Skip to main content
Log in

The fine structure of the submucous plexus of the guinea-pig ileum. II. Description and analysis of vesiculated nerve profiles

  • Published:
Journal of Neurocytology

Summary

A fine structural study has been made of the vesiculated nerve profiles of the submucous plexus of both normally innervated and extrinsically denervated segments of guinea-pig ileum.

Two types of nerve profiles could be readily distinguished by their vesicular content after conventional fixation. The first type, comprising 5% of all intrinsic profiles, consisted of predominantly small vesicles containing electron dense material which usually formed a ring around the inner face of the vesicular membrane but sometimes partially or completely filled the vesicle. These profiles, termed ring-vesicle-containing profiles, remained after extrinsic denervation and their vesicular content did not change following injection of reserpine or 5-hydroxydopamine. Thus ring-vesicle-containing profiles are not noradrenergic. Profiles which were positive for the uranaffin method were similar in morphology and frequency of occurrence to ring-vesicle-containing profiles, although it is not possible to say that they are the same.

The second type of profile, comprising 95% of all intrinsic profiles, contained varying proportions of large granular and small clear vesicles. These heterogeneous profiles were present in both normally innervated and extrinsically denervated tissue. Their vesicular content did not change following injection of reserpine, however, some profiles of this type in normally innervated, but not in extrinsically denervated, intestine contained electron dense deposits after injection of 5-hydroxydopamine. This means that noradrenergic profiles are a subpopulation of the heterogeneous profiles in normally innervated tissue. Analysis of intrinsic heterogeneous profiles showed that the proportion and packing density of large granular vesicles formed continuous distributions which did not provide any basis for further subdivision of this type of profile. Ring-vesicle-containing and heterogeneous profiles often formed synapses with neuronal cell bodies and processes.

Two rarer types of profiles were also seen. The first type contained mainly small flattened vesicles which took up 5-hydroxydopamine and was not present in extrinsically denervated tissue. This type, like the group described above, is considered to be noradrenergic. The second rare type contained large numbers of lysosome-like dense bodies and vesicles of different sizes and content and was seen in both normally innervated and denervated tissue. This type probably represents spontaneously degenerating nerve profiles.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Baumgarten, H. G., Holstein, A.-F. &Owman, Ch. (1970) 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.Zeitschrift für Zellforschung und mikroskopische Anatomie 106, 376–97.

    Google Scholar 

  • Bloom, F. E. (1970) The fine structural localization of biogenic monoamines in nervous tissue.International Review of Neurobiology 13, 27–66.

    Google Scholar 

  • Bloom, F. E. (1972a) Electron microscopy of catecholamine-containing structures. InHandbook of Experimental Pharmacology Vol. 33 (edited byBlaschko, H. &Muscholl, E.), pp. 46–78. Berlin: Springer-Verlag.

    Google Scholar 

  • Bloom, F. E. (1972b) Localization of neurotransmitters by electron microscopy.Research Publications of the Association for Research in Nervous and Mental Disease 50, 25–57.

    Google Scholar 

  • Bryant, M. G., Polak, J. M., Modlin, I., Bloom, S. R., Albuquerque, R. H. &Pearse, A. G. E. (1976) Possible dual role for vasoactive intestinal peptide as gastrointestinal hormone and neurotransmitter substance.The Lancet (i) May, 991–3.

    Google Scholar 

  • Clementi, F. (1965) Modifications ultrastructurelles provoquées par quelques médicaments sur les terminaisons nerveuses adrenergiques et sur la medullaire surrénale.Experientia 21, 171–2.

    Google Scholar 

  • Cook, R. D. &Burnstock, G. (1976) The ultrastructure of Auerbach's plexus in the guinea-pig. I. Neuronal elements.Journal of Neurocytology 5, 171–94.

    Google Scholar 

  • Costa, M., Cuello, A. C., Furness, J. B. &Franco, R. (1980) Distribution of enteric neurons showing immunoreactivity for substance P in the guinea-pig ileum.Neuroscience 5, 323–31.

    Google Scholar 

  • Costa, M. &Furness, J. B. (1971) Storage, uptake and synthesis of catecholamines in the intrinsic adrenergic neurones in the proximal colon of the guinea-pig.Zeitschrift für Zellforschung und microskopische Anatomie 120, 364–85.

    Google Scholar 

  • Costa, M., Furness, J. B., Llewellyn-Smith, I. J. &Cuello, A. C. (1981) Projections of substance P neurons within the guinea-pig small intestine.Neuroscience 6, 411–24.

    Google Scholar 

  • Costa, M., Furness, J. B. &McLean, J. R. (1976) The presence of aromatic I-amino acid decarboxylase in certain intestinal nerve cells.Histochemistry 48, 129–43.

    Google Scholar 

  • Couteaux, R. (1960) Motor end plate structure. InStructure and Function of Muscle Vol. 1 (edited byBourne, G. H.), pp. 337–80. New York: Academic Press.

    Google Scholar 

  • Daniel, E. E., Taylor, G. S., Daniel, V. P. &Holman, M. E. (1977) Can nonadrenergic inhibitory varicosities be identified structurally.Canadian Journal of Physiology and Pharmacology 55, 243–50.

    Google Scholar 

  • Dockray, G. J., Vaillant, C. &Walsh, J. H. (1979) The neuronal origin of bombesin-like immunoreactivity in the rat gastrointestinal tract.Neuroscience 4, 1561–8.

    Google Scholar 

  • Fehér, E. &Csányi, K. (1974) Ultra-architectonics of the neural plexus in chronically isolated small intestine.Acta anatomica 90, 617–28.

    Google Scholar 

  • Fehér, E., Csányi, K. &Vajda, J. (1974) Comparative electron microscopic studies on the preterminal and terminal fibres of the nerve plexus of the small intestine, employing different fixation methods.Acta morphologica Academiae Scientiarum hungaricae 22, 147–59.

    Google Scholar 

  • Furness, J. B. &Costa, M. (1971) Morphology and distribution of intrinsic adrenergic neurones in the proximal colon of the guinea-pig.Zeitschrift für Zellforschung und mikroskopische Anatomie 120, 346–63.

    Google Scholar 

  • Furness, J. B. &Costa, M. (1978) Distribution of intrinsic nerve cell bodies and axons which take up aromatic amines and their precursors in the small intestine of the guinea-pig.Cell and Tissue Research 188, 527–43.

    Google Scholar 

  • Furness, J. B. &Costa, M. (1980) Types of nerves in the enteric nervous system.Neuroscience 5, 1–20.

    Google Scholar 

  • Furness, J. B., Costa, M. &Freeman, C. G. (1979) Absence of tyrosine hydroxylase activity and dopamine β-hydroxylase immunoreactivity in intrinsic nerves of the guinea-pig ileum.Neuroscience 4, 305–10.

    Google Scholar 

  • Gabella, G. (1971) Synapses of adrenergic fibres.Experientia 27, 280–1.

    Google Scholar 

  • Gabella, G. (1972) Fine structure of the myenteric plexus in the guinea-pig ileum.Journal of Anatomy 111, 69–97.

    Google Scholar 

  • Gabella, G. (1976)Structure of the Autonomic Nervous System. London: Chapman and Hall.

    Google Scholar 

  • Gabella, G. (1979) Innervation of the gastrointestinal tract.International Review of Cytology 59, 129–93.

    Google Scholar 

  • Gershon, M. D., Dreyfus, C. F., Pickel, V. M., Joh, T. H. &Reis, D. J. (1977) Serotonergic neurons in the peripheral nervous system: identification in gut by immunohistochemical localization of tryptophan hydroxylase.Proceedings of the National Academy of Sciences (USA) 74, 3086–9.

    Google Scholar 

  • Gibbins, I. L. (1980) Ultrastructural characterization of peripheral nonadrenergic autonomic nerves.Micron 11, 453–4.

    Google Scholar 

  • Grillo, M. A. &Palay, S. L. (1962) Granule-containing vesicles in the autonomic nervous system. InElectron Microscopy Vol. 2 (edited byBreese, S. S., Jr), p. U-1. New York: Academic Press.

    Google Scholar 

  • Hirst, G. D. S. &McKirdy, H. C. (1975) Synaptic potentials recorded from neurones of the submucous plexus of guinea-pig small intestine.Journal of Physiology 249, 369–85.

    Google Scholar 

  • Hökfelt, T. (1968)In vitro studies on central and peripheral monoamine neurons at the ultrastructural level.Zeitschrift für Zellforschung und mikroskopische Anatomie 91, 1–74.

    Google Scholar 

  • Hökfelt, T., Johansson, O., Efendic, S., Luft, R. &Arimura, A. (1975) Are there somatostatin-containing nerves in the rat gut? Immunohistochemical evidence for a new type of peripheral nerve.Experientia 31, 852–4.

    Google Scholar 

  • Hökfelt, T. &Ljungdahl, A. (1972) Application of cytochemical techniques to the study of suspected transmitter substances in the nervous system.Advances in Biochemical Psychopharmacology 6, 1–36.

    Google Scholar 

  • Jacobowitz, D. (1965) Histochemical studies of the autonomic innervation of the gut.The Journal of Pharmacology and Experimental Therapeutics 149, 358–64.

    Google Scholar 

  • Juorio, A. V. &Gabella, G. (1974) Noradrenaline in the guinea-pig alimentary canal: regional distribution and sensitivity to denervation and reserpine.Journal of Neurochemistry 22, 851–8.

    Google Scholar 

  • Larsson, L. -I., Fahrenkrug, J., Schaffalitzky de Muckadell, O., Sundler, F., HåKanson, R. &Rehfeld, J. F. (1976) Localization of vasoactive intestinal polypeptide (VIP) to central and peripheral neurons.Proceedings of the National Academy of Sciences (USA)73, 3197–200.

    Google Scholar 

  • Llewellyn-Smith, I. J., Wilson, A. J., Furness, J. B., Costa, M. &Rush, R. A. (1981) Ultrastructural identification of noradrenergic axons and their distribution within the enteric plexuses of the guinea-pig small intestine.Journal of Neurocytology 10, 331–52.

    Google Scholar 

  • Nilsson, G., Larsson, L.-I., Håkanson, R., Brodin, E., Pernow, B. &Sundler, F. (1975) Localization of substance P-like immunoreactivity in mouse gut.Histochemistry 43, 97–9.

    Google Scholar 

  • Norberg, K.-A. (1964) Adrenergic innervation of the intestinal wall studied by fluorescence microscopy.International Journal of Neuropharmacology 3, 379–82.

    Google Scholar 

  • Norberg, K.-A. &Hamberger, B. (1964) The sympathetic adrenergic neuron. Some characteristics revealed by histochemical studies on the intraneuronal distribution of the transmitter.Acta physiologica scandinavica 63 (Supplement 238) 1–42.

    Google Scholar 

  • Pearse, A. G. E. &Polar, J. M. (1975) Immunocytochemical localization of substance P in mammalian intestine.Histochemistry 41, 373–5.

    Google Scholar 

  • Pellegrino de Iraldi, A. &de Robertis, E. (1961) Action of reserpine on the submicroscopic morphology of the pineal gland.Experientia 17, 122–3.

    Google Scholar 

  • Richards, J. G. &Da Prada, M. (1977) Uranaffin reaction: a new cytochemical technique for the localization of adenine nucleotides in organelles storing biogenic amines.The Journal of Histochemistry and Cytochemistry 25, 1322–36.

    Google Scholar 

  • Richards, J. G. &Da Prada, M. (1980) Cytochemical investigations on subcellular organelles storing biogenic amines in peripheral adrenergic neurons.Advances in Biochemical Psychopharmacology 25, 269–78.

    Google Scholar 

  • Taxi, J. (1965) Contribution à l'étude des connexions des neurones moteurs du système nerveux autonome.Annales des Sciences Naturelles, Zoologie, Series 12 7, 413–674.

    Google Scholar 

  • Tranzer, J.-P. &Richards, J. G. (1976) Ultrastructural cytochemistry of biogenic amines in nervous tissue: methodologic improvements.The Journal of Histochemistry and Cytochemistry 24, 1178–93.

    Google Scholar 

  • Tranzer, J.-P. &Thoenen, H. (1967) Electronmicroscopic localization of 5-hydroxydopamine (3,4,5-trihydroxy-phenyl-ethylamine), a new ‘false’ sympathetic transmitter.Experientia 23, 743–5.

    Google Scholar 

  • Watanabe, H. (1971) Adrenergic nerve elements in the hypogastric ganglion of the guinea-pig.The American Journal of Anatomy 130, 305–30.

    Google Scholar 

  • Wilson, A. J., Furness, J. B. &Costa, M. (1979) A unique population of uranaffin-positive intrinsic nerve endings in the small intestine.Neuroscience Letters 14, 303–8.

    Google Scholar 

  • Wilson, A. J., Furness, J. B. &Costa, M. (1981) The fine structure of the submucous plexus of the guinea-pig ileum. I. The ganglia, neurons, Schwann cells and neuropil.Journal of Neurocytology 10, 759–84.

    Google Scholar 

  • Wong, W. C., Helme, R. D. &Smith, G. C. (1974) Degeneration of noradrenergic nerve terminals in submucous ganglia of the rat duodenum following treatment with 6-hydroxydopamine.Experientia 30, 282–4.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wilson, A.J., Furness, J.B. & Costa, M. The fine structure of the submucous plexus of the guinea-pig ileum. II. Description and analysis of vesiculated nerve profiles. J Neurocytol 10, 785–804 (1981). https://doi.org/10.1007/BF01262653

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01262653

Keywords

Navigation