Summary
The paraganglia of the inferior mesenteric ganglia in the guinea-pig are composed of small chromaffin cells containing an abundance of granule-containing vesicles. The chromaffin cells are almost completely surrounded by satellite cells. In areas in which satellite cell processes do not intervene, the membranes of adjacent chromaffin cells are closely apposed and often form specialized attachment zones. The paraganglia contain a dense capillary network, the endothelial cells of which are often extremely attenuated and show areas of fenestration. The processes of chromaffin cells approach close to the capillary walls and are often bare of satellite cells covering on the side facing the capillary. Evidence has been obtained for the exocytotic release of the contents of chromaffin cell vesicles into pericapillary spaces. Synapses of cholinergic and noradrenergic axons are seen on the chromaffin cells. The cholinergic axons degenerate when the praganglia are decentralized, but the noradrenergic axons, which appear to arise from the local inferior mesenteric ganglia, remain intact. The results suggest that the paraganglia have an endocrine function.
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References
Becker, K.: Paraganglienzellen im Ganglion cervicale uteri der Maus. Z. Zellforsch. 130, 249–261 (1972)
Benitez, H.H., Masurovsky, E.B., Murray, M.R.: Interneurons of the sympathetic ganglia, in organotypic culture. A suggestion as to their function, based on three types of study. J. Neurocytol. 3, 363–384 (1974)
Biscoe, T.J.: Carotid body: structure and function. Physiol. Rev. 51, 437–495 (1971)
Brundin, T.: Studies on the preaortal paraganglia of newborn rabbits. Acta physiol. scand., Suppl. 290, 1–70 (1966)
Chen, I.L., Yates, R.D.: Ultrastructural studies of vagal paraganglia in Syrian hamsters, Z. Zellforsch. 108, 309–323 (1970)
Chiba, T.: Electron microscopic and histochemical studies on the synaptic vesicles in mouse vas deferens and atrium after 5-hydroxydopamine administration. Anat. Rec. 176, 35–48 (1973)
Costa, M., Furness, J.B.: Observations on the anatomy and amine histochemistry of the nerves and ganglia which supply the pelvic viscera and on the associated chromaffin tissue in the guinea-pig. Z. Anat. Entwickl.-Gesch. 140, 85–108 (1973)
Coupland, R.E.: The natural history of the chromaffin cell. London: Longmans, Green & Co. 1965
Coupland, R.E., Hopwood, D.: The mechanism of the differential staining reaction for adrenaline and noradrenaline-storing granules in tissues fixed in glutaraldehyde. J. Anat. (Lond.) 100, 227–243 (1966)
Coupland, R.E., Weakley, B.S.: Electron microscopic observation on the adrenal medulla and extra-adrenal chromaffin tissue of the postnatal rabbit. J. Anat. (Lond.) 106, 213–231 (1970)
Crowcroft, P.J., Jarrot, B., Ostberg, A.: Are there inhibitory mechanisms in mammalian autonomic ganglia. Proc. Aust. Physiol. Pharmacol. Soc. 2, 31–32 (1971)
Douglas, W.W.: Secretomotor control of adrenal medullary secretion: synaptic membrane and ionic events in stimulus-secretion coupling. In: Handbook of physiology, Sect. 7, Vol. 6, (Blaschko, H., Sayers, G., Smith, A.D., eds.), pp. 367–388. Washington: Amer. Physiol. Soc. 1975
Elfvin, L.G.: The ultrastructure of the capillary fenestrae in the adrenal medulla of the rat. J. Ultrastruct. Res. 12, 687–704 (1965)
Elfvin, L.G.: A new granule containing nerve cell in the inferior mesenteric ganglion of the rabbit. J. Ultrastruct. Res. 22, 37–44 (1968)
Elfvin, L.G., Hökfelt, T., Goldstein, M.: Fluorescence microscopical, immunohistochemical and ultrastructural studies on sympathetic ganglia of the guinea-pig, with special reference to the SIF cells and their catecholamine content. J. Ultrastruct. Res. 51, 377–396 (1975)
Eränkö, O., Härkönon, M.: Monoamine-containing small cells in the superior cervical ganglion of the rat and an organ composed of them. Acta physiol. scand. 63, 511–512 (1965)
Furness, J.B., Iwayama, T.: The arrangement and identification of axons innervating the vas deferens of the guinea-pig. J. Anat. (Lond.) 113, 179–196 (1972)
Garner, C.M., Duncan, D.: Observations on the fine structure of the carotid body. Anat. Rec. 130, 691–709 (1958)
Grillo, M.A.: Electron microscopy of sympathetic tissues. Pharmacol. Rev. 18, 387–399 (1966)
Grynszpan-Winograd, O.: Adrenaline and noradrenaline cells in the adrenal medulla of the hamster: a morphological study of their innervation. J. Neurocytol. 3, 341–361 (1974)
Grynszpan-Winograd, O.: Ultrastructure of the chromaffin cell. In: Handbook of physiology, Sect. 7, Vol. 6 (Blaschko, H., Sayers, G., Smith, A.D., eds.), pp. 295–308. Washington: Amer. Physiol. Soc. 1975
Gutman, Y., Boonyavirov, P.: Suppression by noradrenaline of catecholamine secretion from adrenal medulla. Europ. J. Pharmacol. 28, 384–386 (1974)
Jacobowitz, D.: Catecholamine fluorescence studies of adrenergic neurons and chromaffin cells in sympathetic ganglia. Fed. Proc. 29, 1929–1944 (1970)
Kobayashi, S.: Comparative cytological studies of the carotid body. 1. Demonstration of monoaminestoring cells by correlated chromaffin reaction and fluorescence histochemistry. Arch. histol. jap. 33, 319–339 (1971)
Kohn, A.: Die Paraganglien. Arch. mikr. Anat. 62, 263–365 (1903)
Kondo, H.: An electron microscopic study on innervation of the carotid body of guinea pig. J. Ultrastruct. Res. 37, 544–562 (1971)
Lempinen, M.: Extra-adrenal chromaffin tissue of the rat and the effect of cortical hormones on it. Acta physiol. scand. 62, Suppl. 231 (1964)
Lever, J.D., Lewis, P.R., Boyd, J.D.: Observations on the fine structure and histochemistry of the carotid body in the cat and rabbit. J. Anat. (Lond.) 93, 478–490 (1959)
Libet, B., Owman, C.: Concomitant changes in formaldehyde-induced fluorescence of dopamine interneurons and in slow inhibitory postsynaptic potentials of the rabbit superior cervical ganglion, induced by stimulation of the preganglionic nerve or by a muscarinic agent. J. Physiol. (Lond.) 237, 635–662 (1974)
Mascorro, J.A., Yates, R.D.: Ultrastructural studies of the effects of reserpine on mouse abdominal sympathetic paraganglia. Anat. Rec. 170, 269–280 (1971)
Matthews, M.R., Raisman, G.: The ultrastructure and somatic efferent synapses of small granule-containing cells in the superior cervical ganglion. J. Anat. (Lond.) 105, 255–282 (1969)
McDonald, D.M., Mitchell, R.A.: The innervation of glomus cells, ganglion cells, and blood vessels in the rat carotid body: a quantitative ultrastructural study. J. Neurocytol. 4, 177–230 (1975)
Muscholl, E., Vogt, M.: Secretory response of extramedullary chromaffin tissue. Brit. J. Pharmacol. 22, 193–203 (1964)
Mustonen, T., Teräväinen, H.: Synaptic connections of the paracervical (Frankenhäuser) ganglion of the rat uterus examined with the electronmicroscope after division of the sympathetic and sacral parasympathetic nerves. Acta physiol. scand. 82, 264–267 (1971)
Norberg, K.A., Hamberger, B.: The sympathetic adrenergic neuron. Acta physiol. scand. 63, Suppl. 238 1–42 (1965)
Norberg, K.A., Ritzen, M., Ungerstedt, U.: Histochemical studies on a special catecholamine-containing cell type in sympathetic ganglia. Acta physiol. Scand. 67, 260–270 (1966)
Ostberg, A.: Granule-containing cells of the inferior mesenteric ganglion. Proc. Aust. Physiol. Pharm. Soc. 1, 72–73 (1970)
Prentice, F.D., Wood, J.G.: Cytochemical localization of 5-hydroxydopamine in adrenergic element of cat adrenal medulla. Experientia (Basel) 30, 645–648 (1974)
Prentice, F.D., Wood, J.G.: Adrenergic innervation of cat adrenal medulla. Anat. Rec. 181, 689–704 (1975)
Santer, R.M., Lu, K.S., Lever, J.D., Presley, R.: A study of the distribution of chromaffin-positive and small intensely fluorescent cells in sympathetic ganglia of the rat at various ages. J. Anat. (Lond.) 119, 589–599 (1975)
Siegrist, G., Dolivo, M., Dunant, Y., Foroglou-Kerameus, C., Ribaupierre, F. de, Roullier, C.J.: Ultrastructure and function of the chromaffin cells in the superior cervical ganglion of the rat. J. Ultrastruct. Res. 25, 381–407 (1968)
Tranzer, J.P., Thoenen, H.: Electronmicroscopic localization of 5-hydroxydopamine (3, 4, 5-tri-hydroxyphenylethylamine) a new ‘false’ sympathetic transmitter. Experientia (Basel) 23, 743 (1967)
Tranzer, J.P., Thoenen, H., Snipes, R.L., Richards, J.G.: Recent development on the ultrastructural aspect of adrenergic nerve endings in various experimental conditions. Progr. Brain Res. 31, 33–46 (1969)
Viragh, S., Both, A.K.: The fine structure of abdominal paraganglia in the newborn mouse. Acta biol. Acad. Sci. hung. 18, 161–179 (1967)
Watanabe, H.: Adrenergic nerve elements in the hypogastric ganglion of the guinea-pig. Amer. J. Anat. 130, 305–330 (1971)
Watzka, M.: Die Paraganglien. In: Handbuch der mikroskopischen Anatomie des Menschen, Vol. VI/4 (Möllendorff, W. von, ed.), pp. 262–308. Berlin: Springer 1943
Williams, T.H.: Electron microscopic evidence for an autonomic interneuron. Nature (Lond.) 214, 309–310 (1967a)
Williams, T.H.: The question of the intraganglionic (connector) neuron of the autonomic nervous system. J. Anat. (Lond.) 101, 603–604 (1967b)
Williams, T.H., Palay, S.L.: Ultrastructure of the small neurons in the superior cervical ganglion. Brain Res. 15, 17–34 (1969)
Yokota, R.: The granule-containing cell somata in the superior cervical ganglion of the rat, as studied by a serial sampling method for electron microscopy. Z. Zellforsch. 141, 331–345 (1973)
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Furness, J.B., Sobels, G. The ultrastructure of paraganglia associated with the inferior mesenteric ganglia in the guinea-pig. Cell Tissue Res. 171, 123–139 (1976). https://doi.org/10.1007/BF00219704
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DOI: https://doi.org/10.1007/BF00219704