Summary
Ganglia from Auerbach's plexus of the large intestine (caecum, appendix vermiformis, colon transversum and rectum) in man, rhesus monkey and guinea-pig are composed of nerve cells and their processes, typical Schwann cells and a vast neuropil. The neuropil consists of dendrites and axons of intrinsic nerve cell perikarya and axons of extrinsic neurons. Axonal profiles in large nerve fibre bundles are of uniform size and appearance, embedded in infoldings of Schwann cell cytoplasm and contain occasional large granular vesicles, mitochondria and neurotubules. Preterminal axons widen into vesicle filled varicosities, some of which establish synaptic contact with intrinsic nerve cell bodies.
At least three different types of neuronal processes can be distinguished in the myenteric neuropil according to the size, appearance and commutual proportion of vesicles present in axonal varicosities, and their ability to accumulate exogenous 5- and 6-hydroxydopamine and 5-hydroxydopa: 1. Axonal enlargements containing a major population of small electron lucent “synaptic” vesicles (350–600 Å in diameter) together with a small number of membrane-bound, opaque granules (800–1,100 Å). These profiles have been identified as “cholinergic” axons. The boutons establish synaptic contacts with dendritic processes of intrinsic nerve cell bodies; membrane specializations are found at the preand postsynaptic sites. 2. Axonal beads of sometimes very large diameter, containing an approximately equal amount of large granular vesicles (850–1,600 Å) and small, electron lucent or faintly opaque vesicles (400–600 Å). The granular core of the large vesicles is of medium electron density and may either fill the entire vesicle or is separated from the limiting membrane by a more or less clear interspace. The fibres probably belong to intrinsic neurons, and because of the similarity of the large, membrane-bound vesicles with neurosecretory elementary granules, they have been designated “p-type fibres” (polypeptide fibres). The granular core of the vesicles in these fibres becomes more electron dense after treatment with 5-OH-dopa. The accumulation of an amine precursor analogue in combination with a possible storage of a polypeptide substance (or an ATP-like substance) resembles the situation in several diffusely distributed endocrine cell systems. 3. Varicosities of axons equipped with small (400–600 Å) empty or sometimes granular vesicles, medium sized (500–900 Å) vesicles with highly electron dense cores and occasional large (900–1,300 Å) granular vesicles. Pretreatment with 5-OH-dopamine increases the electron density in almost all medium-sized granular vesicles and some of the large granular vesicles; an osmiophilic core develops in some small vesicles. 6-hydroxydopamine results in degenerative changes in the varicosities of this type of neurons. Concomitantly, both catecholamine analogues markedly reduce neuronal noradrenaline in the large intestine, as demonstrated by fluorescence histochemistry and in fluorimetric determinations. The ultrastructural features of these varicosities and their reaction to 5- and 6-OH-dopamine indicate that they belong to adrenergic, sympathetic nerves. No membrane specializations could be detected at sites of close contact of the adrenergic boutons with dendrites and cell bodies of intrinsic nerve cells.
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References
Ambache, N., Freeman, M. A.: Atropine-resistant longitudinal muscle spasms due to excitation of non-oholinergic neurons in Auerbach's plexus. J. Physiol (Lond.) 199, 705–727 (1969).
Aures, D., Hakanson, R., Owman, Ch.: Formation and storage of amines in endocrine cells of gastric mucosa. J. Neurovisc. Rel., in press (1970).
Bargmann, W., Lindner, E., Andres, K. H.: Über Synapsen an endokrinen Epithelzellen und die Definition sekretorischer Neurone. Z. Zellforsch. 77, 282–298 (1967).
Baumgarten, H. G.: Vorkommen und Verteilung adrenerger Nervenfasern im Darm der Schleie (Tinca vulgaris Cuv). Z. Zellforsch. 76, 248–259 (1967).
—: Über die Verteilung von Catecholaminen im Darm des Menschen. Z. Zellforsch. 83, 133–146 (1967).
- Die Verteilung von Noradrenalin, Dopamin und 5-Hydroxytryptamin im Zentralnervensystem von Lampetra fluviatilis; ein Beitrag zur Frage des Vorkommens monoaminerger Neuronensysteme im Gehirn von einfachen Wirbeltieren. (To be published 1970.)
—, 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).
—, Lange, W.: Adrenergic innervation of the oesophagus in the cat (Felis domestica) and rhesus monkey (Macacus rhesus). Z. Zellforsch. 95, 529–545 (1969).
—: Extrinsic adrenergic innervation of the extrahepatic biliary duct system in guineapigs, cats and rhesus monkeys. Z. Zellforsch. 100, 606–615 (1969).
Bennett, M. R., Burnstock, G., Holman, M. E.: Transmission from perivascular inhibitory nerves to the smooth muscle of the guinea-pig taenia coli. J. Physiol. (Lond) 182, 527–540 (1969).
—, Rogers, D. C.: A study of the innervation of the taenia coli. J. Cell Biol. 33, 573–596 (1967).
Bertler, A., Carlsson, A., Rosengren, E., Waldeck, B.: A method for the fluorimetric determination of adrenaline, noradrenaline and dopamine in tissues. Kungl. Fysiogr. Sällsk. Lund Förh. 28, 121–123 (1958).
Burnstock, G.: Evolution of the autonomic innervation of visceral and cardiovascular systems in vertebrates. Pharmacol. Rev. 21, 247–324 (1969).
—, Campbell, G., Rand, M. J.: The inhibitory innervation of the taenia of the guinea-pig caecum. J. Physiol. (Lond.) 182, 504–526 (1966).
—, Robinson, P. M.: Localization of catecholamines and acetylcholinesterase in autonomic nerves. Circulat. Res. 20 and 21, Suppl. III, p. 43–53 (1967).
Campbell, G., Burnstock, G.: Comparative physiology of gastrointestinal motility. In: Code (ed.) Handbook of Physiology, vol. IV, 6, p. 2213–2266. Baltimore: Williams & Wilkins Company 1968.
Cottrell, G. A., Laverack, M. S.: Invertebrate pharmacology. Ann. Rev. Pharmacol. 8, 273–298 (1968).
Devine, C. E.: The fine structure of vascular axons after treatment with 6-hydroxydopamine. Proc. Univ. Otago med. School 47, 4–6 (1969).
Euler, U. S. v., Lishajko, F.: A specific kind of noradrenaline granules in the vesicular gland and the vas deferens of the bull. Life Sci. 5, 687–691 (1966).
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).
—, Sjöstrand, N. O.: Peripherally located adrenergic neurons innervating the vas deferens and the seminal vesicle of the guinea-pig. Experientia (Basel) 21, 98–100 (1965).
Furness, J. B.: The presence of inhibitory nerves in the colon after sympathetic denervation. Europ. J. Pharmacol. 6, 349–352 (1969).
Gershon, M. D.: Inhibition of gastrointestinal movement by sympathetic nerve stimulation: The site of action. J. Physiol. (Lond.) 189, 317–327 (1967).
—, Drakontides, A. B., Ross, L. L.: Serotonin: Synthesis and release from myenteric plexus of the mouse intestine. Science 149, 197–199 (1965).
—, Ross, L. L.: Radioisotopic studies of the binding, exchange, and distribution of 5-hydroxytryptamine synthesized from its radioactive precursor. J. Physiol. (Lond.) 186, 451–476 (1966).
Häggendal, J.: An improved method for fluorimetric determination of small amounts of adrenaline and noradrenaline in plasma and tissues. Acta physiol. scand. 59, 242–254 (1963).
Haeusler, G., Haefely, W., Thoenen, H.: Chemical sympathectomy of the cat with 6-hydroxydopamine. J. Pharmacol. exp. Ther. 170, 50–61 (1969).
Hager, A.: Die feinere Cytologie und Cytopathologie des Nervensystems. Veröffentl. a. d. Morphol. Pathol., 67. Stuttgart: Gustav Fischer 1964.
—, Tafuri, W. L.: Elektronenoptischer Nachweis sogenannter neurosekretorischer Elementargranula in marklosen Nervenfasern des Plexus myentericus (Auerbach) des Meerschweinchens. Naturwissenschaften 46, 332–333 (1959).
—: Elektronenmikroskopische Untersuchungen über die Feinstruktur des Plexus myentericus (Auerbach) im Colon des Meerschweinchens (Cavia Cobaja). Arch. Psychiat. 199, 437–471 (1959).
Iversen, L. L., Neal, M. J.: Subcellular distribution of endogenous and (3H)-GABA in rat cerebral cortex. Brit. J. Pharmacol. 36, 206 P (1969).
Kottegoda, S. R.: An analysis of possible nervous mechanisms involved in peristaltic reflex. J. Physiol. (Lond.) 200, 687–712 (1969).
Langley, I. N.: The autonomic nervous system. Brain 26, 1–26 (1903).
Laverty, R., Phelan, E. L.: Effects of 6-hydroxydopamine on noradrenaline storage and uptake in the rat. Proc. Univ. Otago med. School 47, 18–19 (1969).
—, Sharman, D. F., Vogt, M.: Action of 2,4,5-trihydroxy-phenylethylamine on the storage and release of noradrenaline. Brit. J. Pharmacol. 24, 549–560 (1965).
Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).
Malmfors, T., Sachs, Ch.: Degeneration of adrenergic nerves produced by 6-hydroxydopamine. Europ. J. Pharmacol. 3, 89–92 (1968).
Norberg, K. A.: Adrenergic innervation of the intestinal wall studied by fluorescence microscopy. Int. J. Neuropharmacol. 3, 379–382 (1964).
—: Transmitter histochemistry of the sympathetic adrenergic nervous system. Brain Res. 5, 125–170 (1967).
Obata, K., Takeda, T.: Release of gamma-aminobutyric acid into the fourth ventricle induced by stimulation of the cat's cerebellum. J. Neurochem. 16, 1043–1048 (1969).
Owman, Ch., Sjöberg, N. O.: Difference in rate of depletion and recovery of noradrenaline in “short” and “long” sympathetic nerves after reserpine treatment. Life Sci. 6, 2549–2556 (1967).
Paton, W. D. M.: Cholinergic transmission and acetylcholine output. Canad. J. Biochem. 41, 2673–2653 (1963).
Paton, W. D. M., Vizi, E. S.: The inhibitory action of noradrenaline and adrenaline on acetyloholine output by guinea-pig ileum longitudinal muscle strips. Brit. J. Pharmacol. 35, 10–28 (1969).
Pearse, A. G. E.: 5-Hydroxytryptophane uptake by dog thyroid “C” cells, and its possible significance in polypeptide hormone production. Nature (Lond.) 211, 598–600 (1966).
—: Cytochemical contributions to the functional cytology of polypeptide production (the APUD cells). In: Third International Congr. of Histochemistry and Cytochemistry. Summary-Reports, p. 198–199. Berlin-Heidelberg-New York: Springer 1968.
Pick, J., Lemos, C. de, Ciannella, A.: Pine structure of nerve terminals in the human gut. Anat. Rec. 159, 131–146 (1967).
Porter, C.C., Totaro, J. A., Burcin, A.: The relationship between radioactivity and norepinephrine concentrations in the brains and hearts of mice following administration of labelled methyldopa or 6-hydroxydopamine. J. Pharmacol. exp. Ther. 150, 17–22 (1965).
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).
Reynolds, E. S.: The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).
Richardson, K. C.: Studies on the structure of autonomic nerves in the small intestine correlating the silver-impregnated image in light microscopy with the permanganatefixed ultrastructure in electron microscope. J. Anat. (Lond.) 94, 457–472 (1960).
Scharrer, B., Weitzman, M.: Current problems in invertebrate neuroseeretion. In: Aspects of neuroendocrinology (Vth Symposium of Neuroseeretion, Kiel 1969). Berlin-Heidelberg-New York: Springer 1970 (in press).
Schofield, G. C.: Experimental studies on the myenteric plexus in mammals. J. comp. Neurol. 119, 159–186 (1962).
—: Anatomy of muscular and neural tissues in the elementary canal. In: C. F. Code (ed.), Handbook of physiology, vol. IV, 6, p. 1579–1627. Baltimore: Williams & Wilkins Co. 1968.
Sjöstrand, N. O., Swedin, G.: Effect of reserpine on the noradrenaline content of the vas deferens and the seminal vesicles compared with the submaxillary gland and the heart of the rat. Acta physiol. scand. 72, 370–377 (1968).
Taxi, J.: Sur la structure du Plexus d'Auerbach de la souris étudié au microscope électronique. C. R. Acad. Sic. (Paris) 246, 1922–1925 (1958).
—, Droz, B.: Etude de l'incorporation de noradrenaline-3H (NA-3H) et de 5-hydroxytryptophane-3H (5-HTP-3H) dans les fibres nerveuses de canal déférent et de l'intestin. C. R. Acad. Sci. (Paris) 263, 1237–1240 (1966).
Thaemert, J. C.: The ultrastructure and disposition of vesiculated nerve processes in smooth muscle. J. Cell Biol. 16, 361–377 (1963).
Thoenen, H.: Bildung und funktionelle Bedeutung adrenerger Ersatztransmitter. Experimentelle Medizin, Pathologie und Klinik, Bd. 27. Berlin-Heidelberg-New York: Springer 1969.
—, Haefely, W., Gey, K. F., Huerlimann, A.: Diminished effect of sympathetic nerve stimulation in cats pretreated with 5-hydroxydopa; formation and liberation of false adrenergic transmitters. Naunyn-Schmiedbergs Arch. Pharmak. exp. Path. 259, 17–33 (1967).
—, Huerlimann, A., Haefely, W.: Mechanisms of amphetamine accumulation in the isolated perfused heart of the rat. J. Pharm. Pharmacol. 20, 1–9 (1968).
—, 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).
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 (1967).
—: Various types of amine-storing vesicles in peripheral adrenergic nerve terminals. Experientia (Basel) 24, 484–486 (1968).
Wartenberg, H., Baumgarten, H. G.: Elektronenmikroskopische Untersuchungen zur Frage der photosensorischen und sekretorischen Funktion des Pinealorgans von Lacerta viridis und Lacerta muralis. Z. Anat. Entwickl.-Gesch. 127, 99–120 (1968).
—: Über die elektronenmikroskopische Identifizierung von noradrenergen Nerven durch 5-Hydroxydopamin und 5-Hydroxydopa im Pinealorgan der Eidechse (Lacerta muralis). Z. Zellforsch. 94, 252–260 (1969).
Yamamoto, T.: Electron microscope investigation on the relationship between the smooth muscle cells of the processus vermiformis and the autonomic peripheral nerves. Acta neuroveg. (Wien) 21, 406–425 (1960.
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Supported by grants from the Deutsche Forschungsgemeinschaft.
Supported by a grant from Albert Pahlsson's Foundation, Sweden. The work was carried out within a research organization sponsored by the Swedish Medical Research Council (projects No. B70-14X-1007-05B, B70-14X-712-05, and B70-14X-56-06).
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Baumgarten, H.G., Holstein, A.F. & Owman, C. 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). https://doi.org/10.1007/BF00335780
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DOI: https://doi.org/10.1007/BF00335780