Skip to main content
Log in

Fine structure of the autonomic ganglia of the mouse pulmonary vein

  • Published:
Journal of Neurocytology

Summary

The aim of this study was to describe the architecture of a ganglionated nerve plexus found in the loose connective tissue surrounding the pulmonary vein of the mouse. The input to this plexus was from the vagus nerves and from the stellate ganglia. A large ganglion containing more than 200 neurons was commonly found near the primary bifurcation of the pulmonary vein. The neurons were studied by NADH-diaphorase, zinc iodide-osmium and glyoxylic acid-induced catecholamine fluorescence methods at the light microscopic level, by scanning electron microscopy after the removal of connective tissue, and by transmission electron microscopy. The shape of the neuronal cell bodies was generally a smooth ellipsoid with the average major axis about twice the minor axis. The measured maximum cell diameter ranged from 14 to 42 μm (mean 26 μm). The profile area of individual neurons, as measured from wholemount preparations, ranged from 100 to 800 μm2 (mean 340 μm2) and the calculated neuronal volume ranged from 500 to 12 000 μm3 (mean 3300 μm3). Although there was this wide spread in neuronal size, histograms of cell size showed no separate populations of neurons.

Almost all of the ganglionic neuronal cell bodies showed no catecholamine-specific fluorescence, but about 1% of the neurons exhibited a weak green fluorescence. Only a few noradrenergic nerve fibres were seen within the ganglia and these were associated with intraganglionic blood vessels. Small, intensely fluorescent cells were only rarely associated with the ganglia. Neurons and satellite cells formed units which were surrounded by an intraganglionic connective tissue space and a perineurium. Some of the intraganglionic capillaries were fenestrated. Neurons were entirely surrounded by satellite cells and did not appear to have any long dendrites. The generally smooth neuronal cell bodies had short spine-like processes, which were confined to within the satellite cell sheath. Preganglionic nerve fibres formed pericellular baskets of varicose fibres around neurons and made synapses either directly on the cell body or on somatic spines in about equal numbers. No synapses were found in the neuropil at a distance from the neuronal cell body. A few nerve processes were deeply embedded within the neuronal cell body. Clusters of vesicles were found in the cytoplasm of most neurons and were associated with subplasmalemmal densities. These synapse-like structures were mostly directed towards satellite cells, but some were associated with incoming synapses.

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

  • Arvidson, B. (1979a) A study of the perineurial diffusion barrier of a peripheral ganglion.Acta neuropathologica 46, 139–44.

    Google Scholar 

  • Arvidson, B. (1979b) Distribution of intravenously injected protein tracers in peripheral ganglia of mice.Experimental Neurology 63, 388–410.

    Google Scholar 

  • Baker, D. G., McDonald, D. M., Basbaum, C. B. &Mitchell, R. A. (1986) The architecture of nerves and ganglia of the ferret trachea as revealed by acetylcholine histochemistry.Journal of Comparative Neurology 246, 513–26.

    Google Scholar 

  • Baluk, P., Fujiwara, T. &Matsuda, S. (1985) The fine structure of the ganglia of the guinea-pig trachea.Cell and Tissue Research 239, 51–60.

    Google Scholar 

  • Cameron, A. R. &Coburn, R. F. (1984) Electrical and anatomic characteristics of cells of ferret paratracheal ganglion.American Journal of Physiology 246, C450-C458.

    Google Scholar 

  • Chiang, C. H. &Gabella, G. (1986) Quantitative studies of the ganglion neurons of the mouse trachea.Cell and Tissue Research 246, 243–52.

    Google Scholar 

  • Dalsgaard, C.-J., Franco-Cereceda, A., Saria, A., Lundberg, J. M., Theodorsson-Norheim, E. &Hökfelt, T. (1986) Distribution and origin of substance P and neuropeptide Y-immunoreactive nerves in the guinea-pig heart.Cell and Tissue Research 243, 477–85.

    Google Scholar 

  • Dalsgaard, C.-J. &Lundberg, J. M. (1984) Evidence for a spinal afferent innervation of the guinea-pig lower respiratory tract as studied by the horseradish peroxidase technique.Neuroscience Letters 45, 117–22.

    Google Scholar 

  • De Almeida, O. P., Böhm, G. M., Carvalho, M. De P. &De Carvalho, A. P. (1975) The cardiac muscle in the pulmonary vein of the rat: a morphological and electrophysiological study.Journal of Morphology 145, 409–34.

    Google Scholar 

  • Dey, R. D., Allen Shannon, W. &Said, S. I. (1981) Localization of VIP immunoreactive nerves in airways and pulmonary vessels of dogs, cats, and human subjects.Cell and Tissue Research 220, 231–8.

    Google Scholar 

  • Ellison, J. P. &Hibbs, R. G. (1974) Catecholamine-containing cells of the guinea-pig heart: an ultrastructural study.Journal of Molecular and Cellular Cardiology 6, 17–26.

    Google Scholar 

  • Ellison, J. P. &Hibbs, R. G. (1976) An ultrastructural study of mammalian cardiac ganglia.Journal of Molecular and Cellular Cardiology 8, 89–101.

    Google Scholar 

  • Fisher, A. W. J. (1965) The intrinsic innervation of the pulmonary vessels.Acta anatomica 60, 481–96.

    Google Scholar 

  • Forehand, C. (1985) Density of somatic innervation on mammalian autonomic ganglion cells is inversely related to dendritic complexity and preganglionic convergence.Journal of Neuroscience 5, 3403–8.

    Google Scholar 

  • Forssmann, W. G., Birr, C., Carlquist, M., Christmann, M., Finke, R., Henschen, A., Hock, D., Kirchheim, H., Kreye, V., Lottspeich, J., Metz, J., Mutt, V. &Reinecke, M. (1984) The auricular myocardiocytes of the heart constitute an endocrine organ.Cell and Tissue Research 238, 425–30.

    Google Scholar 

  • Fujiwara, T. &Uehara, Y. (1980) Scanning electron microscopy of myenteric plexus; a preliminary communication.Journal of Electron Microscopy 29, 397–400.

    Google Scholar 

  • Furness, J. B. &Costa, M. (1975) The use of glyoxylic acid for the fluorescence histochemical demonstration of peripheral stores of noradrenaline and 5-hydroxytryptamine in whole mounts.Histochemistry 41, 335–52.

    Google Scholar 

  • Gabella, G. (1969) Detection of nerve cells by a histochemical technique.Experientia 25, 218–19.

    Google Scholar 

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

    Google Scholar 

  • Grigor'eva, T. A. (1962)The Innervation of Blood Vessels. New York: Pergamon Press.

    Google Scholar 

  • Grillo, M. A. &Nadel, J. (1980) Vital staining of tracheal ganglia.Physiologist 23, 70 (Abstract).

    Google Scholar 

  • Gu, J., Polak, J. M., Allen, J. M., Huang, W.-M., Sheppard, M. N., Tatemoto, K. &Bloom, S. R. (1984) High concentrations of a novel peptide, Neuropeptide Y, in the innervation of mouse and rat heart.Journal of Histochemistry and Cytochemistry 32, 466–72.

    Google Scholar 

  • Hökfelt, T. (1969) Distribution of noradrenaline storing particles in peripheral adrenergic neurons as revealed by electron microscopy.Acta physiologica scandinavica 76, 427–40.

    Google Scholar 

  • Honjin, R. (1954) On the ganglia and nerves of the lower respiratory tract of the mouse.Journal of Morphology 95, 263–88.

    Google Scholar 

  • Honjin, R. (1956a) On the nerve supply of the lung of the mouse, with special reference to the structure of the peripheral vegetative nervous system.Journal of Comparative Neurology 105, 587–625.

    Google Scholar 

  • Honjin, R. (1956b) Experimental degeneration of the vagus, and its relation to the nerve supply of the mouse, with special reference to the crossing innervation of the lung by the vagi.Journal of Comparative Neurology 106, 2–12.

    Google Scholar 

  • Hung, K.-S., Hertwich, M. S., Hardy, J. D. &Loosli, C. G. (1973) Ultrastructure of nerves and associated cells in bronchiolar epithelium of the mouse lung.Journal of Ultrastructure Research 43, 426–37.

    Google Scholar 

  • Hung, K.-S. &Loosli, C. G. (1977) Electron-microscopic studies of the innervation of the pulmonary veins of the mouse.Acta anatomica 97, 97–102.

    Google Scholar 

  • Jacobowitz, D. (1967) Histochemical studies of the relationship of chromaffin cells and adrenergic nerve fibres to the cardiac ganglia of several species.Journal of Pharmacology and Experimental Therapeutics 158, 227–40.

    Google Scholar 

  • Kalia, M. &Mesulam, M. M. (1980) Brainstem projections of sensory and motor components of the vagus complex in the cat. II. Laryngeal, tracheobronchial, pulmonary, cardiac, and gastrointestinal branches.Journal of Comparative Neurology 193, 467–508.

    Google Scholar 

  • Knight, D. S. (1980) A light and electron microscopic study of feline intrapulmonary ganglia.Journal of Anatomy 131, 413–28.

    Google Scholar 

  • Kramer, A. W. &Marks, L. S. (1966) The occurrence of cardiac muscle in the pulmonary veins of rodentia.Journal of Morphology 117, 135–50.

    Google Scholar 

  • Lane, M. A., Sastre, A. &Salpeter, M. M. (1976) Innervation of heart cells in culture by an endogenous source of cholinergic neurons.Proceedings of the National Academy of Sciences USA 73, 4506–10.

    Google Scholar 

  • Maillet, M. (1959) Modification de la technique de Champy au tétraoxyde d'osmium-iodure de potassium. Résultats de son application à l'étude des fibres nerveuses.Comptes Rendus des Séances de la Société de Biologie 153, 939–40.

    Google Scholar 

  • Matthews, M. R. (1974) Ultrastructure of ganglionic junctions. InThe Peripheral Nervous System (edited byHubbard, J. I.), pp. 111–50. New York: Plenum Press.

    Google Scholar 

  • Matthews, M. R. (1983) The ultrastructure of junctions in sympathetic ganglia of mammals. InAutonomic Ganglia (edited byElfvin, L.-G.), pp. 27–65. Chichester: Wiley Press.

    Google Scholar 

  • Mitchell, G. A. G. (1953)The Anatomy of the Autonomic Nervous System. Edinburgh: E. & S. Livingstone Ltd.

    Google Scholar 

  • Nonidez, J. F. (1937) Identification of the receptor areas in the venae cavae and pulmonary veins which initiate reflex cardiac acceleration (Bainbridge's reflex).American Journal of Anatomy 61, 203–31.

    Google Scholar 

  • Nonidez, J. F. (1941) Studies on the innervation of the heart. II. Afferent endings in the large arteries and veins.American Journal of Anatomy 68, 151–89.

    Google Scholar 

  • Papka, R. E. (1976) Studies of cardiac ganglia in pre- and postnatal rabbits.Cell and Tissue Research 175, 17–35.

    Google Scholar 

  • Purves, D. &Lichtman, J. W. (1985) Geometrical differences among homologous neurons in mammals,Science 228, 298–302.

    Google Scholar 

  • Reinecke, M., Weihe, E., Carraway, R. E. &Forssmann, W. G. (1981) Localization of neurotensin-immunoreactivity in the heart by immunohistochemistry and radioimmunoassay (Abstract 355).Acta anatomica 111, 123–4.

    Google Scholar 

  • Slavich, E. (1932) Confronti fra la morfologia di ganglia del parasimpatico encefalico e del simpatico cervicale con speciale riguardo alla struttura del ganglio ciliare.Zeitschrift für Zellforschung und mikroskopische Anatomie 15, 688–730.

    Google Scholar 

  • Smith, R. B. &Taylor, I. M. (1971) Observations on the intrinsic innervation of trachea, bronchi and pulmonary vessels in the sheep.Acta anatomica 80, 1–13.

    Google Scholar 

  • Szentágothai, J. (1964) The structure of the autonomic interneuronal synapse.Acta neurovegetativa 26, 247–76.

    Google Scholar 

  • Takino, M. (1933a) Über die Innervation der Lungenge-fässwand, besonders über das Vorkommen der Ganglienzellen an der Gefässwand der Vena pulmonales und über die Verbreitungszustände der Lungenblutgefässnerven bei der Fledermaus.Acta Scholae medicinalis Universitatis imperialis in Kioto 15, 303–7.

    Google Scholar 

  • Takino, M. (1933b) Vergleichende Studien über die histologische Struktur der Arteriae und Venae pulmonales, die Blutgefässnerven der Lunge und die Nerven der Bronchien bei verschiedenen Tierarten, besonders über die Beziehung der Blutgefässnerven zu den glatten Muskeln der Blutgefässe.Acta Scholae medicinalis Universitatis imperialis in Kioto 15, 321–54.

    Google Scholar 

  • Taxi, J., Gautron, J. &L'hermite, P. (1969) Données ultrastructurales sur une éventuelle modulation adrénergique de l'activité du ganglion cervical supérieur du rat.Comptes Rendus de L'Acamedie des Sciences, Paris, Serie D 269, 1281–4.

    Google Scholar 

  • Van Der Zypen, E. (1974) On catecholamine-containing cells in the rat interatrial septum.Cell and Tissue Research 151, 201–8.

    Google Scholar 

  • Wharton, J., Polak, J., Bloom, S. R., Will, J. A., Brown, M. R. &Pearse, A. G. E. (1979) Substance-P like immunoreactive nerves in the mammalian lung.Investigative Cellular Pathology 2, 3–10.

    Google Scholar 

  • Yamakado, M. &Yohro, T. (1977) Population and structure of nerve cells in mouse submandibular ganglion.Anatomy and Embryology 150, 301–12.

    Google Scholar 

  • Yamauchi, A. (1973) Ultrastructure of the innervation of the mammalian heart. InUltrastructure of the Mammalian Heart (edited byChallice, C. E. &Viragh, S.), pp. 127–78. New York: Academic Press.

    Google Scholar 

  • Yamauchi, A., Yokota, R. &Fujimaki, Y. (1974) Reciprocal synapses between cholinergic axons and small granule-containing cells in the rat cardiac ganglion.Anatomical Record 181, 195–210.

    Google Scholar 

  • Yokota, R. &Yamauchi, A. (1974) Ultrastructure of the mouse superior cervical ganglion, with particular reference to the pre- and postganglionic elements covering the soma of its principal neurons.American Journal of Anatomy 140, 281–98.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bałuk, P., Gabella, G. Fine structure of the autonomic ganglia of the mouse pulmonary vein. J Neurocytol 16, 169–184 (1987). https://doi.org/10.1007/BF01795301

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01795301

Keywords

Navigation