Smooth Muscle pp 113-137 | Cite as

Ultrastructure of Autonomic Nerves and Neuroeffector Junctions; Analysis of Drug Action

  • G. Burnstock


Electron microscopy is making an increasingly important contribution in the field of pharmacology. For example, the assumption made by many pharmacologists that smooth muscle preparations are homogeneous in terms of neurotransmitter and drug action is changing. Ultrastructural studies have shown that while some muscle cells are directly innervated and activated by neurotransmitters, others are activated indirectly by spread of excitation or inhibition from neighboring smooth muscle cells (see Section III.A). It is also likely that the density of “receptors” in the regions of muscle membrane in close apposition to nerve may be different from that in other parts of the muscle membrane.


Autonomic Nerve Adrenergic Nerve Adrenergic Neuron Granular Vesicle Electron Microscope Autoradiography 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aghajanian, G. K. and Bloom, F. E. 1966. Electron microscopic autoradiography of rat hypothalamus after intraventricular H3-norepinephrine. Science, 153:308–310.PubMedCrossRefGoogle Scholar
  2. Angeletti, P. U. and Levi-Montalcini, R. 1970. Specific cytoxic effect of 6-hydroxydopamine on sympathetic neuroblasts. Arch. Ital. Biol., 108:213–221.PubMedGoogle Scholar
  3. Bauer, G. R., Croll, F. J. T., Goldrick, R. B., Jeremy, D., Raftos, J., Whyte, H. M., and Young, A. A. 1961. Guanethidine in treatment of hypertension. Br. Med. J., 2:410.PubMedCrossRefGoogle Scholar
  4. Baumgarten, H. G. and Braak, H. 1968. Catecholamine im Gehirn der Eidechse (Lacerta viridis und Lacerta muralis). Z. Zellforsch., 86:574–602.PubMedCrossRefGoogle Scholar
  5. Baumgarten, H. G., Holstein, A. F., and Owman, Ch. 1970. Auerbach’s plexus of mammals and man: electronmicroscopic 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.PubMedCrossRefGoogle Scholar
  6. Baumgarten, H. G., Lachenmayer, L., and Schlossberger, H. G. 1972. Evidence for a degeneration of indoleamine containing nerve terminals in rat brain induced by 5,6-dihydroxytryptamine. Z. Zellforsch., 125:553–569.PubMedCrossRefGoogle Scholar
  7. Bell, C. 1969. Transmission from vasoconstrictor and vasodilator nerves to single smooth muscle cells of the guinea-pig uterine artery. J. Physiol. (Lond.), 205:695–708.Google Scholar
  8. Bennett, M. R. and Burnstock, G. 1968. Electrophysiology of the innervation of intestinal smooth muscle. In: Handbook of Physiology, Section 6. Alimentary Canal, IV. Motility, pp. 1709–1732. American Physiological Society, Washington, D.C.Google Scholar
  9. Bennett, M. R. and Merrillees, N. C. R. 1966. An analysis of the transmission of excitation from autonomic nerves to smooth muscle. J. Physiol. (Lond.), 755:520–535.Google Scholar
  10. Bennett, M. R. and Rogers, D. C. 1967. A study of the innervation of the taenia coli. J. Cell. Biol., 33:573–596.PubMedCrossRefGoogle Scholar
  11. Bennett, T. and Cobb, J. L. S. 1969. Studies on the avian gizzard. Auerbach’s plexus. Z. Zellforsch., 99:109–120.PubMedCrossRefGoogle Scholar
  12. Bennett, T., Burnstock, G., Cobb, J. L. S., and Malmfors, T. 1970. An ultrastructural and histochemical study of the short term effects of 6-hydroxydopamine on adrenergic nerves in the domestic fowl. Br. J. Pharmacol. 35:802–809.CrossRefGoogle Scholar
  13. Bennett, T., Cobb, J. L. S., and Malmfors, T. 1971. Experimental studies on Auerbach’s plexus, with particular reference to the adrenergic component. Referred to in Burnstock and Iwayama (1971).Google Scholar
  14. Bisby, M. A. and Fillenz, M. 1971. The storage of endogenous noradrenaline in sympathetic nerve terminals J. Physiol. (Lond.), 215:163–179.Google Scholar
  15. Bloom, F. E. 1970. The fine structural localization of biogenic monoamines in nervous tissue. Int. Rev. Neurobiol., 13:21–66.Google Scholar
  16. Bloom, F. E. and Barrnett, R. J. 1966. Fine structural localization of noradrenaline in vesicles of autonomic nerve endings. Nature. (Lond.), 270:599–601.CrossRefGoogle Scholar
  17. Bloom, F. E. and Giarman, N. J. 1967. Fine structure of granular vesicles in pineal autonomic nerve endings after serotonin depletion. Anat. Rec., 757:351.Google Scholar
  18. Bloom, F. E., Algeric, S., Groppetti, A., Revuelta, A., and Costa, E. 1969. Lesions of central norepinephrine terminals with 6-OH-dopamine: Biochemistry and fine structure. Science (N.Y.), 166:1284–1286.CrossRefGoogle Scholar
  19. Bondaref, T W. and Gordon, B. 1966. Submicroscopic localization of norepinephrine in sympathetic nerves of rat pineal. J. Pharmacol. Exp. Ther., 153: 42–47.Google Scholar
  20. Boyde, A., James, D. W., Tresman, R. L., and Willis, R. A. 1968. Outgrowth of chick embryo spinal cord in vitro, studied with the scanning electron microscope. Z. Zellforsch., 90:1–18.PubMedCrossRefGoogle Scholar
  21. Budd, G. C. 1971. Recent developments in light and electron microscope autoradiography. Int. Rev. Cytol., 37:21–56.CrossRefGoogle Scholar
  22. Burn, J. H. 1971. Release of noradrenaline from sympathetic endings. Nature. (Lond.), 237:237–240.CrossRefGoogle Scholar
  23. Burn, J. H. and Rand, M. J. 1959. Sympathetic postganglionic mechanism. Nature. (Lond.), 184:163–165.CrossRefGoogle Scholar
  24. Burn, J. H. and Rand, M. J. 1965. Acetylcholine in adrenergic transmission. Ann. Rev. Pharmacol., 5:163–182.CrossRefGoogle Scholar
  25. Burnstock, G. 1969. Evolution of the autonomic innervation of visceral and cardio-vascular systems in vertebrates. Pharmacol. Rev.,, 27:247–324.Google Scholar
  26. Burnstock G. 1970. Structure of smooth muscle and its innervation. In: Smooth Muscle, pp. 1–69. Ed. by Bülbring, E., Brading, A. P., Jones, A. W., and Tomita, T. Edward Arnold, London.Google Scholar
  27. Burnstock, G. 1971. Neural nomenclature. Nature. (Lond.), 229:282–283.CrossRefGoogle Scholar
  28. Burnstock, G. 1972. Purinergic nerves. Pharmacol. Rev.,, 24:509–581.PubMedGoogle Scholar
  29. Burnstock, G. 1974. Purinergic transmission. In Handbook of Neuropsychopharmacology. Eds. L. Iversen, S. Iversen, and S. Snyder. Vol. 1. Plenum Press, N.Y. (in Press).Google Scholar
  30. Burnstock, G., and Iwayama, T. 1971. Fine structural identification of autonomic nerves and their relation to smooth muscle. In: Histochemistry of Nervous Transmission, Progress in Brain Research, Vol. 34, pp. 389–404. Elsevier, Amsterdam.Google Scholar
  31. Burnstock, G. and Robinson, P. M. 1967. Localization of catecholamines and acetylcholinesterase in autonomic nerves. Circ. Res., 21(Suppl. 3):43–55.Google Scholar
  32. Burnstock, G., Campbell, G., Satchell, D. G., and Smythe, A. 1970a. Evidence that adenosine triphosphate or a related nucleotide is the transmitter substance released by non-adrenergic inhibitory nerves in the gut. Br. J. Pharmacol., 40:668–688.PubMedCrossRefGoogle Scholar
  33. Burnstock, G., Gannon, B. J., and Iwayama, T. 1970b. Sympathetic innervation of vascular smooth muscle in normal and hypertensive animals. In: Symp. on Hypertensive Mechanisms, Circ. Res., 27(Suppl. II):5–24.Google Scholar
  34. Burnstock, G., Doyle, A. E., Gannon, B. J., Gerkins, J. F., Iwayama, T., and Mashford, M. L. 1971a. Prolonged hypotension and ultrastructural changes in sympathetic neurones following guanacline treatment. Eur. J. Pharmacol., 13:175–187.PubMedCrossRefGoogle Scholar
  35. Burnstock, G., Evans, B., Gannon, B. J., Heath, J., and James, V. 1971b. A new method for destroying adrenergic nerves in adult animals using guanethidine. Br. J. Pharmacol., 295–301.Google Scholar
  36. Burt, A. M. 1971. The histochemical localization of choline acetyltransferase. In: Progress in Brain Research, Vol. 34, pp. 327–335. Elsevier, Amsterdam.Google Scholar
  37. Campbell, G. 1970. Autonoic nervous supply to effector tissues. In: Smooth Muscle, pp. 451–495. Ed. by Bülbring, E., Brading, A. F., Jones, A. W., and Tomita, T. Edward Arnold, London.Google Scholar
  38. Campbell, G. R., Uehara, Y., Mark, G., and Burnstock, G. 1971. Fine structure of smooth muscle cells grown in tissue culture. J. Cell Biol., 49:21–34.PubMedCrossRefGoogle Scholar
  39. Carr, K. E. 1972. Applications of scanning electronmicroscopy in biology. In: International Review of Cytology, Vol. 30, pp. 183–255. Ed. by Borne, G. H., Danielli, J. F., and Jeon, K. W. Academic Press, New York and London.Google Scholar
  40. Castaing, R. 1951. Ph.D. Dissertation, University of Paris.Google Scholar
  41. Chandler, J. A. 1972. An introduction to analytical electron microscopy. Micron, 3:85–92.CrossRefGoogle Scholar
  42. Clementi, F., Montegazza, P., and Botturi, M. 1966. A pharmacologic and morphologic study on the nature of the dense-core granules present in the presynaptic endings of sympathetic ganglia. Int. J. Neuropharmacol., 5:281–285.PubMedCrossRefGoogle Scholar
  43. Dawborn, J. K., Doyle, A. E., Ebringer, A., Howqua, J., Jerums, G., Johnston, C. I., Mashford, M. L., and Perkin, J. D. 1969. Persistent postural hypotension due to guanacline. Pharmacol. Clin., 2:1.CrossRefGoogle Scholar
  44. De Potter, W. P., Smith, A. D., and De Schaepdryver, A. F. 1970. Subcellular fractionation of splenic nerve: ATP, chromogranin A and dopamine-β-hydroxylase in noradrenergic vesicles. Tissue and Cell, 2:529–546.PubMedCrossRefGoogle Scholar
  45. De Robertis, E. and Bennett, H. S. 1955. Some features of the submicroscopic morphology of synapses in frog and earthworm. J. Biophys. Biochem. Cytol., 7:47–58.CrossRefGoogle Scholar
  46. Descarries, L. and Droz, B. 1970. Intraneural distribution of exogenous norephrine in the central nervous system of the rat. J. Cell Biol., 44:385–399.PubMedCrossRefGoogle Scholar
  47. Devine, C. E. and Simpson, F. O. 1967. The fine structure of vascular sympathetic neuromuscular contacts in the rat. Am. J. Anat., 121:153–174.PubMedCrossRefGoogle Scholar
  48. Devine, C. E. and Simpson, F. O. 1968. Localization of tritiated norepinephrine in vascular sympathetic axons of the rat intestine and mesentery by electron microscope radioautography. J. Cell Biol., 184–192.Google Scholar
  49. Devine, C. E., Simpson, F. O., and Bertaud, W. S. 1971. Surface features of smooth muscle cells from the mesenteric artery and vas deferens. J. Cell Sci., <5:427–443.Google Scholar
  50. Dewey, M. M. and Barr, L. 1962. Intercellular connection between smooth muscle cells: the nexus. Science (N.Y.), 137:610–612.CrossRefGoogle Scholar
  51. Duncumb, P. 1966. Precipitation studies with EMMA—A combined electron microscope and x-ray microanalyzer. In: The Electron Microprobe, pp. 490–499. Ed. by McKinley, T. D., Heinrich, K. F. J., and Wittry, D. B. Wiley, New York.Google Scholar
  52. Ehinger, B., and Falck, B. 1971. Autoradiography of some suspected neurotransmitter substances: gaba glycine, glutamic acid, histamine, dopamine and L-dopa. Brain Res., 33:157–172.PubMedCrossRefGoogle Scholar
  53. Eränkö, O., Ed. 1971. Histochemistry of Nervous Transmission. Progress in Brain Research, Vol. 34. Elsevier, Amsterdam.Google Scholar
  54. Eränkö, L. and Eränkö, O. 1971. 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.CrossRefGoogle Scholar
  55. Eränkö L. and Eränkö, O.1972. Effect of 6-hydroxydopamine on the ganglion ceils and the small intensely fluorescent cells in the superior cervical ganglion of the rat. Acta. Physiol. Scand., 84:115–124.PubMedCrossRefGoogle Scholar
  56. Eränkö, O., Rechardt, L., Eränkö, L., and Cunningham, A. 1970. Light and electron microscopic histo- chemical observations on cholinesterase-containing sympathetic nerve fibres in the pineal body of the rat. Histochem. J., 2:479–489.PubMedCrossRefGoogle Scholar
  57. Euler, U. S. von and Hillarp, N.-Ä. 1956. Evidence for the presence of noradrenaline in submicroscopic structures in adrenergic axons. Nature. (Lond.), 177:44–45.CrossRefGoogle Scholar
  58. Evans, B. K., Armstrong, S., Cook, R. D., Singer, G., and Burnstock, G. 1975. Intracranial injection of drugs: comparison of diffusion of 6-OHDA and guanethidine. Pharmac. Biochem. Behav. (in press).Google Scholar
  59. Evans, B. K., Gannon, B. J., Heath, J. W., and Burnstock, G. 1972. Long-lasting damage to the internal male genital organs and their adrenergic innervation following chronic treatment of rats with the antihypertensive drug guanethidine. Fertil. Steril, 23:651–661.Google Scholar
  60. Farrell, K. E. 1968. Fine structure of nerve fibres in smooth muscle of the vas deferens in normal and reserpinized rats. Nature. (Lond.), 277:279–281.CrossRefGoogle Scholar
  61. Furness, J. B. and Burnstock, G. 1969. A comparative study of spike potentials in response to nerve stimulation in the vas deferens of the mouse, rat and guinea-pig. Comp. Biochem. Physiol., 31:337–345.PubMedCrossRefGoogle Scholar
  62. Furness, J. B., Campbell, G. R., Gillard, S. M., Malmfors, T., and Burnstock, G. 1970. Cellular studies of sympathetic denervation produced by 6-hydroxydopamine in the vas deferens. J. Pharmacol. Exp. Ther., 174:111–122.PubMedGoogle Scholar
  63. Furness, J. B. and Iwayama, T. 1971. Terminal axons ensheathed in smooth muscle cells of the vas deferens. Z. Zellforsch., 113:259–210.PubMedCrossRefGoogle Scholar
  64. Fuxe, K., Hökfelt, T., and Nilsson, O.1965. A fluorescence and electronmicroscopic study on certain brain regions rich in minoamine terminals. Am. J. Anat., 777:33–45.CrossRefGoogle Scholar
  65. Gannon, B. J., Iwayama, T., Burnstock, G., Gerkens, J., and Mashford, M. L. 1971. Prolonged effects of chronic guanethidine treatment on the sympathetic innervation of the genitalia of male rats. Med. J. Aust., 2:201–208.Google Scholar
  66. Geffen, L. B. and Livett, B. G. 1971. Synaptic vesicles in sympathetic neurons. Physiol. Rev., 57:98–157.Google Scholar
  67. Grillo, M. A. 1966. Electronmicroscopy of sympathetic tissues. Pharmacol. Rev.,, 75:387–399.Google Scholar
  68. Gross, W., Bracharz, H., and Laas, H. 1965. Vergleichende klinischtherapeutische Erfahrungen beim Hochdruck. In: Hochdruckforschung, Fortschritte auf dem Gebiete der Inneren Medizin, II, Symposium held in Freiburg i Br., July 18 and 19, 1964, George Thieme, Stuttgart.Google Scholar
  69. Hagen, E. and Wittkowski, W. 1969. Licht- und electronen-mikroskopische Untersuchung zur Innervation der Piagefasse. Z. Zellforsch., 95:429–444.PubMedCrossRefGoogle Scholar
  70. Hall, T. A., Haie, A. J., and Switsur, V. R. 1966. Some applications of microprobe analysis in biology and medicine. In: The Electron Microprobe, pp. 805–833. Ed. by McKinley, T. D., Heinrich, K. F. J., and Wittry, D. B. Wiley, New York.Google Scholar
  71. Hayat, M. A. 1970. Principles and Techniques of Electron Microscopy: Biological Applications, Vol. I. Van Nostrand Reinhold, New York.Google Scholar
  72. Heath, J. W., Evans, B., Gannon, B. J., Burnstock, G., and James, V. 1972. Degeneration of adrenergic nerves following guanethidine: an ultrastructural study. Virchow. Arch. Abt. 3 Zellpath. B., 11: 182–197.Google Scholar
  73. Heath, J. W., Hill, C. E., and Burnstock, G. 1974. Axon retraction following guanethidine treatment. Studies of sympathetic neurons in tissue culture. J. Neurocytol., 1: 263–276.CrossRefGoogle Scholar
  74. Hebb, C., Kasa, P., and Mann, S. 1968. The relation between nerve fibres and dopamine cells of the ruminant lung. Histochem. J., 7:166–175.CrossRefGoogle Scholar
  75. Hill, C. E., Chamley, J., and Burnstock, G. 1974. Cell surface and fibre relationships in sympathetic ganglion cultures: a scanning electron microscope study. J. Cell Sci., 14:651–669.Google Scholar
  76. Hökfelt, T. 1966. The effect of reserpine on the intraneuronal vesicles of the rat vas deferens. Experientia, 22:56–57.PubMedCrossRefGoogle Scholar
  77. Hökfelt, T. 1968. In vitro studies on central and peripheral monoamine neurons at the ultrastructural level. Z. Zellforsch., 91:1–74.PubMedCrossRefGoogle Scholar
  78. Hökfdt, T., 1969. Distribution of noradrenaline storing particles in peripheral adrenergic neurons as revealed by electron microscopy. Acta Physiol. Scand.,, 76:427–440.CrossRefGoogle Scholar
  79. Hökfelt, T. 1971. Ultrastructural localization of intraneuronal monoamines —some aspects on methodology. Progress in Brain Research, Vol. 34, pp. 213–222. Elsevier, Amsterdam.Google Scholar
  80. Hökfelt, T. and Jonsson, G. 1968. Studies on reaction and binding of monoamines after fixation and processing for electron microscopy with potassium permanganate. Histochemie, 76:45–67.Google Scholar
  81. Hökfelt, T. and Nilsson, O. 1965. The relationship between nerves and smooth muscle cells in the rat iris. Z. Zellfor 66:848–853.CrossRefGoogle Scholar
  82. Ivanov, D. P. 1971. Connexions neuro-musculaires specialisees dans le canal deferent du rat. J. Neuro- Viscer. Relat., i2:143.CrossRefGoogle Scholar
  83. Iwayama, T. and Furness, J. B. 1971. Enhancement of the granulation of adrenergic storage vesicles in drug-free solution. J. Cell Biol., 699–703.Google Scholar
  84. Iwayama, T., Furness, J. B., and Burnstock, G. 1970. Dual adrenergic and cholinergic innervation of the cerebral arteries of the rat. An ultrastructural study. Circ. Res. 26:635–646.Google Scholar
  85. Iwayama, T., Fleming, W. W., and Burnstock, G. 1972. Ultrastructure of mitochondria in atrial muscle associated with depression and supersensitivity produced by reserpine. J. Pharmacol. Exp. Ther., 184:95–105.Google Scholar
  86. Jacob, J. 1971. The practice and application of electron microscope autoradiography. Int. Rev. Cytol., 30:91–174.PubMedCrossRefGoogle Scholar
  87. Jaim Etcheverry, G. and Zieher, L. M. 1968a. Cytochemistry of 5-hydfoxytryptamine at the electron microscope level. I. Study of the specificity of the reaction in isolated blood platelets. J. Histochem. Cytochem., 16:162–171.CrossRefGoogle Scholar
  88. Jaim Etcheverry, G. and Zieher, L. M. 1968b. Cytochemistry of 5-hydroxytryptamine at the electron microscope level. Z. Zellforsch., 86:393–400.CrossRefGoogle Scholar
  89. Jensen-Holm, J. and Juul, P. 1970. Ultrastructure of rat sympathetic ganglia following guanethidine. Acta Pharmacol. Toxicol., 25(Suppl. 1):56.Google Scholar
  90. Karnovsky, M. J. 1964. The localization of Cholinesterase activity in rat cardiac muscle by electron microscopy. J. Cell Biol., 21: 217–233.CrossRefGoogle Scholar
  91. Kasa, P. 1971. Ultrastructural localization of choline acetyltransferase and acetylcholinesterase in central and peripheral nervous tissue. In: Histochemistry of Nervous Transmission. Progress in Brain Research, Vol. 34, pp. 337–344. Ed. by Eränkö, O. Elsevier, Amsterdam.Google Scholar
  92. Kasa, P. and Csillik, B. 1966. Electron microscopic localization of Cholinesterase by a copper-lead-thio- choline technique. J. Neurochem., 13:1345–1349.PubMedCrossRefGoogle Scholar
  93. Koelle, G. B. and Friedenwald, J. S. 1949. A histochemical method for localizing Cholinesterase activity. Proc. Soc. Exp. Biol., 70:617–622.PubMedGoogle Scholar
  94. Kröneberg, G., Schlossmann, K., and Stoepel, K. 1967. Zur pharmakologie von N-(2-guanidinöchyl)-4- methyl-1,2,3,6-tetrahydro-pyridin, einer neuen antihypertensiv wirkenden Verbindung. Arzneimittel- Forsch., 17:199.Google Scholar
  95. Kubozoe, T., Daikoku, S., and Takita, S. 1969. Electronmicroscopic observations on Auerbach’s plexus in a 12 mm human embryo. J. Neuro-vise. Rel., J7:291–307.CrossRefGoogle Scholar
  96. Lacy, D. and Pettitt, A. J. 1972. Biological applications of combined transmission electron microscopy and x-ray microanalysis with special reference to studies on the mammalian testis. Micron, 3:115–129.CrossRefGoogle Scholar
  97. Lagercrantz, H. 1971. Isolation and characterization of sympathetic nerve trunk vesicles. Acta. Physiol. Scand. 82(Suppl. 366): 1–44.Google Scholar
  98. Lane, B. P. 1967. Localization of products of ATP hydrolysis in mammalian smooth muscle cells. J. Cell Biol., 34:713–720.PubMedCrossRefGoogle Scholar
  99. Lane, B. P. and Rhodin, J. A. G. 1964. Cellular interrelationships and electrical activity in two types of smooth muscle. J. Ultrastruct. Res., 10:470–488.PubMedCrossRefGoogle Scholar
  100. Lever, J. D., Graham, J. D. P., Irvine, G., and Chick, W. J. 1965. The vesiculated axons in relation to arteriolar smooth muscle in the pancreas. A fine structural and quantitative study. J. Anat., 99:299–313.PubMedGoogle Scholar
  101. Lever, J. D., Spriggs, T. L. B., and Graham, J. D. P. 1968. A formol-fluorescence fine-structural and auto-radiographic study of the adrenergic innervation of the vascular tree in the intact and sympathectomized pancreas of the cat. J. Anat., 103:15–34.PubMedGoogle Scholar
  102. Malmfors, T. and Thoenen, H. 1971. 6-Hydroxydopamine and Catecholamine Neurons. North Holland, Amsterdam, London.Google Scholar
  103. Marshall, D. J., Hall, T. A., and Hale, A. J. 1967. Optique des Rayons X et Micro-analyse. Hermann, Paris.Google Scholar
  104. Merrillees, N. C. R. 1968. The nervous environment of individual smooth muscle cells of the guinea-pig vas deferens. J. Cell Biol., 17:794–817.CrossRefGoogle Scholar
  105. Merrillees, N. C. R., Burnstock, G., and Holman, M. E. 1963. Correlation of fine structure and physiology of the innervation of smooth muscle in the guinea-pig vas deferens. J. Cell Biol., 79:529–550.CrossRefGoogle Scholar
  106. Moor, H. 1964. Freeze-etching technique. J. Appl. Phys. 35:3077.Google Scholar
  107. Moor, H. 1966. Use of freeze etching in the study of biological ultrastructure. Int. Rev. Exp. Pathol., 5:179–216.PubMedGoogle Scholar
  108. Moor, H. and Mühlethaler, K. 1963. Fine structure in frozen-etched yeast cells. J. Cell Biol., 17:609–628.PubMedCrossRefGoogle Scholar
  109. Nagasawa, J. and Mito, S. 1967. Electron microscope observations on the innervation of the smooth muscle. Tohoku. Exp. Med., 97:277–293.CrossRefGoogle Scholar
  110. Nilsson, O. 1964. The relationship between nerves and smooth muscle cells in the rat iris. I. The dilator muscle. Z. Zellforsch., 64:166–171.Google Scholar
  111. Owman, Ch. and Sjöstrand, N. O. 1965. Short adrenergic neurons and catecholamine-containing-cells in vas deferens and accessory male genital glands of different mammals. Z. Zellforsch., 66:300–320.PubMedCrossRefGoogle Scholar
  112. Paul, D., Grobe, A., Zimmer, F. 1970. Autoradiography in the scanning electron microscope. Nature. (Lond.), 277:488–489.CrossRefGoogle Scholar
  113. Pellegrinode Iraldi, A., Guedet, R., and Suburo, A. M. 1971. Differentiation between 6-hydroxytryptamine and catecholamines in synaptic vesicles. In: Histochemistry of Nervous Transmission. Progress in Brain Research, Vol. 34, pp. 161–170. Ed. by Eränkö, O. Elsevier, Amsterdam.Google Scholar
  114. Pick, J., De Lemos, C., and Ciannella, A. 1967. Fine structure of nerve terminals in the human gut. Anat. Rec., 159:131–138.CrossRefGoogle Scholar
  115. Richardson, K. C. 1962. The fine structure of autonomic nerve endings in smooth muscle of the rat vas deferens. J. Anat., 96:427–442.PubMedGoogle Scholar
  116. Richardson, K. C. 1966. Electronmicroscopic identification of autonomic nerve endings. Nature. (Lond.), 210:156.CrossRefGoogle Scholar
  117. Robertson, A. J. 1968. The electron probe microanalyser and its application in medicine. Phys. Med. Biol., 13:505–522.PubMedCrossRefGoogle Scholar
  118. Robinson, P. M. 1969. A cholinergic component in the innervation of the longitudinal smooth muscle of the guinea-pig vas deferens: the fine structural localization of acetylcholinesterase. J. Cell Biol., 47:462–476.CrossRefGoogle Scholar
  119. Robinson, P. M. 1971. The demonstration of acetylcholinesterase in autonomic axons with the electron microscope. In: Histochemistry of Nervous Transmission. Progress in Brain Research, Vol. 34, pp. 357–370. Ed. by Eränkö, O. Elsevier, Amsterdam.Google Scholar
  120. Robinson, P. M., McLean, J. R., and Burnstock, G. 1971. Ultrastructural identification of non-adrenergic inhibitory nerve fibres. J. Pharmacol. Exp. Ther., 779:149–160.Google Scholar
  121. Rogers, A. W. 1971. Recent developments in the use of autoradiographic techniques with electron microscopy. Phil. Trans. R. Soc. Lond. B, 267:159–171.CrossRefGoogle Scholar
  122. Rogers, D. and Burnstock, G. 1966. Multiaxonal autonomic junctions in intestinal smooth muscle of the toad (Bufo marinus). J. Comp. Neurol., 726:625–652.Google Scholar
  123. Rosenbloom, S. E., Shadera, R. P., Goldbloom, R. S., Sheps, M. C., and Shapiro, A. P. 1963. Technic of controlled drug assay. III. Comparison of guanethidine, mecanylamine, and a placebo in the hypertensive patient. New Engl. J. Med., 268:797–803.PubMedCrossRefGoogle Scholar
  124. Rostgaard, J. and Barrnett, R. J. 1964. Fine structure localization of nucleotide phosphatases in relation to smooth muscle cells and unmyelinated nerves in the small intestine of the rat. J. Ultrastruct. Res., 11:193–207.PubMedCrossRefGoogle Scholar
  125. Sah, H. J., Sah, P. P. T., and Peoples, S. A. 1966. The new antihypertensive agent guanethidine—a review. Part II. Clinical uses/Dosage routes of administration/Side effects/Important notes/Summary/ Bibliography. Arzneimittelforsch., 16: 199–202.PubMedGoogle Scholar
  126. Salpeter, M. M. and Paeder, I. 1971. The role of sheath cells in glutamate uptake by insect nerve muscle preparations. In. Histochemistry of Nervous Transmission. Progress in Brain Research, Vol. 34, pp. 103–114. Ed. by Eränkö, O. Elsevier, Amsterdam.Google Scholar
  127. Satchell, D. G. and Burnstock, G. 1971. Quantitative studies of the release of purine compounds following stimulation of non-adrenergic inhibitory nerves in the stomach. Biochem. Pharmacol., 20:1694–1697.CrossRefGoogle Scholar
  128. Schümann, H. J. and Philippu, A. 1968. Die Wirkung von Cyclazenin auf dei Speicherung und Freisetzung sympathicomimetisher Amine im Herzen. Arzneimittel-Forsch., 18:1571–1574.Google Scholar
  129. Silva, D. G., Farrall, K. E., and Smith, G. C. 1968. Ultrastructural and histochemical studies on the innervation of the mucous membrane of the mouse colon. Anat. Rec., 162:157–176.PubMedCrossRefGoogle Scholar
  130. Sjöstrand, F. S. 1967. Electron microscopy of cells and tissues. In: Instrumentation and Techniques, Vol. 1. Academic Press, New York.Google Scholar
  131. Steere, R. L. 1957. Electron microscopy of structural detail in frozen biological specimens. J. Biophys. Biochem. Cytol., 3: 45–60.PubMedCrossRefGoogle Scholar
  132. Su, C., Bevan, J., and Burnstock, G. 1971. (3H) Adenosine triphosphate: Release during stimulation of enteric nerves. Science (N.Y.), 173:337–339.CrossRefGoogle Scholar
  133. Taxi, J. 1965. Contribution ä I’etude des connexions des neurones moteurs du systeme nerveux autonome. Ann. Sci. Nature.lles Zoologie, 12e serie, VII: 413–674.Google Scholar
  134. Taxi, J. 1969. Morphological and cytochemical studies on the synapses in the autonomic nervous system. In: Progress in Brain Research, Vol. 31, pp. 5–20. Elsevier, Amsterdam.Google Scholar
  135. Taxi, J. and Droz, B. 1966. Etude de I’incorporation de noradrenaline-3H(NA-3H) et de 5-hydroxy- tryptophane-3H (5 HTP-3H) dans les fibres nerveuses du canal deferent et de I’intestin. C R. Acad. Sci. D, 263:1237–1240.Google Scholar
  136. Tennyson, V. M., Brzin, M., and Duffy, P. E. 1965. Electron microscopic localization of acetylcholinesterase in the neurons of frog sympathetic ganglia. J. Cell Biol., 27:105–106 A.Google Scholar
  137. Thaemert, J. C. 1963. The ultrastructure and disposition of vesiculated nerve processes in smooth muscle. J. Cell Biol., 16:361–377.PubMedCrossRefGoogle Scholar
  138. Thaemert, J. C. 1966. Ultrastructural interrelationships of nerve processes and smooth muscle cells in three dimensions. J. Cell Biol., 28:37–49.PubMedCrossRefGoogle Scholar
  139. Thoenen, H., Tranzer, J. P., Hürlimann, A., and Haefely, W. 1966. Untersuchungen zur Frage eines cholinergischen Gliedes in der postganglionären sympathischen Transmission. Helv. Physiol. Pharmac. Acta, 24:229–246.Google Scholar
  140. Thoenen, H., Haefely, W., Gey, K. F., and Hürhmann, A. 1967. Diminished effect of sympathetic nerve stimulation in cats pretreated with 5-hydroxydopa: formation and liberation of false adrenergic transmitters. Arch. Exp. Pathol. Pharmakol., 259:17–33.CrossRefGoogle Scholar
  141. Tranzer, J. P. and Thoenen, H. 1967. Electronmicroscopic localization of 5-hydroxydopamine (3,4,5- trihydroxy-phenylethylamine), a new “false” sympathetic transmitter. Experientia, 23: 743–745.PubMedCrossRefGoogle Scholar
  142. Tranzer, J. P. and Thoenen, H. 1968a. An electron microscopic study of selective acute degeneration of sympathetic nerve terminals after administration of 6-hydroxydopamine. Experientia, 24:155–156.PubMedCrossRefGoogle Scholar
  143. Tranzer, J. P. and Thoenen, H. 1968b. Various types of amine-storing vesicles in peripheral adrenergic nerve terminals. Experientia, 34:484–486.CrossRefGoogle Scholar
  144. Tranzer, J. P., Thoenen, H., Snipes, R., and Richards, J. 1969. Recent developments on the ultrastructural aspect of adrenergic nerve endings in various experimental conditions. In: Progress in Brain Research, Vol. 31, pp. 33–46. Elsevier, Amsterdam.Google Scholar
  145. Uehara, Y. and Burnstock, G. 1972. Postsynaptic specialization of smooth muscle at close neuromuscular junctions in the guinea-pig sphincter pupillae. J. Cell Biol., 53: 849–853.PubMedCrossRefGoogle Scholar
  146. Ungerstedt, U. 1968. Efforts of 6-Hydroxydopamine induced degeneration of central monoamine neurons. Eur. J. Pharmacol., 5:107–110.PubMedCrossRefGoogle Scholar
  147. Uretsky, N. J. and Iversen, L. L. 1970. Effects of 6-hydroxydopamine on catecholamine containing neurons in the cat brain. J. Neurochem., 77:269–278.CrossRefGoogle Scholar
  148. Van Orden III L. S., Bensch, K. G., and Giarman, N. J. 1967. Histochemical and functional relationships of catecholamines in adrenergic nerve endings. II Extra vesicular norepinephrine. J. Pharmacol. Exp. Ther., 755:428–439.Google Scholar
  149. Van Orden III L. S., Bloom, F. E., Barrnett, R. J., and Giarman, N. J. 1966. Histochemical and functional relationships of catecholamines in adrenergic nerve endings. I. Participation of granular vesicles. J. Pharmacol. Exp. Ther., 754:185–199.Google Scholar
  150. Vejlsgaard, V., Christensen, M., and Clausen, E. 1967. Double-blind trial of four hypotensive drugs (Methyldopa and three sympatholytic agents). Br. Med. J., 2:598.PubMedCrossRefGoogle Scholar
  151. Watanabe, H. 1969. Electron microscopic observations on the innervation of smooth muscle in the guinea- pig vas deferens. Acta. Anat. Nippon., 189–202.Google Scholar
  152. Whittaker, V. P. 1966. Catecholamine storage particles in the central nervous system. Pharmacol. Rev.,, 18:401–412.PubMedGoogle Scholar
  153. Whittaker, V. P., Michaelson, I. A., and Kirkland, R. J. A. 1964. The separation of synaptic vesicles from nerve-ending particles (“synaptosomes”). Biochem. J., 90:293–303.PubMedGoogle Scholar
  154. Wilson, B. W., Schenkel, J. L., and Fry, D. M. 1971. Acetylcholinesterase, isoenzymes and the maturation of normal and dystrophic muscle. In: Cholinergic Ligand Interactions. Ed. by Triggle, Moran, and Barnard.Google Scholar
  155. Wolfe, D. E., Potter, L. T., Richardson, K. C., and Axelrod, J. 1962. Localizing tritiated norepinephrine in sympathetic axons by electronmicroscopic autoradiography. Science (N.Y.), 138:440–442.CrossRefGoogle Scholar
  156. Yamauchi, A. and Burnstock, G. 1969. Postnatal development of the innervation of the mouse vas deferens. A fine structural study. J. Anat. Lond., 104:17–32.Google Scholar

Copyright information

© Plenum Press, New York 1975

Authors and Affiliations

  • G. Burnstock
    • 1
  1. 1.Department of ZoologyUniversity of MelbourneAustralia

Personalised recommendations