Skip to main content
SpringerLink
Log in

Fine structure and innervation of the avian adrenal gland

V. Innervation of interrenal cells

  • Published:
Zeitschrift für Zellforschung und Mikroskopische Anatomie Aims and scope Submit manuscript

Summary

In all bird species investigated interrenal cells are reached by cholinergic nerve fibers forming synapses without postsynaptic membrane thickenings at their basis, more rarely at the lateral or apical cell surfaces. The density of innervation is considerably low if compared to the adrenal chromaffin organ; it is about 3 mm nerve length per 1 mm3 interrenal tissue in the house sparrow, 5 in the domestic fowl and 8 inCorvus frugilegus. P-type fibers which are only rarely to be seen also penetrate the basal lamina surrounding interrenal cells. Adrenergic fibers are only found outside the basal lamina.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alpert, L. K.: The innervation of the suprarenal glands. Anat. Rec.50, 221–233 (1931)

    Article  Google Scholar 

  • Bachmann, R.: Die Nebenniere. In: Handbuch der mikroskopischen Anatomie des Menschen, Bd. VI/5. Berlin-Göttingen-Heidelberg: Springer 1954

    Google Scholar 

  • Bargmann, W., Lindner, E.: Über den Feinbau des Nebennierenmarkes des Igels (Erinaceus europaeus L.) Z. Zellforsch.64, 868–912 (1964)

    Article  CAS  PubMed  Google Scholar 

  • 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)

    Article  CAS  PubMed  Google Scholar 

  • Baumgarten, H. G., Holstein, A. F.: Noradronerge Nervenfasern im Hoden von Mammaliern and anderen Vertebraten. J. nouro-vise. Rel., Suppl.10, 563–572 (1971)

    Google Scholar 

  • Bennett, H. S.: The life history and secretion of the cells of the adrenal cortex of the cat. Amer. J. Anat.67, 151–227 (1940)

    Article  CAS  Google Scholar 

  • Bennett, M. R., Rogers, D. C.: A study of the innervation of the taenia coli. J. Cell Biol.33, 573–596 (1967)

    Article  CAS  PubMed  Google Scholar 

  • Borruel, M., Lantos, C., Poumeau-Delille, G.: Action in vitro de l'adrénaline sur la synthèse des corticostéroides chez le rat et la souris. C. R. Acad. Sci. (Paris) D266, 2464 (1968)

    Google Scholar 

  • Brudieux, R., Delost, P.: Sécrétion des corticostéroides après déstruction de la médullosurrénale. J. Physiol. (Paris)59, 362 (1967)

    CAS  Google Scholar 

  • Brudieux, R., Delost, P.: Sécrétion des corticostéroides après autogreffe surrénalienne chez le rat. J. Physiol. (Paris)60, Suppl. 2, 411 (1968)

    Google Scholar 

  • Cauwenberge, H. van, Palem-Vliers, M., Lecomte, J.: Sur le pouvoir corticostimulant de la 5-hydroxytryptamine. C. R. Soc. Biol. (Paris)161, 2089–2091 (1967)

    Google Scholar 

  • Chester Jones, L: The adrenal cortex. Cambridge University Press 1957

  • Comsa, J.: Méchanisme de l'influence de la sympathectomie cervicale sur la cortico-surrénale du rat. Ann. Endocr. (Paris)24, 393 (1963)

    CAS  Google Scholar 

  • Coupland, R. E.: Nerve endings on chromaffin cells in the rat adrenal medulla. Nature (Lond.)194, 310–312 (1962)

    CAS  Google Scholar 

  • Coupland, R. E.: The innervation of the rat adrenal medulla. An electron microscopic study. J. Anat. (Lond.)97, 141–142 (1963)

    Google Scholar 

  • Coupland, R. E.: Electron microscopic observations on the structure of the rat adrenal medulla. II. Normal innervation. J. Anat. (Lond.)99, 255–272 (1965)

    Google Scholar 

  • Coupland, R. E., Weakeley, B. S.: Electron microscopic observation on the adrenal medulla and extraadrenal chromaffin tissue of the postnatal rabbit. J. Anat. (Lond.)106, 213–231 (1970)

    CAS  Google Scholar 

  • Cowley, L. H., Shackleford, J. M.: An ultrastructural study of the submandibular glands of the squirrel monkey,Saimiri sciureus. J. Morph.132, 117–136 (1971)

    Google Scholar 

  • Cushman, P., Alter, S., Hilton, J. G.: Cortisol secretion by the dog adrenal: effects of cyclic adenosine monophosphate, dichloroisoproterenol, dihydroergotamine and adrenaline. J. Endocr.34, 271–272 (1966)

    CAS  PubMed  Google Scholar 

  • Deane, H. W.: The Adrenocortical Hormones. In: Handbuch der experimentellen Pharmakologie, Bd. XIV/1. Berlin-Göttingen-Heidelberg: Springer 1962

    Google Scholar 

  • Denber, H.C.B.: Recherches sur l'innervation des capsules surrénales de l'homme et quelques autres mammifères. Schweiz. Arch. Neurol.54, 361–399 (1944)

    Google Scholar 

  • De Robertis, E., Ferreira, V. A.: Submicroscopic changes of the nerve endings in the adrenal medulla after stimulation of the splanchnio nerve. J. biophys. biochem. Cytol.3, 611–614 (1957)

    Google Scholar 

  • Dogiel, A.: Nervenendigungen in den Nebennieren der Sdugetiere. Arch. Anat. Physiol.1894, 90–104 (1894)

    Google Scholar 

  • Douglas, W. W., Kano, T., Sampson, S. R.: Effects of acetylcholine and other medullary secretagogues in chromaffin cells: and analysis employing techniques of tissue culture. J. Physiol. (Lond.)188, 107–120 (1967)

    CAS  Google Scholar 

  • Elfvin, L.-G.: The fine structure of the cell surface of chromaffin cells in the rat adrenal medulla. J. Ulstrastruct. Res.12, 263–286 (1965)

    CAS  Google Scholar 

  • Evans, D.H.L.: Endings produced by somatic nerve fibers growing into the adrenal gland. J. Anat. (Lond.)81, 225–232 (1947)

    Google Scholar 

  • Feldberg, W., Hinz, B., Tsudzimura, H.: The mechanism of the nervous discharge of adrenaline. J. Physiol. (Lond.)81, 286–304 (1934)

    CAS  Google Scholar 

  • Fusari, R.: De la terminaison des fibres nerveuses dans les capsules surrénales des mammifères. Arch. ital. Biol.16, 262–275 (1891)

    Google Scholar 

  • Garcia-Alvarez, F.: Estudio ultraestructural sobre la inervacion de la eorteza suprarenal. An. Anatomia (Zaragoza)19, 267–279 (1970)

    Google Scholar 

  • Gaudarias, J. M.: El acide ascorbico en las glandulas sobrarenales despues de la estimulacion de les nervios esplancnicos. Rev. esp. Fisiol.7, 165 (1951)

    Google Scholar 

  • Gershberg, H., Fry, E. G., Brobeck, T. R., Long, C.N.H.: Role of epinephrine in the secretion of the adrenal cortex. Yale J. Biol. Med.23, 32 (1950)

    CAS  PubMed  Google Scholar 

  • Giacomini, E.: Sur les terminaisons nerveuses dans le capsules surrénales des oiseaux. Arch. ital. Biol.29, 482–483 (1898)

    Google Scholar 

  • Gorbman, A., Bern, H. A.: A textbook of comparative endocrinology. New York-London-Sidney: John Wiley & Sons, Inc. 1962

    Google Scholar 

  • Grassé, P.-P., Devillers, Ch.: Précis de Zoologie. II. Vertébrés, Paris: Masson & Cie 1965

    Google Scholar 

  • Gray, E. G., Guillery, R. W.: Synaptic morphology in the normal and degenerating nervous system. Int. Rev. Cytol.19, 111–182 (1966)

    CAS  PubMed  Google Scholar 

  • Grynszpan-Winograd, O.: Persistance des synapses an niveau de cellules chromaffines en mitose, pendant le développement. C. R. Acad. Sci. (Paris)269, 348–350 (1969)

    CAS  Google Scholar 

  • Hennig, A.: Linge eines dreidimensionalen Linienzuges. Proc. I. Int. Congr. Stereology, vol. 44, p. 1–8. Wien: Med. Akad. 1963

    Google Scholar 

  • Hollinshead, W. H.: The innervation of the adrenal glands. J. comp. Neurol.64, 449–467 (1936)

    Article  Google Scholar 

  • Hoshi, T.: Histologie der Nebennierennerven [Japanese]. Tohoku Igaku Zasshi9, 443–468 (1926)

    Google Scholar 

  • Hubbard, J. I.: Mechanism of transmitter release. Progr. Biophys.21, 33–124 (1970)

    CAS  PubMed  Google Scholar 

  • Iwaki, K.: Über die Innervation der Nebenniere vom Meerschweinchen. Kurume med. J.2, 204–217 (1955)

    Google Scholar 

  • Jung, A., Comsa, J.: Conséquences de l'extirpation unilatérale du ganglion cervicale supérieur sur l'état fonctionnel de la corticosurrénale du rat. Ann. Endocr. (Paris)19, 17 (1958)

    CAS  Google Scholar 

  • Kagayama, M.: The fine structure of the monkey submandibular gland with a special reference to intra-acinar nerve endings. Amer. J. Anat.131, 185–196 (1971)

    Article  CAS  PubMed  Google Scholar 

  • Kiss, T.: Experimentell-morphologische Analyse der Nebenniereninnervation. Acta anat. (Basel)13, 81–89 (1951)

    CAS  Google Scholar 

  • Koch, B., Mialke, C., Stutinsky, F.: Dissociation entre excrétion et sécrétion de la corticostérone chez le rat porteur d'une autogreffe surrénalienne. C. R. Acad. Sci. (Paris)254, 744–746 (1962a).

    CAS  Google Scholar 

  • Koch, B., Mialke, C., Stutinsky, F.: Influence de la médullo-surrénale sur la production de la corticostérone chez le rat au cours d'une agression. C. R. Acad. Sci. (Paris)255, 1021–1023 (1962b)

    Google Scholar 

  • Kühnel, W.: Struktur und Cytochemie der Harderschen Drüsen vom Kaninchen. Z. Zellforsch.119, 384–404 (1971a).

    Article  PubMed  Google Scholar 

  • Kühnel, W.: Synapsen und exokrinen Drüsen. Naturwissenschaften58, 369 (1971b)

    Article  PubMed  Google Scholar 

  • Kühnel, W.: Morphologische Untersuchungen an der Glandula infraorbitalis buccalis vom Kaninchen. Z. Zellforsch.123, 55–65 (1972a)

    Article  PubMed  Google Scholar 

  • Kühnel, W.: On the innervation of the salt gland. Z. Zellforsch.134, 435–438 (1972b)

    Article  PubMed  Google Scholar 

  • Kura, N.: Über die Innervation der Nebenniere (japanese). Mitt. Med. Akad. Kyoto1, 107–124 (1927)

    Google Scholar 

  • Lever, J. D.: Nerve fibers in the adrenal cortex of the rat. Nature (Lond.)171, 882–883 (1953)

    CAS  Google Scholar 

  • Lever, J. D.: Electron microscopic observations on the normal and denervated adrenal medulla of the rat. Endocrinology57, 621–635 (1955)

    CAS  PubMed  Google Scholar 

  • Lewis, P. R., Shute, C. C. D.: The simultaneous demonstration of catecholamines and cholinesterases with the electron microscope. J. Physiol. (Lond.)189, 53P-55P (1967)

    Google Scholar 

  • Lewis, P. R., Shute, C. C. D.: An electron microscopic study of cholinesterase distribution in the rat adrenal medulla. J. Microscopy89, 181–193 (1969)

    CAS  Google Scholar 

  • Loewenstein, W. R., Socolar, S. J., Higashino, S., Kauno, Y., Davodson, N.: Intercellular communication: renal, urinary bladder, sensory and salivary cells. Science149, 295 (1965)

    Google Scholar 

  • Long, C.N.H., Fry, E. G.: Effect of epinephrine on adrenal cholesterol and ascorbic acid. Proc. Soc. exp. Biol. (N.Y.)59, 67 (1945)

    CAS  Google Scholar 

  • MacFarland, W. E., Davenport, H. E.: Adrenal innervation. J. comp. Neurol.75, 219–233 (1941)

    Article  Google Scholar 

  • Marley, E., Prout, G. J.: Physiology and pharmacology of the splanchnic-adrenal medullary junction. J. Physiol. (Lond.)180, 483–513 (1965)

    CAS  Google Scholar 

  • Marley, E., Prout, G. J.: Innervation of the cats adrenal medulla. J. Anat. (Lond.)102, 257–273 (1968)

    CAS  Google Scholar 

  • Maycock, W. A., Heslop, T. S.: An experimental investigation of the nerve supply of the adrenal medulla of the cat. J. Anat. (Lond.)73, 551–558 (1939)

    Google Scholar 

  • Mikkail, Y.: Innervation of the different zones of the adrenal cortex. J. comp. Neurol.117, 365–369 (1961)

    Google Scholar 

  • Mikolajczyk, H.: Urinary output of 17-Ks and microscopic changes in the adrenal cortex of rats treated with heparin, histamine or serotonin. Endocr. Polska16, 347–358 (1965)

    CAS  Google Scholar 

  • Moe, H., Bojsen-Müller, F.: The fine structure of the lateral nasal gland (Steno's gland) of the rat. J. Ultrastruct. Res.36, 127–148 (1971)

    Article  CAS  PubMed  Google Scholar 

  • Okinaka, S., Nakao, K., Nishikawa, M., Ikeda, M., Ibayashi, H.: Tohoku J. exp. Med.56, 153 (1962). Quoted after Rosenfeld (1955)

    Google Scholar 

  • Pines, L., Narowtschatowa, K.: Über die Innervation der Nebennieren. Z. mikr.-anat. Forsch.25, 518–538 (1931)

    Google Scholar 

  • Piroth, M., Oberhausen, E., Comsa, J.: L'influence du système nerveux sympathique sur les glandes à sécrétion interne. Path-Biol. (Paris)12, 1000–1017 (1964)

    CAS  Google Scholar 

  • Ratzenhofer, M., Müller, O., Becker, H.: Zur Innervation der Drüsen- und Stromazellen ira Kaninchenmagen. Mikroskopie25, 283–296 (1969)

    CAS  PubMed  Google Scholar 

  • Renner, O.: Die Innervation der Nebenniere. Dtsch. Arch. Klin. Ond.114, 473–483 (1914)

    Google Scholar 

  • Richardson, K. C.: The fine structure of autonomic nerve endings in smooth muscles of the rat vas deferens. J. Anat. (Lond.)96, 427–442 (1962)

    CAS  Google Scholar 

  • Richardson, K. C.: Fine structure of the albino rabbit iris with special reference to the identification of adrenergic and cholinergic nerves and nerve endings in its intrinsic muscles. Amer. J. Anat.114, 173–205 (1964)

    Article  CAS  PubMed  Google Scholar 

  • Robinson, P.M.: A cholinergic component in the innervation of the longitudinal smooth muscle of the guinea pig vas deferens. J. Cell Biol.41, 462–476 (1969)

    Article  CAS  PubMed  Google Scholar 

  • Rogers, D. C.: Fine structure of smooth muscle and neuromuscular junctions in the optic tentacles ofHelix aspersa andLimax flavus. Z. Zellforsch.89, 80–94 (1968)

    Article  CAS  PubMed  Google Scholar 

  • Romer, A. S.: Vergleichende Anatomie der Wirbeltiere. Übersetzt and bearbeitet von H. Frick. 2. Aufl. Hamburg u. Berlin: Paul Parey 1966

    Google Scholar 

  • Rosenfeld, G.: Stimulative effect of acetylcholine on the adrenocortical function of isolated perfused calf adrenals. Amer. J. Physiol.183, 272–278 (1955)

    CAS  PubMed  Google Scholar 

  • Sarter, Y.: Histologische Studie über die Innervation der Nebexmierenrinde. Z. Zellforsch.40, 207–221 (1954)

    Article  CAS  PubMed  Google Scholar 

  • Sato, A.: Innervation of corpus suprarenale in human adult. Tohoku J. exp. Med.55, 259–271 (1952)

    CAS  PubMed  Google Scholar 

  • Schaefer, H., Kraemer, H., Kurten, B.: Conséquences de la sympathectomie cervicale droite sur la teneur en acide ascorbique de la surrénale de la ratte thyréoprive. Ann. Endocr. (Paris)30, 413–416 (1969)

    CAS  Google Scholar 

  • Sherrington, C. S.: In: A textbook of physiology (ed. M. Foster), 7th ed., vol. 3. London: Macmillan 1897

    Google Scholar 

  • Shioda, T., Nishida, S.: The innervation of the adrenal cortex. Arch. histol. jap.28, 23–43 (1967)

    CAS  PubMed  Google Scholar 

  • Smollich, A., Döcke, F.: Nervale Einflußnahme des Hypothalamus auf die Funktion der Nebennierenrinde. J. neuro-vise. Rel.31, 128–135 (1969)

    CAS  Google Scholar 

  • Stöhr, Ph. jr.: Zur Innervation der menschlichen Nebenniere. Z. Anat. Entwickl.-Gesch.104, 475–490 (1935)

    Google Scholar 

  • Sweat, M. L., Bryson, M. J.: Steroid 11 ß-oxygenation, ascorbic acid, epinephrine, and adrenochrome interrelations in the adrenal gland. Endocrinology76, 773–774 (1965)

    CAS  PubMed  Google Scholar 

  • Swinyard, C. A.: The innervation of the suprarenal glands. Anat. Rec.68, 417–429 (1937)

    Article  Google Scholar 

  • Unsicker, K.: Zur Innervation der Nebenniere vom Goldhamster. Eine fluoreszenz- und elektronenmikroskopische Studie. Z. Zellforsch.95, 608–619 (1969)

    Article  Google Scholar 

  • Unsicker, K.: On the innervation of the rat and pig adrenal cortex. Z. Zellforsch.116, 151–156 (1971)

    Article  CAS  PubMed  Google Scholar 

  • Unsicker, K.: Fine structure and innervation of the avian adrenal gland. II. Cholinergic innervation of adrenal chromaffin cells. Z. Zellforsch. (in press) (1973b)

  • Unsicker, K.: Fine structure and innervation of the avian adrenal gland. III. Non-cholinergic nerve fibres. Z. Zellforsch. (in press) (1973 c)

  • Unsicker, K.: Fine structure and innervation of the avian adrenal gland. IV. Fine structure of interrenal cells. Z. Zellforsch. (in press) (1973d)

  • Vogt, M.: Observations on some conditions affecting the rate of hormone output by the suprarenal cortex. J. Physiol. (Lond.)103, 317–332 (1944)

    CAS  Google Scholar 

  • Vogt, M.: In: Ciba Colloquia endocr. 8, 241–248 (1954). Quoted after: Vitamins and hormones, vol. XV. New York: Academic Press 1957

  • Wetzstein, R.: Elektronenmikroskopische Untersuchungen am Nebennierenmark von Maus, Meerschweinchen und Katze. Z. Zellforsch.46, 517–576 (1957)

    Article  CAS  PubMed  Google Scholar 

  • Wilkens, I.M.S.: The intrinsic innervation of the suprarenal gland. Acta anat. (Basel)46, 127–134 (1961)

    Google Scholar 

  • Willard, D. M.: The innervation of the adrenal glands of mammals. Quart. J. micr. Sci.78, 475–486 (1936)

    Google Scholar 

  • Yi-Chao, Pei-Chen, C., Hsiung-Sin, T., Yung-Kong, Y., Jen-Yü, S.: The effect of 5-hydroxytryptamine on adrenocortical function of rats. (Chinese). Acta physiol. Sinica28, 309–314 (1965)

    Google Scholar 

  • Zorgan, V. G.: A study of the serotonin action upon the adrenal cortex function. (Russian). Farmakol. i Toksikol.31, 292–295 (1968)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, University of Kiel, 2300, Kiel, FRG

    K. Unsicker

Authors
  1. K. Unsicker
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This work was supported by a grant from the “Deutsche Forschungsgemeinschaft” (Un 34/1).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Unsicker, K. Fine structure and innervation of the avian adrenal gland. Z.Zellforsch 146, 403–416 (1973). https://doi.org/10.1007/BF02346231

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02346231

Key words

Search

Navigation