored vesicles and sometimes small clear vesicles establish contacts with Leydig cells. Three types of contact are described. 1. “Contacts” par distance at a distance of about 2000 Å and basal lamina interposed; 2. membranous contacts having a 200 Å gap only between axolemma and Leydig cell plasmalemma; 3. invaginations of terminals into Leydig cell perikarya. The latter may exhibit surface specialisations, which strongly resemble postsynaptic membrane thickenings. Experiments using 6-hydroxydopamine underline the adrenergic character of testicular nerve fibers, which can be regarded as another example of non-cholinergic, ache-positive neurons. In the testis of the immature tortoise profiles of axons occur which probably represent purinergic, ache-positive neurons.
Similar content being viewed by others
References
Anton, A. H., Sayre, D. F.: A study of factors affecting the aluminium oxide trihydroxyindole procedure for the analysis of catecholamine. J. Pharmacol. exp. Ther. 138, 360–375 (1962)
Baumgarten, H. G., Falck, B., Holstein, A. F., Owman, Chr., 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)
Baumgarten, H. G., Holstein, A. F.: Catecholaminhaltige Nervenfasern im Hoden des Menschen. Z. Zellforsch. 79, 389–395 (1967)
Baumgarten, H. G., Holstein, A. F.: Adrenerge Innervation im Hoden und Nebenhoden vom Schwan (Cygnus olor). Z. Zellforsch. 91, 402–410 (1968)
Baumgarten, H. G., Holstein, A. F.: Noradrenerge Nervenfasern im Hoden von Mammaliern und anderen Vertebraten. J. neuro-visc. Rel., Suppl. 10, 563–572 (1971)
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 (1970)
Belt, W. D., Cavazos, L. F.: Personal communication. Quoted after Hodson, (1970)
Bennett, 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)
Bennett, M. R., Rogers, D. C.: A study of the innervation of the taenia coli. J. Cell Biol. 33, 573–596 (1967)
Burnstock, G.: Evolution of the autonomic innervation of visceral and cardiovascular systems in vertebrates. Pharmacol. Rev. 21, 247–324 (1969)
Burnstock, G.: Purinergic nerves. Pharmacol. Rev. 24, 509–581 (1972)
Burnstock, G., Iwayama, T.: Fine structural identification of autonomic nerves and their relation to smooth muscle. Progr. Brain Res. 34, 389–404 (1971)
Campenhout, E. van: Les relations nerveuses de la glande interstitielle des glandes génitales chez les mammifères. Rev. Can. Biol. 8, 374 (1949)
Dayan, A. D.: Variation between species in the innervation of intratesticular blood vessels. Experientia (Basel) 26, 1359–1360 (1970)
Dodd, J. M.: Gonadal and gonadotrophic hormones in lower vertebrates. In: Marshall's physiology of reproduction (ed. by A. S. Parkes), vol. I, part 2, p. 417–582. London: Longmans-Green 1960
Eränkö, O., Rechardt, L., Eränkö, F., Cunningham, A.: Light and electron microscopic histochemical observations on cholinesterase-containing sympathetic nerve fibers in the pineal body of the rat. Histochem. J. 2, 479–489 (1970)
Eyeson, K. N.: The role of the pituitary gland in testicular function in the lizard Agama agama. Gen. comp. Endocr. 16, 342–355 (1971)
Fillenz, M.: Fine structure of noradrenaline storage vesicles in nerve terminals of the rat vas deferens. Phil. Trans. B, 261, 319–323 (1971)
Furness, J. B., Campbell, G. R., Gillard, S. M., Malmfors, T., Cobb, J.L S., Burnstock, G.: Cellular studies of sympathetic denervation produced by 6-hydroxydopamine in the vas deferens. J. Pharmacol. exp. Ther. 174, 111–122 (1970)
Geffen, L. B., Livett, B. G.: Synaptic vesicles in sympathetic neurons. Physiol. Rev. 51, 98–157 (1971)
Gray, D. J.: The intrinsic nerves of the testis. Anat. Rec. 98, 325–331 (1947)
Gwyn, D. G., Flumerfelt, B. A.: Acetylcholinesterase in non-cholinergic neurons: A histochemical study of dorsal root ganglion cells in the rat. Brain Res. 34, 193–198 (1971)
Haase, E.: Histochemische und elektronenmikroskopische Untersuchungen über die Innervation des Hodens vom Bergfink (Fringilla montifringilla). Verh. der Dtsch. Zool. Ges., 66. Jahresvers. Stuttgart: Gustav Fischer 1973
Haeusler, G., Haefely, W., Thoenen, H.: Chemical sympathectomy of the cat with 6-hydroxydopamine. J. Pharmacol. exp. Ther. 170, 50–61 (1969)
Hajos, F., Priymak, E. K., Kerpel-Fronius, S.: The electron microscopic demonstration of acetylcholinesterase activity in some cholinergic and non-cholinergic synapse of the rat brain. Acta histochem. (Jena) 35, 114–122 (1970)
Hervonen, A., Kanerva, L., Rechardt, L.: Localization of catecholamines and acetylcholinesterase in the terminal nerve fibres of the rabbit myometrium. Histochemic 32, 89–93 (1972)
Hodson, 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
Hökfelt, T.: In vitro studies on central and peripheral monoamine neurons at the ultrastructural level. Z. Zellforsch. 91, 1–74 (1968)
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: Springer 1971
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)
Holzbauer, M., Sharman, D. F.: The distribution of catecholamines in vertebrates. In: Handbook of experimental pharmacology, vol. XXXIII (ed. by O. Eichler, A. Farah, H. Herken, and A. D. Welch). Berlin-Heidelberg-New York: Springer 1972
Hooker, C. W.: The intertubular tissues of the testis. In: The Testis, (ed. by A. D. Johnson, W. R. Gomes and N. L. Vandemark), vol. I, p. 483–550. New York and London: Academic Press 1970
Jaim-Etcheverry, G., Zieher, L. M.: Cytochemistry of 5-hydroxytryptamine at the electron microscope level. 2. Localization in the autonomic nerves of the rat pineal gland. Z. Zellforsch. 86, 393–400 (1968)
Kuntz, A.: The innervation of the gonads in the dog. Anat. Rec. 17, 203–219 (1919a)
Kuntz, A.: Experimental degeneration in the testis in the dog. Anat. Rec. 17, 221–234 (1919b)
Licht, P.: Actions of mammalian pituitary gonadotropins (FSH and LH) in reptiles. I. Male snakes. Gen. comp. Endocr. 19, 273–281 (1972)
Licht, P.: Actions of mammalian pituitary gonadotropins (FSH and LH) in reptiles. II. Turtles. Gen. comp. Endocr. 19, 282–289 (1972)
Licht, P., Pearson, A. K.: Effects of mammalian gonadotropins (FSH and LH) on the testes of the lizard Anolis carolinensis. Gen. comp. Endocr. 13, 367–381 (1969)
Lofts, B.: Seasonal cycles in reptilian testes. Gen. comp. Endocr. Suppl. 2, 147–155 (1969)
Mitchell, G.A.G.: The innervation of the ovary, uterine, tube, testis and epididymis. J. Anat. (Lond.) 72, 508–517 (1938)
Murakami, T., Kawakara, G.: Über die Nervenendapparate im Hodensack und Hoden des menschlichen Foetus. Arch. hist. jap. 4, 351–357 (1952)
Okkels, H., Sand, K.: Nerfs du testicule et glande interstitielle. C. R. Soc. Biol. (Paris) 129, 807–810 (1938)
Okkels, H., Sand, K.: Morphologische Relation zwischen Nervensystem und Leydig-Zellen in menschlichen Hoden. Endokrinologie 21, 231–239 (1939)
Okkels, H., Sand, K.: Morphological relationship between testicular nerves and Leydig cells in man. J. Endocr. 2, 38 (1940)
Pearse, A.G.E.: Histochemistry. Theoretical and applied. Third edit. vol. 2. Edinburgh and London: Churchill Livingstone, 1972
Peters, H.: Über die feinere Innervation des Hodens, insbesondere des interstitiellen Gewebes und der Hodenkanälchen beim Menschen. Acta neuroveg. (Wien) 15, 235–242 (1917)
Retzius, G.: Über die Nerven der Ovarien und Hoden. Biol. Untersuch., N. S. 5, 31 (1893). Quoted after Hodson (1970)
Risley, R. L., Skrepetos, C. N.: Histochemical distribution of cholinesterases in the testis, epididymis and vas deferens of the rat. Anat. Rec. 148, 231–249 (1964)
Robinson, P. M., McLean, J. R., Burnstock, G.: Ultrastructural identification of non-adrenergic inhibitory nerve fibres. J. Pharmacol. exp. Ther. 179, 149–160 (1971)
Rodríguez de Lores Arnaiz, G., Pellegrino de Iraldi, A.: Cholinesterase in cholinergic and adrenergic nerves: A study of the superior cervical ganglia and the pineal gland of the rat. Brain Res. 42, 230–233 (1972)
Sclavunos, G.: Über die feinere Nerven und ihre Endigungen in den männlichen Genitalen. Anat. Anz. 9, 42–55 (1894)
Shioda, T., Nishida, S.: Innervation of the bull testis. Jap. J. vet. Sci. 28, 251 (1966). Quoted after Hodson, N. (1970)
Stach, W.: Zur Innervation der Leydigschen Zwischenzellen im Hoden. Z. mikr.-anat. Forsch. 69, 569–584 (1963)
Stöhr, Ph., jr.: Mikroskopische Anatomie des vegetativen Nervensystems. In: Handbuch der mikroskopischen Anatomie des Menschen (W. Bargmann, ed.), Bd. IV/5. Berlin-Göttingen-Heidelberg: Springer 1957
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)
Timofeew, D.: Zur Kenntnis der Nervenendigungen in den männlichen Geschlechtsorganen der Säuger. Anat. Anz. 9, 342–348 (1894)
Tranzer, J. P., Thoenen, H.: Ultramorphologische Veränderungen der sympathischen Nervenendigungen der Katze nach Vorbehandlung mit 5- und 6-Hydroxydopamin. Naunyn-Schmiedebergs Arch. Pharmak. exp. Path. 257, 343–344 (1967)
Tranzer, J. P., Thoenen, H.: Various types of amine-storing vesicles in peripheral adrenergic nerve terminals. Experientia (Basel) 24, 484–486 (1968)
Unsicker, K.: Fine structure and innervation of the avian adrenal gland. III. Non-cholinergic nerve fibers. Z. Zellforsch. (in press) (1973)
Unsicker, K.: Innervation of the reptilian interrenal gland (in preparation)
Author information
Authors and Affiliations
Additional information
Supported by a grant from the Deutsche Forschungsgemeinschaft (Un 34/1).
I am much indebted to Mrs. R. Sprang for her skillfull technical assistance.
Rights and permissions
About this article
Cite this article
Unsicker, K. Innervation of the testicular interstitial tissue in reptiles. Z.Zellforsch 146, 123–138 (1973). https://doi.org/10.1007/BF00306762
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00306762