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Morphology and distribution of intrinsic adrenergic neurones in the proximal colon of the guinea-pig

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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.

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References

  • Andrew, A.: The origin of intramural ganglia. III. The “vagal” source of enteric ganglion cells. J. Anat. (Lond.) 107, 327–336 (1970).

    Google Scholar 

  • 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).

    Google Scholar 

  • Bennett, T.: Studies on the avian gizzard: Histochemical analysis of the extrinsic and intrinsic innervation. Z. Zellforsch. 98, 188–201 (1969).

    Google Scholar 

  • Birmingham, A. T.: Sympathetic denervation of the smooth muscle of the vas deferens. J. Physiol. (Lond.) 206, 645–661 (1970).

    Google Scholar 

  • 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.

    Google Scholar 

  • Campenhout, E. van: Further experiments on the origin of the enteric nervous system in the chick. Physiol. Zool. 5, 333–353 (1932).

    Google Scholar 

  • 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).

    Google Scholar 

  • 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).

    Google Scholar 

  • —, Willman, V. L., Jellinek, M., Hanlon, C. R.: Heart autotransplantation: effect on myocardial catecholamines and histamine. Science 138, 40–41 (1962).

    Google Scholar 

  • 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).

    Google Scholar 

  • 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).

    Google Scholar 

  • - 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).

    Google Scholar 

  • Dale, H. H.: Nomenclature of fibres in the autonomic nervous system and their effects. J. Physiol. (Lond.) 80, 10–11P (1933).

    Google Scholar 

  • —: Pharmacology and nerve endings. Proc. roy. Soc. Med. 28, 319–332 (1935).

    Google Scholar 

  • —: Natural chemical stimulators. Edinb. med. J. 45, 461–480 (1938).

    Google Scholar 

  • 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).

    Google Scholar 

  • 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).

    Google Scholar 

  • —, Mchedlishvili, G. J., Owman, C.: Histochemical demonstration of adrenergic nerves in cortex-pia of rabbit. Acta pharmacol. (Kbh.) 23, 133–142 (1965).

    Google Scholar 

  • —, Rorsman, H.: Observation on the adrenergic innervation of the skin. Experientia (Basel) 19, 205–206 (1963).

    Google Scholar 

  • 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).

    Google Scholar 

  • —, Muti, R.: Á propos d'une technique de dénervation du canal alimentaire au moyen du froid. C. R. Ass. Anat. 141, 873–879 (1968).

    Google Scholar 

  • Furness, J. B.: The presence of inhibitory nerve fibres in the colon after sympathetic denervation. Europ. J. Pharmacol. 6, 349–352 (1969).

    Google Scholar 

  • —: The origin and distribution of adrenergic nerve fibres in guinea-pig colon. Histochemie 21, 295–306 (1970).

    Google Scholar 

  • —: Secondary excitation of intestinal smooth muscle. Brit. J. Pharmacol. 41, 213–226 (1971).

    Google Scholar 

  • Gabella, G., Costa, M.: Le fibre adrenergiche nel canale alimentare. G. Accad. Med. Torino 130, 1–12 (1967).

    Google Scholar 

  • —: Adrenergic innervation of the intestinal smooth musculature. Experientia (Basel) 25, 395–396 (1969).

    Google Scholar 

  • Gaskell, W. H.: The involuntary nervous system. London: Longmans, Green & Co. 1916.

    Google Scholar 

  • Goodall, McC.: Studies of adrenaline and noradrenaline in mammalian hearts and supra renals. Acta physiol. scand. 24, Suppl. 85, 1–51 (1951).

    Google Scholar 

  • 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).

    Google Scholar 

  • —: Adrenergic synaptic terminals and nerve cells in bladder ganglia of a cat. Int. J. Neuropharmacol. 4, 41–45 (1965b).

    Google Scholar 

  • 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).

    Google Scholar 

  • 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).

    Google Scholar 

  • Irwin, D. A.: Anatomy of Auerbach's plexus. Amer. J. Anat. 49, 141–166 (1931).

    Google Scholar 

  • Jacobowitz, D.: Histochemical studies of the autonomic innervation of the gut. J. Pharmacol. exp. Ther. 149, 358–364 (1965).

    Google Scholar 

  • 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).

    Google Scholar 

  • 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).

    Google Scholar 

  • Kuntz, A.: The role of the vagi in the development of the sympathetic nervous system. Anat. Anz. 35, 381–390 (1910a).

    Google Scholar 

  • Kuntz, A.: The development of the sympathetic nervous system in mammals. J. comp. Neurol. 20, 211–258 (1910b).

    Google Scholar 

  • —: The development of the sympathetic nervous system in man. J. comp. Neurol. 32, 173–229 (1920).

    Google Scholar 

  • —: The autonomic nervous system. London: Baillere, Tindale & Cox. 1953.

    Google Scholar 

  • —, Jacobs, M. W.: Components of periarterial extensions of celiac and mesenteric plexuses. Anat. Rec. 123, 509–520 (1955).

    Google Scholar 

  • —, Moseley, R. L.: An experimental analysis of the pelvic autonomic ganglia in the cat. J. comp. Neurol. 64, 63–75 (1936).

    Google Scholar 

  • Langley, J. N.: The autonomic nervous system. Brain 26, 1–26 (1903).

    Google Scholar 

  • —: The autonomic nervous system. London: W. Hefter & Sons. 1921.

    Google Scholar 

  • Lawrentjew, B. I.: Über die Erscheinungen der Degeneration und Regeneration im sympathischen Nervensystem. Z. mikr.-anat. Forsch. 2, 201–223 (1925).

    Google Scholar 

  • Matsuo, H.: A contribution on the anatomy of Auerbach's plexus. Jap. J. med. Sci. Anat. 4, 417–428 (1937).

    Google Scholar 

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

    Google Scholar 

  • Mitchell, G. A. G.: Anatomy of the autonomic nervous system. Edinburgh: E. & S. Livingstone Ltd. 1953.

    Google Scholar 

  • Mitchell, P. C.: On the intestinal tract of mammals. Trans. Zool. Soc. (Lond.) 17, 437–536 (1905).

    Google Scholar 

  • 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).

    Google Scholar 

  • Norberg, K. A.: Adrenergic innervation of the intestinal wall studied by fluorescence microscopy. Int. J. Neuropharmacol. 3, 379–382 (1964).

    Google Scholar 

  • —, 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).

    Google Scholar 

  • 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).

    Google Scholar 

  • Owman, C.: Sympathetic nerves probably storing two types of monoamines in the rat pineal gland. Int. J. Neuropharmacol. 2, 105–112 (1964).

    Google Scholar 

  • —, Rosengren, E., Sjöberg, N. O.: Origin of the adrenegic innervation to the female genital tract of the rabbit. Life Sci. 5, 1389–1396 (1966).

    Google Scholar 

  • 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).

    Google Scholar 

  • 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).

    Google Scholar 

  • Sano, Y., Yoshikawa, H., Ochi, J.: Intraneuroplasmic transport of catecholamines as studied by fluorescence and electronmicroscopy. Arch. Histol. Jap. 32, 329–345 (1970).

    Google Scholar 

  • 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.

    Google Scholar 

  • Sedvall, G.: Noradrenaline storage in skeletal muscle. Acta physiol. scand. 60, 39–50 (1964).

    Google Scholar 

  • Sidman, R. L., Perkins, M., Weiner, N.: Noradrenaline and adrenaline content of adipose tissue. Nature (Lond.) 93, 36–37 (1962).

    Google Scholar 

  • Silva, D. G., Ross, G., Osborne, L. W.: Adrenergic innervation of the ileum of the cat. Amer. J. Physiol. 220, 347–352 (1971).

    Google Scholar 

  • Sjöberg, N. O.: The adrenergic transmitter of the female reproductive tract: Distribution and functional changes. Acta physiol. scand. 72, Suppl. 305, 1–32 (1968).

    Google Scholar 

  • Stewart, F. W.: The development of the cranial sympathetic ganglia in the rat. J. comp. Neurol. 31, 163–217 (1920).

    Google Scholar 

  • 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).

    Google Scholar 

  • 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).

    Google Scholar 

  • 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).

    Google Scholar 

  • 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).

    Google Scholar 

  • Wegmann, A., Chiba, C., Chrysohou, A., Bing, R. J.: Catecholamines in homologous heart grafts. Proc. Soc. exp. Biol. (N.Y.) 109, 543–545 (1962).

    Google Scholar 

  • 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).

    Google Scholar 

  • Yoshikawa, H.: An experimental study on the sympathetic neuron chains using the fluorescence method for biogenic amines. Arch. histol. jap. 31, 459–509 (1970).

    Google Scholar 

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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.

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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

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