Summary
The fluorescence histochemical method has been used to examine the adrenergic innervation of the proximal colon of the guinea-pig. Previous investigations have shown that the adrenergic fibres of the gastrointestinal tract arise from extrinsic ganglia. However, in this work it is shown that adrenergic nerve cells are found in the myenteric plexus of the proximal colon and that these cells provide varicose terminals about ganglion cells in the nodes of the plexus. About 75% of the nodes of the myenteric plexus in the proximal colon contain adrenergic cells. A few cells are also observed along the internodal strands. The cells have a cytoplasmic fluorescence, which is of different intensity in different cells, but there is no fluorescence of the nucleus. Processes can be traced from most cells and in some cases these are seen to become varicose. Interruption of extrinsic nerve pathways to the intestine causes a disappearance of the fluorescence reaction of the adrenergic terminals in the ileum, most of the distal colon and in the submucosal and perivascular plexuses of the proximal colon. In contrast, about 60% of the adrenergic terminals in the myenteric plexus of the proximal colon survive extrinsic denervation. From cell counts, it is estimated there are about 10000 adrenergic cells in the proximal colon.
Similar content being viewed by others
References
Andrew, A.: The origin of intramural ganglia. III. The “vagal” source of enteric ganglion cells. J. Anat. (Lond.) 107, 327–336 (1970).
Benmiloud, M., Euler, U. S. von: Effects of bretylium, reserpine, guanethidine and sympathetic denervation on the noradrenaline content of the rat submaxillary gland. Acta physiol. scand. 59, 34–42 (1963).
Bennett, T.: Studies on the avian gizzard: Histochemical analysis of the extrinsic and intrinsic innervation. Z. Zellforsch. 98, 188–201 (1969).
Birmingham, A. T.: Sympathetic denervation of the smooth muscle of the vas deferens. J. Physiol. (Lond.) 206, 645–661 (1970).
Campbell, G.: Autonomic nervous supply of effector tissues. In: Smooth Muscle, eds. E. Bülring, A. Brading, A. Jones, T. Tomita, p. 451–495. London: Arnold 1970.
Campenhout, E. van: Further experiments on the origin of the enteric nervous system in the chick. Physiol. Zool. 5, 333–353 (1932).
Castro, F. de: Recherches sur la dégénération et la régénération du système nerveux sympathique. Quelques observations sur la constitution des synapses dans les ganglions. Études anatomiques et physiologiques. Trav. Lab. Rech. Biol. Madrid 26, 357–456 (1930).
Cooper, T., Gilbert, J. W., Bloodwell, R. D., Crout, J. R.: Chronic extrinsic cardiac denervation by regional neural ablation. Circulat. Res. 9, 275–281 (1961).
—, Willman, V. L., Jellinek, M., Hanlon, C. R.: Heart autotransplantation: effect on myocardial catecholamines and histamine. Science 138, 40–41 (1962).
Corrodi, H., Jonsson, G.: The formaldehyde fluorescence method for the histochemical demonstration of biogenic monoamines. A review of the methodology. J. Histochem. Cytochem. 15, 65–78 (1967).
Costa, M., Furness, J. B.: Storage, uptake and synthesis of catecholamines in the intrinsic adrenergic neurons in the proximal colon of the guinea-pig. Z. Zellforsch. 220, (1971).
Costa, M., Furness, J. B., Gabella, G.: Catecholamine containing nerve cells in the mammalian myenteric plexus. Histochemie 25, 103–106 (1971).
- Gabella, G.: Adrenergic innervation of the alimentary canal. Z. Zellforsch. (in press) (1971).
Crema, A., Frigo, G., Mazzanti, L.: The time course of adrenergic fibre degeneration following extrinsic sympathectomy “a frigore” in the guinea-pig distal colon. Abstracts of 4th Int. Cong. Pharmacol. 131 (1969).
Dahlström, A. B., Zetterström, B. E. M.: Noradrenaline stores in nerve terminals of the spleen. Changes during hemorrhargic shock. Science 147, 1583–1585 (1965).
Dale, H. H.: Nomenclature of fibres in the autonomic nervous system and their effects. J. Physiol. (Lond.) 80, 10–11P (1933).
—: Pharmacology and nerve endings. Proc. roy. Soc. Med. 28, 319–332 (1935).
—: Natural chemical stimulators. Edinb. med. J. 45, 461–480 (1938).
Euler, U. S. von, Purkhold, A.: Effect of sympathetic denervation on the noradrenaline and adrenaline content of the spleen, kidney and salivary glands in the sheep. Acta physiol. scand. 24, 212–217 (1951).
Falck, B.: Observations on the possibilities of the cellular localisation of monoamines by a fluorescent method. Acta physiol. scand. 56, Suppl. 197, 1–26 (1962).
—, Mchedlishvili, G. J., Owman, C.: Histochemical demonstration of adrenergic nerves in cortex-pia of rabbit. Acta pharmacol. (Kbh.) 23, 133–142 (1965).
—, Rorsman, H.: Observation on the adrenergic innervation of the skin. Experientia (Basel) 19, 205–206 (1963).
Filogamo, G., Marchisio, P. C.: Choline acetyltransferase activity of rabbit ileum wall. The effects of extrinsic and intrinsic denervation and of combined experimental hypertrophy. Arch. int. Physiol. 78, 141–152 (1970).
—, Muti, R.: Á propos d'une technique de dénervation du canal alimentaire au moyen du froid. C. R. Ass. Anat. 141, 873–879 (1968).
Furness, J. B.: The presence of inhibitory nerve fibres in the colon after sympathetic denervation. Europ. J. Pharmacol. 6, 349–352 (1969).
—: The origin and distribution of adrenergic nerve fibres in guinea-pig colon. Histochemie 21, 295–306 (1970).
—: Secondary excitation of intestinal smooth muscle. Brit. J. Pharmacol. 41, 213–226 (1971).
Gabella, G., Costa, M.: Le fibre adrenergiche nel canale alimentare. G. Accad. Med. Torino 130, 1–12 (1967).
—: Adrenergic innervation of the intestinal smooth musculature. Experientia (Basel) 25, 395–396 (1969).
Gaskell, W. H.: The involuntary nervous system. London: Longmans, Green & Co. 1916.
Goodall, McC.: Studies of adrenaline and noradrenaline in mammalian hearts and supra renals. Acta physiol. scand. 24, Suppl. 85, 1–51 (1951).
Hamberger, B., Norberg, K.-A.: Studies on some systems of adrenergic synaptic terminals in the abdominal ganglia of the cat. Acta physiol. scand 65, 235–242 (1965a).
—: Adrenergic synaptic terminals and nerve cells in bladder ganglia of a cat. Int. J. Neuropharmacol. 4, 41–45 (1965b).
Hillarp, N. A.: Structure of the synapse and the peripheral innervation apparatus of the autonomic nervous system. Acta anat. (Basel), Suppl. 4, 1–153 (1946).
Hollands, B. C. S., Vanov, S.: Localization of catecholamines in visceral organs and ganglia of the rat, guinea-pig and rabbit. Brit. J. Pharmacol. 25, 307–316 (1965).
Irwin, D. A.: Anatomy of Auerbach's plexus. Amer. J. Anat. 49, 141–166 (1931).
Jacobowitz, D.: Histochemical studies of the autonomic innervation of the gut. J. Pharmacol. exp. Ther. 149, 358–364 (1965).
Johansson, B., Ljung, B., Malmfors, T., Olson, L.: Prejunctional supersensitivity in the rat portal vein as related to its pattern of innervation. Acta physiol. scand. 80, Suppl. 349, 5–16 (1970).
Kirpekar, S. M., Cervoni, P., Furchgott, R. F.: Catecholamine content of the cat nictitating membrane following procedures sensitizing it to norepinephrine. J. Pharmacol. exp. Ther. 135, 180–190 (1962).
Kuntz, A.: The role of the vagi in the development of the sympathetic nervous system. Anat. Anz. 35, 381–390 (1910a).
Kuntz, A.: The development of the sympathetic nervous system in mammals. J. comp. Neurol. 20, 211–258 (1910b).
—: The development of the sympathetic nervous system in man. J. comp. Neurol. 32, 173–229 (1920).
—: The autonomic nervous system. London: Baillere, Tindale & Cox. 1953.
—, Jacobs, M. W.: Components of periarterial extensions of celiac and mesenteric plexuses. Anat. Rec. 123, 509–520 (1955).
—, Moseley, R. L.: An experimental analysis of the pelvic autonomic ganglia in the cat. J. comp. Neurol. 64, 63–75 (1936).
Langley, J. N.: The autonomic nervous system. Brain 26, 1–26 (1903).
—: The autonomic nervous system. London: W. Hefter & Sons. 1921.
Lawrentjew, B. I.: Über die Erscheinungen der Degeneration und Regeneration im sympathischen Nervensystem. Z. mikr.-anat. Forsch. 2, 201–223 (1925).
Matsuo, H.: A contribution on the anatomy of Auerbach's plexus. Jap. J. med. Sci. Anat. 4, 417–428 (1937).
McKenna, O. C., Angelakos, E. T.: Adrenergic innervation of the canine kidney. Circulat. Res. 22, 345–354 (1968).
Mitchell, G. A. G.: Anatomy of the autonomic nervous system. Edinburgh: E. & S. Livingstone Ltd. 1953.
Mitchell, P. C.: On the intestinal tract of mammals. Trans. Zool. Soc. (Lond.) 17, 437–536 (1905).
Mohri, K., Ohgushi, N., Ikeda, M., Yamamoto, K., Tsunekawa, K., Fujiwara, M., Muryobayashi, T.: Histochemical demonstration of adrenergic fibres in the smooth muscle layer of media of arteries supplying abdominal organs. Arch. Jap. Chir. 38, 236–248 (1969).
Norberg, K. A.: Adrenergic innervation of the intestinal wall studied by fluorescence microscopy. Int. J. Neuropharmacol. 3, 379–382 (1964).
—, Risley, P. L., Ungerstedt, U.: Adrenergic innervation of the male reproductive ducts in some mammals. II. The effects of vasectomy and castration. Experientia (Basel) 23, 392–396 (1967).
Ohkubo, K.: Studien über das intramurale Nervensystem des Verdauungskanals. II. Die Plexus myentericus und Plexus subserosus des Meerschweinchens. Jap. J. med. Sci. Anat. 6, 21–37 (1937).
Owman, C.: Sympathetic nerves probably storing two types of monoamines in the rat pineal gland. Int. J. Neuropharmacol. 2, 105–112 (1964).
—, Rosengren, E., Sjöberg, N. O.: Origin of the adrenegic innervation to the female genital tract of the rabbit. Life Sci. 5, 1389–1396 (1966).
Read, J. B., Burnstock, G.: Comparative histochemical studies of adrenergic nerves in the enteric plexuses of vertebrate large intestine. Comp. Biochem. Physiol. 27, 505–517 (1968).
Rintoul, J. R.: The comparative morphology of the enteric nerve plexuses. Ph. D. thesis, University of St. Andrews, 1960.
Ritzén, M.: Cytochemical identification and quantitation of biogenic monoamines. Thesis Institute for Medical Cell Research and Genetics, Medical Nobel Institute, Karolinska Institute, 1967.
Rosengren, E., Sjöberg, N. O.: The adrenergic nerve supply to the female reproductive tract of the cat. Amer. J. Anat. 121, 271–284 (1967).
Sano, Y., Yoshikawa, H., Ochi, J.: Intraneuroplasmic transport of catecholamines as studied by fluorescence and electronmicroscopy. Arch. Histol. Jap. 32, 329–345 (1970).
Schofield, G. C.: Anatomy of muscular and neural tissues in the alimentary canal. In: Handbook of physiology, edit. by Code, C. F. Washington: American Physiol. Soc. 1968.
Sedvall, G.: Noradrenaline storage in skeletal muscle. Acta physiol. scand. 60, 39–50 (1964).
Sidman, R. L., Perkins, M., Weiner, N.: Noradrenaline and adrenaline content of adipose tissue. Nature (Lond.) 93, 36–37 (1962).
Silva, D. G., Ross, G., Osborne, L. W.: Adrenergic innervation of the ileum of the cat. Amer. J. Physiol. 220, 347–352 (1971).
Sjöberg, N. O.: The adrenergic transmitter of the female reproductive tract: Distribution and functional changes. Acta physiol. scand. 72, Suppl. 305, 1–32 (1968).
Stewart, F. W.: The development of the cranial sympathetic ganglia in the rat. J. comp. Neurol. 31, 163–217 (1920).
Tafuri, W. L.: Auerbach's plexus in the guinea-pig. 1. A quantitative study of the ganglia and nerve cells in the ileum, caecum and colon. Acta anat. (Basel) 31, 522–530 (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).
Tsunekawa, K., Ohgushi, N., Ohsumi, K., Sato, M., Mohri, K., Yamamoto, K., Ikeda, M., Kimura, T.: Fluorescent histochemical studies on the adrenergic innervation of the blood vessels. Saishin Igaku 25, 2068–2089 (1970).
Waterson, J. G., Smale, D. E.: Location of noradrenergic structures in the central artery of the rabbit ear. Aust. J. exp. Biol. med. Sci. 45, 301–308 (1967).
Wegmann, A., Chiba, C., Chrysohou, A., Bing, R. J.: Catecholamines in homologous heart grafts. Proc. Soc. exp. Biol. (N.Y.) 109, 543–545 (1962).
Yntema, C. L., Hammond, W. S.: The origin of intrinsic autonomic ganglia of trunk viscera from vagal neural crest in the chick embryo. J. comp. Neurol. 101, 515–541 (1954).
Yoshikawa, H.: An experimental study on the sympathetic neuron chains using the fluorescence method for biogenic amines. Arch. histol. jap. 31, 459–509 (1970).
Author information
Authors and Affiliations
Additional information
This work was supported by grants from the Australian Research Grants Committee and the National Health and Medical Research Council. We thank Prof. G. Burnstock for his support and for his critical reading of the manuscript. We also thank Dr. R. O. Jones for his comments on the manuscript.
Rights and permissions
About this article
Cite this article
Furness, J.B., Costa, M. Morphology and distribution of intrinsic adrenergic neurones in the proximal colon of the guinea-pig. Z. Zellforsch. 120, 346–363 (1971). https://doi.org/10.1007/BF00324897
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00324897