Histochemistry

, Volume 60, Issue 2, pp 189–224 | Cite as

A cytochemical and ultrastructural study of the “S.I.F.” cells in cat sympathetic ganglia

  • Amapola Autillo-Touati
Article

Summary

According to the hypothesis of Eccles and Libet, the small intensely fluorescent cells (S.I.F. cells) in the sympathetic ganglion would represent an essential element in the inhibition of the principal neuron. As a contribution to the study of this important problem, we have investigated serial sections in superior cervical (S.C.G.) and celiac (C.G.) ganglia of the cat, a species that has not been extensively studied up to now, both by fluorescence and electron microscopy. We have shown that the “S.I.F.” cells are three times fewer in the cat S.C.G. than in the rat S.C.G. There are five times more “S.I.F.” cells in the C.G. of the cat than in the S.C.G. of the same species. Moreover we have described two types of “S.I.F.” cells.

Type I is composed of cells characterized by highly polymorphous large dense-cored vesicles. These cells lack processes and are grouped in clusters centered on fenestrated capillaries. They could be endocrine function cells. Type II is formed of isolated cells which exibit long processes and establish synaptic junctions with the dendrites of the principal neurons. In this case, the dense-cored vesicles are very regular and much smaller. These cells could be equivalent to interneurons. Type I very strongly predominates in the S.C.G. and C.G. of the cat where it represents more than 90% of the “S.I.F.” cell total observed by fluorescence microscopy. A priori such a quantitative and qualitative heterogeneity hardly consistent with Eccles and Libet's hypothesis based on the existence of dopaminergic interneurons only, allows the question to be raised as to the functional significance of the “S.I.F.” cells in ganglion physiology. The notion of modulation of ganglionic transmission does not seem to be quiered by these new data but could be founded on different forms of action embodied in the broader conception of the neuromodulation phenomenon.

Keywords

Fluorescence Microscopy Function Cell Cell Total Serial Section Essential Element 

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References

  1. 1.
    Aloe, L., Mugnaini, E., Levi-Montalcini, R.: Light and electron microscopic studies on the excessive growth of sympathetic ganglia in rats injected daily from birth with 6-OHDA and NGF. Arch. Ital. Biol. 113, 326–353 (1975)Google Scholar
  2. 2.
    Autillo, A., Seite, R.: Recherches sur les petites cellules intensément fluorescentes (S.I.F. cells) des ganglions coeliaques du Chat. Etude préliminaire par la méthode de Grillo (Proc. 60ème Congr. Association des Anatomistes, Nice mai 1976). In: Bull. Assoc. Anat. (1976a) (in press)Google Scholar
  3. 3.
    Autillo, A., Seite, R.: Small intensely fluorescent cells (“S.I.F.” cells) in cervical superior ganglia of the Cat as revealed by the Grillo's method. In: Histochemistry and Cytochemistry 1976. Proc. Fifth Intern. Congr. Histochem. Cytochem. Bucarest 1976, pp. 33 (1976b)Google Scholar
  4. 4.
    Axelsson, S., Björklund, A., Falck, B., Lindvall, O., Svensson, L.A.: Glyoxylic acid condensation: a new fluorescence method for the histochemical demonstration of biogenic monoamines. Acta Physiol. Scand. 87, 57–62 (1973)Google Scholar
  5. 5.
    Behrendt, H., Lindl, T., Cramer, H.: In vitro effects of histamine liberator compound 48/80 on rat superior cervical ganglia with special regard to the small granule containing cells. Cell Tissue Res. 166, 71–81 (1976)Google Scholar
  6. 6.
    Benitez, H.H., Masurovsky, E.B.: Interneurons of the sympathetic cervical ganglia in organotypic cultures. A suggestion as their functions, based on three types of study. J. Neurocytol. 3, 363–384 (1974)Google Scholar
  7. 7.
    Bennett, T., Malmfors, T.: The adrenergic nervous system of the domestic fowl. Z. Zellforsch. 106, 22–50 (1970)Google Scholar
  8. 8.
    Björklund, A., Ehinger, B., Falck, B.: A method for differenciating dopamine from noradrenaline in tissue sections by microspectrofluorometry. J. Histochem. Cytochem. 16, 263–270 (1968)Google Scholar
  9. 9.
    Björklund, A., Cegrell, B., Falck, B., Ritzen, M., Rosengren, E.: Dopamine-containing cells in sympathetic ganglia. Acta Physiol. Scand. 78, 334–338 (1970)Google Scholar
  10. 10.
    Björklund, A., Falck, B., Lindvall, O., Svensson, L.A.: New aspects on reaction mechanisms in the formaldehyde histofluorescence method for monoamines. J. Histochem. Cytochem. 21, 17–25 (1973)Google Scholar
  11. 11.
    Böck, P.: Die Feinstruktur des paraganglionären Gewebes im Plexus suprarenalis des Meerschweinchens. Z. Zellforsch. 105, 389–404 (1970)Google Scholar
  12. 12.
    Brundin, T.: Studies on the preaortal paraganglia of new born rabbits. Acta Physiol. Scand. 70, Suppl. 290, 1–54 (1966a)Google Scholar
  13. 13.
    Brundin, T.: Storage and in vitro release rate of catecholamines from granules isolated from preaortal paraganglia and adrenals of newborn rabbits. Acta Physiol Scand. 66, 406–409 (1966, b)Google Scholar
  14. 14.
    Brundin, T., Hamberger, B., Norberg, K.A.: Postnatal changes in the preaortal paraganglia of rabbits. Acta Physiol. Scand. 66, 255–256 (1966)Google Scholar
  15. 15.
    Burlet, D.B.: Exitabilité du ganglion sympathique du rat et catecholamines endogènes. J. Physiol. (Paris) 72, 589–606 (1976)Google Scholar
  16. 16.
    Burnstock, G., Costa, M.: Adrenergic neurons. Their organization, function and development in the peripheral nervous system, pp. 225. London: Chapman and Hall 1975Google Scholar
  17. 17.
    Chiba, T.: Monoamine-containing paraneurons in the sympathetic ganglia of mammals. In: Paraneurons. New concepts on neuroendocrine relatives (Kobayashi, S., Chiba, T., Eds). Arch. Histol. Jap. 40, Suppl. 163–176 (1977)Google Scholar
  18. 18.
    Chiba, T., Black, A.C., Williams, J.R.: Evidence for dopamine-storing interneurons and paraneurons in rhesus monkey sympathetic ganglia. J. Neurocytol. 6, 441–453 (1977)Google Scholar
  19. 19.
    Chiba, T., Williams, T.H.: Histofluorescence characteristics and quantification of small, intensely fluorescent cells (“S.I.F.” cells) in sympathetic ganglia of several species. Cell Tissue Res. 162, 331–341 (1975)Google Scholar
  20. 20.
    Chun, L.L.Y., Patterson, P.H.: Role of nerve growth factor in the development of rat sympathetic neurons in vitro. I. Survival growth, and differenciation of catecholamines production. J. Cell Biol. 75, 694–704 (1977)Google Scholar
  21. 21.
    Cook, R.R., Burnstock, G.: The ultrastructure of Auerbach's plexus in the Guinea-pig. I. Neuronal elements. J. Neurocytol. 5, 171–194 (1976)Google Scholar
  22. 22.
    Coupland, R.E.: Observations on the chromaffin reaction. J. Anat. 88, 142–151 (1954)Google Scholar
  23. 23.
    Couteaux, R.: Principaux critères morphologiques et cytochimiques utilisables aujourd'hui pour définir les divers types de synapses. In: Actualités Neurophysiologiques, 3nd série. Monnier, A. M. (Ed.), pp. 145–173. Paris: Masson 1961Google Scholar
  24. 24.
    Crowcroft, P.J., Szurszewski, J. H.: A study of the inferior mesenteric and pelvic ganglia of Guinea-Pigs with intracellular electrodes. J. Physiol. (Lond.) 219, 421–441 (1971)Google Scholar
  25. 25.
    De Groat, W.C., Volle, L.R.: Interaction between the catecholamines and ganglionic stimulating agents in sympathetic ganglia. J. Pharmacol. Exp. Ther. 154, 200–215 (1966)Google Scholar
  26. 26.
    Della Bella, D., Benelli, G.: Evidence of a modulatory role of SIF cells on cat celiac ganglion. Synaptic transmission. In: Advances in biochemical psychopharmacology, vol. 16. Costa, E., Gessa, G.L. (eds.), p. 513. New-York: Raven Press 1977Google Scholar
  27. 27.
    De Ribaupierre, F., Siegrist, G., Dunant, Y., Dolivo, M.: Etude de la morphologie et de la fonction probable des cellules chromaffines du ganglion sympathique cervical supérieur de Rat. J. Physiol. (Paris) 58, 5 (1966)Google Scholar
  28. 28.
    Dun, N., Nishi, S.: Effects of dopamine in the superior cervical ganglion of the rabbit. J. Physiol. (Lond.) 239, 155–164 (1974)Google Scholar
  29. 29.
    Dunant, Y.: Organisation topographique et fonctionnelle du ganglion cervical supérieur du Rat. J. Physiol. (Paris) 59, 17–38 (1967)Google Scholar
  30. 30.
    Eccles, R.M., Libet, B.: Origin and blockade of the synaptic responses of curarized sympathetic ganglia. J. Physiol. (Lond.) 157, 484–503 (1961)Google Scholar
  31. 31.
    Ehinger, B., Falck, B.: Uptake of some catecholamines and their precursors into neurons of the cat ciliary ganglion. Acta Physiol. Scand. 78, 132–141 (1970)Google Scholar
  32. 32.
    Elfvin, L.G.: The fine structure of the cell surface of the chromaffin cells in the rat adrenal medulla. J. Ultrastruct. Res. 12, 263–286 (1965)Google Scholar
  33. 33.
    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 S.I.F. cells and their catecholamines content. J. Ultrastruct. Res. 51, 377–396 (1975)Google Scholar
  34. 35.
    Eränkö, O.: The pratical histochemical demonstration of catecholamines by formaldehyde induced fluorescence. J. Royal. Micr. Soc. 87, 259–276 (1967)Google Scholar
  35. 36.
    Eränkö, L., Eränkö, O.: Effect of guanethidine on nerve cells and small intensely fluorescent cells in sympathetic ganglia of newborn and adult rats. Acta Pharmacol. Toxicol. 30, 403–416 (1971)Google Scholar
  36. 37.
    Eränkö, L., Eränkö, O.: Effect of 6-hydroxydopamine on the ganglion cells and the small intensely fluorescent cells in the superior cervical ganglion of the rat. Acta Physiol. Scand. 84, 115–124 (1972,a)Google Scholar
  37. 38.
    Eränkö, L., Eränkö, O.: Effect of hydrocortisone on histochemically demonstrable catecholamines in the sympathetic ganglia and extra adrenal chromaffin tissue of the rat. Acta Physiol. Scand. 84, 125–133 (1972,b)Google Scholar
  38. 39.
    Eränkö, L., Eränkö, O.: Development aspects of SIF cells. In: Advances in biochemical psychopharmacology, vol. 16. Costa, E., Gessa, G. L. (eds.), p. 525. New-York: Raven Press 1977Google Scholar
  39. 40.
    Eränkö, O., Eränkö, L.: Morphological indications of SIF cell functions. In: Advances in biochemical psychopharmacology, vol. 16. Costa, E., Gessa, G.L. (eds.), p. 525. New York: Raven Press 1977Google Scholar
  40. 41.
    Eränkö, O., Eränkö, L.: Differenciation of dopamine from noradrenaline in tissue sections by microspectrofluorometry. J. Histochem. Cytochem. 19, 131–132 (1971,a)Google Scholar
  41. 42.
    Eränkö, O., Eränkö, L.: Small, intensely fluorescent granule-containing cells in the sympathetic ganglion of the rat. In: Progress in Brain Research, vol. 34: Histochemistry of nervous transmission. Eränkö, O. (ed.), pp. 39–51. Amsterdam: Elsevier 1971, bGoogle Scholar
  42. 43.
    Eränkö, O., Eränkö, L.: Fluorescence and electron microscopic observations on the small intensely fluorescent granule-containing cells in the sympathetic ganglia. In: Amine fluorescence histochemistry. Fujiwara, M., Tanaka, Ch. (eds.), pp. 117–124. Tokyo: Igaku-Shoin 1974Google Scholar
  43. 44.
    Eränkö, L., Hill, C., Eränkö, O., Burnstock, G.: Lack of toxic effect of guanethidine on nerve cells and small intensely fluorescent cells in cultures of sympathetic ganglia of new born rats. Brain Res. 43, 501–513 (1972)Google Scholar
  44. 45.
    Eränkö, O., Härkönen, M.: Histochemical demonstration of fluorogenic amines in the cytoplasm of sympathetic ganglion cells of the rat. Acta Physiol. Scand. 58, 285–286 (1963)Google Scholar
  45. 46.
    Eränkö, O., Härkönen, 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)Google Scholar
  46. 47.
    Eränkö, O., Heath, J.W., Eränkö, L.: Effect of hydrocortisone on the ultrastructure of the small granule-containing cells in the superior cervical ganglion of the newborn rat. Experientia 29, 457–459 (1973)Google Scholar
  47. 48.
    Eränkö, O., Lempinen, M., Raisänen, L.: Adrenaline and noradrenaline in the organ of Zuckerkandl and adrenals of newborn rats treated with hydrocortisone. Acta Physiol. Scand. 66, 253–254 (1966)Google Scholar
  48. 49.
    Falck, B.: Observations on the possibilities of the cellular localization of monoamines by a fluorescence method. Acta Physiol. Scand. 56, Suppl. 197, 1–25 (1962)Google Scholar
  49. 50.
    Falck, B., Hillarp, N.A., Thieme, G., Torp, A.: Fluorescence of catecholamines and related compounds condensed with formaldehyde. J. Histochem. Cytochem. 10, 348–354 (1962)Google Scholar
  50. 51.
    Falck, B., Owman Ch.: A detailed methodological description of the fluorescence method for the cellular demonstration of biogenic monoamines. Acta Univer. Lund, Sectio 2, 7, 1–27 (1965)Google Scholar
  51. 52.
    Fujita, T.: Concept of paraneurons. In: Paraneurons. New concepts on neuroendocrine relatives. Kobayashi, S., Chiba, T. (Eds). Arch. Histol. Jap. 40, suppl., 1–12 (1977)Google Scholar
  52. 53.
    Furness, J.B., Costa, M.: Some observations on extra-adrenal chromaffin cells in the lower abdomen and pelvis. In: Chromaffin, Enterochromaffin and related Cells. Coupland, R.E., Fujita, T. (eds), p. 33. Amsterdam: Elsevier 1976Google Scholar
  53. 54.
    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)Google Scholar
  54. 55.
    Fuxe, K., Goldstein, M., Hökfelt, T., Joh, T. H.: Cellular localization of dopamine-β-hydroxylase and phenylethanol-amine-N-methyl transferase as revealed by immunochemistry. In: Progress in Brain Research, vol. 34: Histochemistry of nervous transmission. Eränkö, O. (ed.), pp. 127–138. Amsterdam: Elsevier 1971Google Scholar
  55. 56.
    Fuxe, K., Jonsson, G.: The histochemical fluorescence method for the demonstration of catecholamines. Theory, practice and application. J. Histochem. Cytochem. 21, 293–311 (1973)Google Scholar
  56. 57.
    Gabella, G.: Structure of the autonomic nervous system. London: Chapman and Hall 1976Google Scholar
  57. 58.
    Gianutsos, G., Moore, K.E.: Effects of pre-or postnatal dexamethasone, adrenocorticotrophic hormone and environmental stress on phenyl-ethanolamine N-methyltransferase activity and catecholamines in sympathetic ganglia of neonatal rats. J. Neurochem. 28, 935–940 (1977)Google Scholar
  58. 59.
    Gray, E. G.: The fine structural caracterization of different types of synapses. In: Progress in Brain Research, vol. 34: Histochemistry of nervous transmission. Eränkö, O. (ed.), pp. 149–160. Amsterdam: Elsevier 1971Google Scholar
  59. 60.
    Greengard, P., Kebabian, J.W.: Role of cyclic AMP, in synaptic transmission in the mammalian peripheral nervous system. Fed. Proc. 33, 1059–1067 (1974)Google Scholar
  60. 61.
    Greengard, P., Nathason, J.A., Kebabian, J.W.: Dopamine-octapamine and serotonine-sensitive adenylate cyclases: possible receptors in aminergic neurotransmission. In: Frontiers in Catecholamines Research. Vusdin, E., Snyder, S. (eds.), pp. 317–382. Oxford: Pergamon Press 1973Google Scholar
  61. 62.
    Grillo, M.A.: Electron microscopy of sympathetic tissues. Pharmacol. Rev. 18, 387–399 (1966)Google Scholar
  62. 63.
    Grillo, M.A., Jacobs, L., Comroe, J.H.: A combined fluorescence histochemical and electron microscopic method for studying special monoamine containing cells. J. Comp. Neurol. 153, 1–14 (1974)Google Scholar
  63. 64.
    Haefely, W.: Electrophysiology of the adrenergic neuron. In: Catecholamines. Blaschko, H., Muscholl, E. (eds.) pp. 661–725. Berlin-Heidelberg-New York: Springer-Verlag 1972Google Scholar
  64. 65.
    Haefely, W.: Muscarinic post-synaptic events in the cat superior cervical ganglion in situ. Naunyn-Schmiedeberg Arch. Pharmacol. 281, 119–143 (1974)Google Scholar
  65. 66.
    Hamberger, B., Norberg, K.A.: Monoamines in sympathetic ganglia studied with fluorescence microscopy. Experientia 19, 580–581 (1963)Google Scholar
  66. 67.
    Hamberger, B., Norberg, K.A., Sjöqvist, F.: Evidence for adrenergic nerve terminals and synapses in sympathetic ganglia. Int. J. Pharmacol. 2, 279–282 (1964)Google Scholar
  67. 68.
    Hartman, B.K.: Immunofluorescence of dopamine-β-hydroxylase. Application of improved methodology to the localization of the peripheral and central noradrenergic nervous system. J. Histochem. Cytochem. 21, 312–332 (1973)Google Scholar
  68. 69.
    Hervonen, A.: Development of catecholamines storing cells in human fetal paraganglia and adrenal medulla. Acta Physiol. Scand., suppl. 368, 1–94 (1971, a)Google Scholar
  69. 70.
    Hervonen, A.: On the innervation and differentiation of human fetal chromaffin tissue. In: Progress in Brain Research, vol. 34: Histochemistry of nervous transmission. Eränkö, O. (ed.), pp. 445–454. Amsterdam: Elsevier 1971, bGoogle Scholar
  70. 71.
    Hervonen, A., Kanerva, L.: Catecholamines storing cells in human fetal superior cervical ganglion. Acta Physiol. Scand. 84, 538–542 (1972)Google Scholar
  71. 72.
    Hervonen, A., Vaalasti, A., Vaalasti, T., Partanen M., Kanerva, L.: Paraganglia in the urogenital tract of man. Histochemistry 46, 307–313 (1976)Google Scholar
  72. 73.
    Heym, Ch.: Monoamine storage sites in the rat superior cervical ganglion following synthesis inhibition. Cell Tissue Res. 165, 239–248 (1976)Google Scholar
  73. 74.
    Ivanov, D.P.: Recherches ultrastructurales sur les cellules paraganglionnaires du ganglion coeliaque du Rat et leurs connexions avec les neurones. Acta Anat 89, 266–286 (1974)Google Scholar
  74. 75.
    Jacobowitz, D.M.: Catecholamine fluorescence studies of adrenergic neurons and chromaffin cells in sympathetic ganglion. Fed. Proc. 29, 1929–1944 (1970)Google Scholar
  75. 76.
    Jacobowitz, D.M.: The peripheral autonomic system. In: The peripheral nervous system. Hubbard, J.I. (ed.) pp. 87–111. New-York and London: Plenum Press 1974Google Scholar
  76. 77.
    Jacobowitz, D.M., Greene, L.A.: Histofluorescence study of chromaffin cells in dissociated cells cultures of chick embryo-sympathetic ganglia. J. Neurobiol. 5, 65–83 (1974)Google Scholar
  77. 78.
    Jacobowitz, D.M., Woodward, J.K.: Adrenergic neurons in the cat superior cervical ganglion and cervical sympathetic nerve trunk. A histochemical study. J. Pharmacol. Exp. Ther. 162, 213–226 (1968)Google Scholar
  78. 79.
    Jonsson, G.: Quantification and differenciation of biogenic monoamines demonstrated with the formaldehyde fluorescence method. In: Progress in Brain Research. vol. 34: Histochemistry of nervous transmission. Eränkö, O. (ed.), pp. 53–61. Amsterdam: Elsevier 1971Google Scholar
  79. 80.
    Kanerva, L.: The post development of monoamines and cholinesterases in the paracervical ganglion of the rat uterus. In: Progress in Brain Research. vol. 34: Histochemistry of nervous transmission. Eränkö, O. (ed.), pp. 433–443. Amsterdam Elsevier 1971Google Scholar
  80. 81.
    Kanerva, L.: Development, histochemistry and connections of the paracervical (Frankenhaüser) ganglion of the rat uterus. A light and electron microscopy study. Acta Inst. Anat. Universitatis Helsinkiensis, suppl. 2 (1972)Google Scholar
  81. 82.
    Kanerva, L, Hervonen, A., Rechardt, L.: Permanganate fixation demonstrates the monoamine-containing granular vesicles in the SIF cells but not in the adrenal medulla or mast cells. Histochemistry 52, 61–72 (1977)Google Scholar
  82. 83.
    Karnovsky, J.M: A formaldehyde-glutaraldehyde fixative of high osmolality of use in electron microscopy. J. Cell Biol. 27, 137A (1965)Google Scholar
  83. 84.
    Kebabian, J.W.: Cyclic nucleotides and synaptic transmission in sympathetic ganglia. In: Advances in biochemical psychopharmacology, vol. 16. Costa, E., Gessa, G. L. (eds.), p. 533. New-York: Raven Press 1977Google Scholar
  84. 85.
    Kebabian, J.W., Bloom, F.E., Steiner, A.L., Greengard, P.: Neurotransmitters increase cyclic nucleotides in postganglionic neurons: immunocytochemical demonstration. Science 190, 157–159 (1975)Google Scholar
  85. 86.
    Kebabian, J.W., Greengard, P.: Dopamine sensitive adenyl cyclase: possible role in synaptic transmission. Science 174, 1346–1349 (1971)Google Scholar
  86. 87.
    Kemp, K.W., Santer, R.M., Lever, J.D., Lu, K.S, Presley, R.: A numerical relationship between chromaffin-positive and small intensely fluorescent cells in sympathetic ganglia. J. Anat. 124, 269–273 (1977)Google Scholar
  87. 88.
    Kondo, H.: Innervation of SIF cells in the superior cervical and nodose ganglia: an ultrastructural study with serial sections. Biol. Cell 30, 253–264 (1977)Google Scholar
  88. 89.
    Kopin, I.J., Palkovits, M., Kobayashi, R.M., Jacobowitz, D.M.: Quantitative relationship of catecholamines content and histofluorescence in brain of rats. Brain Res. 80, 229–235 (1974)Google Scholar
  89. 90.
    Koslow, S.H.: Dopamine and other catecholamines containing SIF cells. In: Advances in biochemical psychopharmacology, vol. 16. Costa, E., Gessa, G.L. (eds.), p. 553. New-York: Raven Press, 1977 aGoogle Scholar
  90. 91.
    Koslow, S.H.: Introduction: SIF cells. In: Advances in Biochemical Psychopharmacology, vol. 16. Costa, E., Gessa, G.L. (eds.), p. 501. New-York: Raven Press 1977 bGoogle Scholar
  91. 92.
    Koslow, S.H., Bjegovic, M., Costa, E.: Catecholamines in sympathetic ganglia of rat: effects of dexamethasone and reserpine. J. Neurochem. 24, 277–282 (1975)Google Scholar
  92. 93.
    Lempinen, M.: Extra-adrenal chromaffin tissue of the rat and the effect of cortical hormones on it. Acta Physiol. Scand. 62, suppl. 231, 1–91 (1964)Google Scholar
  93. 94.
    Lempinen, M.: Effect of hydrocortisone on histochemically demonstrable catecholamines of the para-aortic body of the rat. Acta Physiol. Scand. 66, 251–252 (1966)Google Scholar
  94. 95.
    Lever, J.D., Lu, K.S., Presley, R., Santer, R.M.: The distribution of small intensely fluorescent (S.I.F.) and a chromaffin-positive cells in rat sympathetic ganglia. J. Anat. (Lond.) 117, 643–644 (1974)Google Scholar
  95. 96.
    Lever, J.D., Presley, R.: Studies on the sympathetic neuron in vitro. In: Progress in Brain Research, vol. 34: Histochemistry of nervous transmission. Eränkö O. (ed.), pp. 499–512. Amsterdam: Elsevier 1971Google Scholar
  96. 97.
    Lever, J.D., Santer, R.M., Lu, K.S., Presley, R.: Chromaffin-positive and small intensely fluorescent cells in normal and amine depleted sympathetic ganglia. In: Chromaffin, Enterochromaffin and related cells. Coupland, R.E., Fujita, T. (eds.), p. 91. Amsterdam: Elsevier 1976Google Scholar
  97. 98.
    Lever, J.D., Santer, R.M., Lu, K.S., Presley, R.: Electron probe X-ray micro-analysis of small granulated cells in rat sympathetic ganglia after aldehyde and dichromate treatment. J. Histochem. Cytochem. 25, 275–279 (1977)Google Scholar
  98. 99.
    Libet, B.: The role SIF cells play in ganglionic transmission. In: Advances in biochemical psychopharmacology, vol. 16 Costa, E., Gessa, G.L. (eds.), p. 541. New-York: Raven Press 1977Google Scholar
  99. 100.
    Libet, B.: Generation of slow-inhibitory and exitatory post-synaptic potentials. Fed. Proc. 29, 1945–1955 (1970)Google Scholar
  100. 101.
    Libet, B., Owman, Ch.: Concomittant changes in formaldehyde-induced fluorescence of dopamine interneurons, and in slow-inhibitory post-synaptic potentials of the rabbit, induced by stimulation of the pre-ganglionic nerve or by a muscarinic agent. J. Physiol. (Lond.) 237, 635–662 (1974)Google Scholar
  101. 102.
    Libet, B., Tanaka, T., Tosaka, T.: Different sensitivities of acetylcholine-induced “after hyperpolarization” compared to dopamine-induced hyperpolarization to ouabain or to lithium-replacement of sodium, in rabbit sympathetic ganglia. Life Sci. 20, 1863–1870 (1977)Google Scholar
  102. 103.
    Lindvall, O., Björklund, A.: The glyoxylic acid fluorescence histochemical method: a detailed account of methodology of the visualization of central catecholamine neurons. Histochemistry 39, 97–127 (1974)Google Scholar
  103. 104.
    Lindvall, O., Björklund, A., Nobin, A., Stenevi, U.: The adrenergic innervation of the rat thalamus as revealed by the glyoxylic acid fluorescence method. J. Comp. Neurol. 154, 317–348 (1974)Google Scholar
  104. 105.
    Liuzzi, A., Foppen, F.H., Saavedra, J.M., Jacobowitz, D., Kopin, I.J.: Effect of NGF and dexamethasone on phenyl ethanolamine-N-methyl transferase (PNMT) activity in neonatal rat superior cervical ganglia. J. Neurochem. 28, 1215–1220 (1977)Google Scholar
  105. 106.
    Lu, K.S., Lever, J.D., Santer, R.M., Presley, R.: Small granulated cell types in rat superior cervical and celiac-mesenteric ganglia. Cell Tissue Res. 172, 331–343 (1976)Google Scholar
  106. 107.
    Mc Afee, D.A., Greengard, P.: Adenosine 3′–5′-monophosphate: electrophysiological evidence for a role in synaptic transmission. Science 178, 310–312 (1972)Google Scholar
  107. 108.
    Mc Donald D.M., Mitchell, R.A.: The innervation of glomus cells, ganglion cells and blood vessels in the rat carotid-body: a quantitative ultrastrutural analysis. J. Neurocytol. 4, 177–236 (1975)Google Scholar
  108. 109.
    Machova, J., Kristofova, A.: The effect of dibutyryl-cyclic AMP dopamine and aminophylline on ganglionic surface potential and transmission. Life Sci. 13, 525–536 (1973)Google Scholar
  109. 110.
    Marx, J.L.: Cyclic-AMP in brain: role in synaptic transmission. Science 178, 1188–1190 (1972)Google Scholar
  110. 111.
    Mascorro, J.A., Yates, R.D.: Microscopic observations on abdominal sympathetic paraganglia. Texas Rep. Biol. 28, 1–2 (1970)Google Scholar
  111. 112.
    Masurovsky, E.B., Benitez, H.H., Murray, M.R.: Development of interneurons in long-term organotypic cultures of rat superior cervical and stellate ganglia. J. Cell Biol. 55, 166a (1972)Google Scholar
  112. 113.
    Matthews, M.R.: Evidence from degeneration experiments for the pre-ganglionic origin of afferent fibers to the small granule-containing cells of the rat superior cervical ganglion. J. Physiol. (Lond.) 218, 95–96 (1971)Google Scholar
  113. 114.
    Matthews, M.R.: Synaptic and other relationships of small granule- containing cells (SIF cells) in sympathetic ganglia. In: Chromaffin, Enterochromaffin and related Cells, Coupland, R.E., Fujita, T. (eds.), p. 144. Amsterdam: Elsevier 1976Google Scholar
  114. 115.
    Matthews, M.R., Nash, J.R.G.: An efferent synapse from a small granule-containing cells to a principal neuron in the superior cervical ganglion. J. Physiol. (Lond.) 210, 11–13 (1970)Google Scholar
  115. 116.
    Matthews, M.R., Ostberg, A.: Effects of preganglionic nerve section upon the afferent innervation of the small granule-containing cells in the rat superior cervical ganglion. Acta Physiol. Pol. 24, 215–223 (1973)Google Scholar
  116. 117.
    Matthews, M.R., Raisman, G.: Two cell types in the superior cervical ganglion of the rat. J. Anat. 103, 397–398 (1968)Google Scholar
  117. 118.
    Matthews, M.R., Raisman, G.: The ultrastructure and somatic efferent synapses of small granule-containing cells in superior cervical ganglion. J. Anat. 105, 255–282 (1969)Google Scholar
  118. 119.
    Moore, K.E., Phillipson, O.: Effect of dexamethasone on phenylethanolamine-N-methyltransferase and adrenaline in the brain and superior cervical ganglion of adult and neonatal rats. J. Neurochem. 25, 289–294 (1975)Google Scholar
  119. 120.
    Norberg, K.A.: Drugs-induced changes in monoamine levels in the sympathetic adrenergic ganglion cells and terminals. A histochemical study. Acta Physiol. Scand. 65, 221–234 (1965)Google Scholar
  120. 121.
    Norberg, K.A., Hamberger, B.: The sympathetic adrenergic neuron. Acta Physiol. Scand. 63, suppl. 238, 5–42 (1964)Google Scholar
  121. 122.
    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)Google Scholar
  122. 123.
    Norberg, K.A., Sjöqvist, F.: New possibilities for adrenergic modulation of ganglionic transmission. Pharmacol. Rev. 18, 743–751 (1966)Google Scholar
  123. 124.
    Olson, L.: Outgrowth of sympathetic adrenergic neurons in mice treated with a nerve growth factor (N.G.F.). Z. Zellforsch. 81, 155–173 (1967)Google Scholar
  124. 125.
    Olson, L.: Fluorescence histochemical evidence for axonal growth and secretions from transplanted adrenal medullary tissue. Histochemie 22, 17 (1970)Google Scholar
  125. 126.
    Palay, S.L.: The morphology of synapses in the central nervous system. Exp. Cell Res., suppl. 5, 275–293 (1958)Google Scholar
  126. 127.
    Papka, R.E.: The ultrastructure of adrenergic neurons in sympathetic ganglia of the new born rabbit after treatment with 6-hydroxydopamine. Amer. J. Anat. 137, 447–466 (1973)Google Scholar
  127. 128.
    Pearse, A.G.E.: SIF cells as APUD cells: a possible endocrine role. In: Advances in biochemical psychopharmacology, vol. 16. Costa, E., Gessa, G.L. (eds.), p. 547. New-York: Raven Press 1977Google Scholar
  128. 129.
    Phillipson, O.T., Moore, K.E.: Effect of dexamethasone and nerve-growth factor on phenylethanolamine-N-methyl transferase and adrenaline in organ cultures of newborn rat superior cervical ganglion. J. Neurochem. 25, 295–298 (1975)Google Scholar
  129. 130.
    Richards, J.G., Tranzer, J.P.: Localization of amine storage sites in the adrenergic cell body. A study of the superior cervical ganglion of the rat by fine structural cytochemistry. J. Ultrastruct. Res. 53, 204–216 (1975)Google Scholar
  130. 131.
    Santer, R.M., Lu, K.S., Lever, J.D., Presley, R.: A study of the distribution of chromaffin positive (Ch+) and small intensely fluorescent cells in sympathetic ganglia of a rat at various ages. J. Anat. 119, 589–599 (1975)Google Scholar
  131. 132.
    Santer, R.M., Presley, R., Lever, J.D., Lu, K.S.: Quantitative fluorescence studies of the effects of catecholamines and hydrocortisone on endogenous amine levels in neurons and small intensely fluorescent cells of embryonic chick sympathetic ganglia in vivo and in vitro. Cell Tissue Res. 175, 333–344 (1976)Google Scholar
  132. 133.
    Schorderet, M.: AMP-cyclique et système nerveux J. Physiol. (Paris) 68, 474–497 (1974)Google Scholar
  133. 134.
    Siegrist, G., De Ribaupierre, F., Dolivo, M., Rouiller, Ch.: Les cellules chromaffines des ganglions cervicaux supérieurs du rat. J. Microscopie 5, 791–794 (1966)Google Scholar
  134. 135.
    Siegrist, G., Dolivo, M., Dunant, Y., Foroglou-Kerameus, C., De Ribaupierre, F., Rouiller, Ch.: Ultrastructure and function of the chromaffin cells in the superior cervical ganglion of the rat. J. Ultrastruct. Res. 25, 381–407 (1968)Google Scholar
  135. 136.
    Smith, R.E., Farquhar, M.G.: Preparation of thick sections for cytochemistry and electron microscopy by a non-freezing technique. Nature 16, 691 (1963)Google Scholar
  136. 137.
    Tamarind, D.L., Quilliam, J.P.: Synaptic organization and other structural feature of the superior cervical ganglion of the rat, kitten and rabbit. Micron 2, 204–234 (1971)Google Scholar
  137. 138.
    Taxi, J., Gautron, J., L'Hermitte, P.: Donnees ultrastructurales sur une éventuelle modulation adrénergique de l'activité du ganglion cervical supérieur du Rat. C.R. Acad. Sci. (Paris) 269, 1281–1284 (1969)Google Scholar
  138. 139.
    Taxi, J., Mikulajova, M.: Some cytochemical and cytological features of the socalled S.I.F. cells of the superior cervical ganglion of the rat. J. Neurocytol. 5, 283–295 (1976)Google Scholar
  139. 140.
    Tosaka, T., Kobayashi, H.: The SIF cell as a functional modulator of ganglionic transmission through the release of dopamine. In: Paraneurons. New concepts on neuro-endocrine relatives. Kobayashi, S., Chiba, T. (eds.). Arch. Histol. Jap. 40, suppl., 187–196 (1977)Google Scholar
  140. 141.
    Tranzer, J.P., Thoenen, H.: Various types of amine storing vesicles in peripheral adrenergic nerve terminals. Experientia 24, 484–486 (1968)Google Scholar
  141. 142.
    Tranzer, J.P., Thoenen, H.: Significance of “empty vesicles” in postganglionic sympathetic nerve terminals. Experientia 23, 123–124 (1967)Google Scholar
  142. 143.
    Van Orden, L.S. III, Burke, J.P., Geyer, M., Lodoen, F.V.: Localization of depletion sensitive and depletion resistant norepinephrine storages sites in autonomic ganglia. J. Pharmacol. Exp. Ther. 174, 56–71 (1970)Google Scholar
  143. 144.
    Von Euler, U.S., Liskajko, F.: Effect of drugs on the storage granules of adrenergic nerves. In: Pharmacology of cholinergic and adrenergic transmission. Proc. of the 2nd Intern. Pharmacol. Meet., Prague 1963, p. 245. Oxford: Pergamon Press 1965Google Scholar
  144. 145.
    Watanabe, H.: Adrenergic nerve elements in the hypogastric ganglion of the Guinea-pig. Amer. J. Anat. 130, 305–329 (1971)Google Scholar
  145. 146.
    Watanabe, H.: Ultrastructure and function of the granule-containing cells in the anuran sympathetic ganglia. In: Paraneurons. New Concepts on neuroendocrine relatives. Kobayashi, S., Chiba, T. (eds.). Arch. Histol. Jap. 40, Suppl. 177–186 (1977)Google Scholar
  146. 147.
    Watanabe, H., Burnstock, G.: A special type of small granule-containing cell in the abdominal para-aortic region of the frog. J. Neurocytol. 5, 465–478 (1976)Google Scholar
  147. 148.
    Weight, F.F., Weitsen, H.H.: Identification of small intensely fluorescent (SIF) cells as chromaffin cells in bullfrog sympathetic ganglia. Brain Res. 128, 213–226 (1977)Google Scholar
  148. 149.
    Williams, T.H.: Electron microscopic evidence for an autonomic interneurons. Nature 214, 309–310 (1967, a)Google Scholar
  149. 150.
    Williams, T.H.: The question of the intraganglionic (connector) neuron of the autonomic nervous system. J. Anat. 101, 603–604 (1967, b)Google Scholar
  150. 151.
    Williams, T.H., Black, A.C., Chiba, T., Bahalla, R.C.: Morphology and biochemistry of small, intensely fluorescent cells of sympathetic ganglia. Nature 256, 315–317 (1975)Google Scholar
  151. 152.
    Williams, T.H., Palay, S.L.: Ultrastructure of the small neurons in the superior cervical ganglion. Brain Res. 15, 17–34 (1969)Google Scholar
  152. 153.
    Williams, T.H., Black, A.C., Jr., Jew, J.: Interneurons/SIF cells in sympathetic ganglia of various mammals. In: Chromaffin, Enterochromaffin and related cells. Coupland, R.E., Fujita, T. (eds.), p. 112. Amsterdam: Elsevier 1976Google Scholar
  153. 154.
    Williams, T.H., Black, A.C. Jr., Chiba, T., Jew, J.Y.: Species differences in mammalian SIF cells. In: Advances in biochemical psychopharmacology, vol. 16. Costa, E., Gessa, G.L. (eds), p. 505. New-York: Raven Press 1977Google Scholar
  154. 155.
    Wilson, W.S., Robert, R., Cooper, J.: The subcellular localization of noradrenaline and dopamine in bovine superior cervical ganglion. Life Sci. 3, 281–285 (1973)Google Scholar
  155. 156.
    Yamauchi, A.: Ultrastructure of chromaffin-like interneurons in the autonomic ganglia. In: Chromaffin, Enterochromaffin and related Cells. Coupland, R.E., Fujita, T. (eds.), p. 128. Amsterdam, Elsevier 1976Google Scholar
  156. 157.
    Yamauchi, A.: On the recepto-endocrine property of granule-containing (GC) cells in the autonomic nervous system. In: Paraneurons. New concepts on neuroendocrine relatives Kobayashi, S., Chiba, T. (eds.). Arch. Histol. Jap. 40, suppl., 147–161 (1977)Google Scholar
  157. 158.
    Yokota, R.: The granule containing-cell somata on the superior cervical ganglion of the rat as studied by a serial sampling method for electron microscopy. Z. Zellforsch. 141, 331–345 (1973)Google Scholar
  158. 159.
    Yokota, R., Yamauchi, A.: Ultrastructure of the mouse superior cervical ganglion with the particular reference to the pre- and post-ganglionic elements covering the soma of its principal neurons. Amer. J. Anat. 148, 281–286 (1974)Google Scholar

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© Springer-Verlag 1979

Authors and Affiliations

  • Amapola Autillo-Touati
    • 1
  1. 1.Laboratoire d'Histologie I, Groupe de Recherches en NeurocytobiologieFaculté de Médecine de MarseilleMarseille Cédex 4France

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