Nonadrenergic, Noncholinergic (NANC) Neuronal Inhibitory Interactions with Smooth Muscle

  • E. E. Daniel
Part of the Contemporary Biomedicine book series (CB, volume 5)

Abstract

Nonadrenergic, noncholinergic nerves innervating smooth muscle were first clearly recognized in the guinea-pig taenia caecum by Burnstock et al. (22), Holman and Hughes (90), Bennett et al. (14), and Bennett and Burnstock (12). These nerves were inhibitory, causing hyperpolarization of the membrane potential and relaxation of contractile activity, and were not susceptible to atropine or other muscarinic cholinergic antagonists, to adrenergic antagonists of either alpha- or beta-receptor effects, or to adrenergic neuronal blocking agents such as guanethidine, to antagonists of serotonin, histamine, or inhibitors of prostaglandin synthesis. The definition of nonadrenergic, noncholinergic nerves was one of exclusion, based on absence of evidence for a particular transmitter. Subsequently, Burnstock and his colleagues (for review, see refs. 19,20) have marshalled evidence for ATP or another purine as transmitter whereas others (e.g., 65 and 75) have suggested the existence of a peptidergic transmission, usually with VIP as the putative transmitter in this subset of NANC nerves. As will become apparent, there is reason to remain skeptical of both identifications, and we shall retain the negative term, nonadrenergic, noncholinergic, and abbreviate it as NANC.

Keywords

Norepinephrine Propranolol Adenine Indomethacin Triphosphate 

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References

  1. 1.
    Alumets, J., R. Hakanson, F. Sundler, and R. Uddman. VIP-, enkephalin-, substance P- and somatostatin-like immunoreactivity in neurons intrinsic to the intestine. Immunohistochemical evidence from organotypic tissue cultures. Brain Res. 155: 239–248, 1978.Google Scholar
  2. 2.
    Ambache, N. Unmasking after cholinergic paralysis by botulinum toxin of a reversed action of nicotine on the mammalian intestine revealing the probable presence of local inhibitory ganglion cells in the enteric plexuses. Br. J. Pharmacol. 6: 51–67, 1951.Google Scholar
  3. 2a.
    Axelsson J. B. Holmberg. The effects of extracellularly applied ATP and related compounds on electrical and mechanical activity of the smooth muscle taenia coli from the guinea-pig. Acta Physiol. Scand. 75: 149–156, 1969.PubMedGoogle Scholar
  4. 3.
    Baer, H. P., R., Frew, and G. Burnstock. Effect of dipyridamole and 6-(2-hydroxy-5-nitrobenzyl-thioguanosine) on low frequency-stimulated relaxation in the guinea pig taenia coli, Can. J. Physiol. Pharmacol. 55: 394–398, 1977.PubMedGoogle Scholar
  5. 4.
    Baer, H. P. and R. Frew. Relaxation of guinea pig fundic strip by adenosine, adenosine triphosphate and electrical stimulation; lack of antagonism by theophylline or ATP treatment. Br. J. Pharmacol. 67: 293–299, 1979.PubMedGoogle Scholar
  6. 5.
    Bartlett, V., R. R. Steward and K. Nakatsu. Evidence for two adenine derivative receptors in the rat ileum which are not involved in the non-adrenergic, non-cholinergic response. Can. J. Physiol. Pharmacol. 57: 1130–1137, 1979.PubMedGoogle Scholar
  7. 6.
    Banks, B. E. C., C. Brown, G. M. Burgess, G. Burnstock, M. Claret, T. M. Cocks and D. H. Jenkinson. Apamin blocks certain neurotransmitter-induced increases in potassium permeability. Nature 282: 415–417, 1979.PubMedGoogle Scholar
  8. 7.
    Bauer, V. and H. Kuriyama. Evidence for non-cholingeric, nonadrenergic transmission in the guinea pig ileum. J. Physiol. (Lond.) 330: 95–110, 1982.Google Scholar
  9. 8.
    Bauer, V., O. Matusak, and H. Kuriyama. Non-cholinergic, nonadrenergic responses to nerve stimulation of different regions of the guinea pig small intestine. Naunyn-Schmiedeberg’s Arch. Pharmacol. 319: 108–114, 1982b.Google Scholar
  10. 9.
    Bauer, V., O. Matusak, H. Kuriyama, M. Bezekova, and L. Benes. Role of Ca’ in non-cholinergic, non-adrenergic responses to nerve stimulation. Naunyn-Schmiedeberg’s Arch. Pharmacol. 319: 115–120, 1982a.Google Scholar
  11. 10.
    Bayliss, W. M. and E. H. J. Starling. The movements and innervation of the small intestine. J. Physiol. (Lond.) 24: 99–143, 1899.Google Scholar
  12. 11.
    Beani, L., C. Bianchi, and A. Crema. Vagal non-adrenegic inhibition of guinea pig stomach. J. Physiol. (Lond.) 217: 259–279, 1971.Google Scholar
  13. 11a.
    Beck, C. S. and J. Osa. Membrane activity in guinea-pig gastric sling muscle: a nerve-dependent phenomenon. Am. J. Physiol. 220: 1397–1403, 1971.PubMedGoogle Scholar
  14. 11b.
    Behar, J., S. Field, and C. Marin. Effect of glucagon, secretin and vasoactive intestinal polypeptide on the feline lower esophageal sphineter: mechanisms of action. Gastroenterology 77: 1001–1007, 1979.PubMedGoogle Scholar
  15. 12.
    Bennett, M. R. and Burnstock, G. Electrophysiology of the innervation of intestinal smooth muscle. In Handbook of Physiology—Vol. IV, Section 6. Alimentary Canal. Ed. Code, Cf. Am. Physiol Soc., Washington, D.C. pp 1709–1732, 1968.Google Scholar
  16. 13.
    Bennett, M. R., G. Burnstock, and M. E. Holman. The affect of potassium and chloride ions on the inhibitory potential recorded in the guinea pig taenia coli, J. Physiol. (Lond.) 169: 33P - 34P, 1963.Google Scholar
  17. 14.
    Bennett, M. R., G. Burnstock, and M. E. Holman. Transmission from intramural inhibitory nerves to the smooth muscle of the guinea pig taenia coli, J. Physiol. (Lond.) 182: 541–558, 1966.Google Scholar
  18. 15.
    Berezin, I., M. S. Sheppard, E. E. Daniel and N. Yanaihara. Electron microscopic localization of VIP-like immunoreactivity in dog ileum. Regulatory Peptides. Submitted.Google Scholar
  19. 15a.
    Bianchi, C. L. Beani, G. M. Frigo and A. Crema. Further evidence for the presence of non-adrenergic inhibitory structures in the guinea-pig colon. Eur. J. Pharmacol. 4: 51–61 1968.PubMedGoogle Scholar
  20. 16.
    Bitar, K. N., S. J. Said, G. C. Weir, B. Saffouri, and G. M. Makhlouf. Neutral release of vasoactive intestinal peptide from the gut. Gastroenterology 79: 1288–1294, 1980.PubMedGoogle Scholar
  21. 17.
    Bloom, S. R. and A. V. Edwards, Effects of autonomic stimulation on the release of vasoactive intestinal peptide from the gastro-intestinal tract. J. Physiol. (Lond.) 299: 437–452m 1980.Google Scholar
  22. 18.
    Burks, T. F. and M. N. Grubb. Stimulatory actions of adenosine triphosphate in dog intestine. In Gastrointestinal Motility in Health and Disease. H. J. Duthie, ed. University Part Press, Baltimore, pp 151–159, 1978.Google Scholar
  23. 18a.
    Burleigh, D. E., A. D’Mello, and A. G. Parks. Responses of human internal anal sphincter to drugs and electrical field stimulation. Gastroenterology 77: 484–490, 1979.PubMedGoogle Scholar
  24. 19.
    Burnstock, G. Purinergic Nerves. Pharmacological Rev. 24: 509–581, 1972.Google Scholar
  25. 20.
    Burnstock, G. Past and current evidence for the purinergic nerve hypothesis. In Physiological and Regulating functions of Adenosine and Adenine Nucleotides. H. Bauer and G. I. Diamond, eds. Raven Press, New York, pp 3–32, 1979.Google Scholar
  26. 21.
    Burnstock, G. Neurotransmitters and trophic factors in the autonomic nervous system. J. Physiol. (Lond.) 313: 1–35, 1981.Google Scholar
  27. 22.
    Burnstock, G., G. Campbell, M. Bennett and M. E. Holman. Innervation of the guinea pig taenia coli: Are there intrinsic inhibitory nerves which are distinct from sympathetic nerves? Int. J. Neuropharmacol. 3: 163–166, 1964.PubMedGoogle Scholar
  28. 23.
    Burnstock, G., G. Campbell, D. Satchell, and A. Smythe. 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, 1970.PubMedGoogle Scholar
  29. 24.
    Burnstock, G., T. Cocks, and G. Crowe. Evidence for purinergic innervation of the anococcygeus muscle. Br. J. Pharmacol. 64: 13–20, 1978a.PubMedGoogle Scholar
  30. 25.
    Burnstock, G., T. Cocks, G. Crowe, and L. Kasakov. Purinergic innervation of the guinea pig urinary bladder. Br. J. Pharmacol. 63: 125–138, 1978b.PubMedGoogle Scholar
  31. 26.
    Burnstock, G., T. Cocks, L. Kosakov, and A. Wong. Direct evidence for ATP release from non-adrenergic, non-cholinergic (“purinergic”) nerves in the guinea pig taenia coli and bladder. Eur. J. Pharmacol. 49: 145–149, 1978c.PubMedGoogle Scholar
  32. 26a.
    Burnstock, G., D. G. Satchell and A. Smythe. A comparison of the excitatory and inhibitory effects of non-adrenergic, non-cholinergic nerve stimulation and exogenously applied. ATP on a variety of smooth muscle preparations from different vertebrate species. Br. J. Pharmacol 46: 234–242, 1972.PubMedGoogle Scholar
  33. 27.
    Bywater, R. A. R., M. E. Holman, and G. S. Taylor. Atropine—resistant deplorization in the guinea pig small intestine. J. Physiol. (Lond.) 316: 369–378, 1981.Google Scholar
  34. 28.
    Campbell, G. The inhibitory nerve fibers in the vagal supply to the guinea pig stomach. J. Physiol. (Land.) 185: 600–612, 1966.Google Scholar
  35. 29.
    deCarle, D. J. and M. Pye. Is vasoactive intestinal polypeptide an inhibitory neurotransmitter in the human stomach? In Motility of the Digestive Tract. M. Wienbeck, ed. Raven Press, New York, pp 67–72, 1982.Google Scholar
  36. 30.
    Chayvialle, J-A., M. Miyata, P. L. Rayford, and J. C. Thompson. Effects of test meal, intragastric nutrients and intraduodenal bile in plasma concentrations of immunoreactive somatostatin and vasoactive intestinal peptide in dogs. Gastroenterology 79: 844–852, 1980.PubMedGoogle Scholar
  37. 31.
    Cheung, D. W. and E. E. Daniel. Comparative study of the smooth muscle layers of the rabbit duodenum. J. Physiol. (Land.) 309: 13–27, 1980.Google Scholar
  38. 32.
    Coburn, R. F. and T. Tomita. Evidence for non-adrenergic inhibitory nerves in the guinea pig trachealis muscle. Am. J. Physiol. 1072–1080, 1973.Google Scholar
  39. 33.
    Cocks, J. and G. Burnstock. Effects of neuronal polypeptides on intestinal smooth muscle: a comparison with non-adrenergic, noncholinergic nerve stimulation and ATP. Eur. J. Pharmacol. 54: 251–259, 1979.PubMedGoogle Scholar
  40. 34.
    Cohen, M. L. and A. S. Landry. Vasoactive intestinal peptide: increased tone, enhancement of acetylcholine release and stimulation of adenylate cyclase in intestinal smooth muscle. Life Sciences 26: 811–822, 1980.PubMedGoogle Scholar
  41. 35.
    Coleman, R. A. Effects of some purine derivatives on the guinea pig trachea and their interaction with drugs that block adenosine uptake. Br. J. Pharmacol. 57: 51–59, 1976.PubMedGoogle Scholar
  42. 36.
    Coleman, R. A. and G. P. Levy. A non—adrenergic inhibitory nervous pathway in guinea pig trachea. Br. J. Pharmacol. 52: 167–174, 1974.PubMedGoogle Scholar
  43. 36a.
    Costa, M. and J. B. Furness. The innervation of the internal anal sphincter of the guinea-pig. In Proceedings of the 4th International Symposium of Gastrointestinal Motility. (E. Daniel, ed.) Mitchell Press, Vancouver, pp 681–689, 1974.Google Scholar
  44. 37.
    Costa, M. and J. B. Furness. The origins, pathways and terminations of neurones with VIP-like immunoreactivity in the guinea pig small intestines. Neuroscience 8: 665–676, 1983.PubMedGoogle Scholar
  45. 38.
    Costa, M. and J. B. Furness. Nervous control of intestinal motility. In Mediators and Drugs in Gastrointestinal Motility I. Morphological and Neurophysiological Control. G. Bertaccini, ed. Springer Verlag, Berlin, pp 279–382, 1982a.Google Scholar
  46. 39.
    Costa, M. and J. B. Furness. Neuronal peptides in the intestine. Br. Med. Bull. 38: 247–252, 1982b.Google Scholar
  47. 40.
    Costa, M., J. B. Furness, R. Buffa, and S. J. Said. Distribution of enteric neurons showing immunoreactivity for vasoactive intestinal polypeptide (VIP) in the guinea pig intestine. Neuroscience 5: 587–596, 1980.PubMedGoogle Scholar
  48. 41.
    Creed, K. C. and J. C. Gillespie. Some electrical properties of the rabbit anococcygeus muscle and a comparison of the effects of inhibitory nerve stimulation in the rat and rabbit. J. Physiol. (Lond.) 273: 137–153, 1977.Google Scholar
  49. 42.
    Creed, K. C., J. C. Gillespie, and H. McCoffery. The rabbit anococcygeus muscle and its response to field stimulation and to some drugs. J. Physiol. (Lond.) 273: 121–135, 1977.Google Scholar
  50. 43.
    Crema, A., L. D’Angelo, G. M. Frigo, S. Lechini, L. Onori, and M. Tonini. Effects of desensitization to adenosine 5′-triphosphate and adenosine on non-adrenergic inhibitory responses in the circular muscle of rabbit colon. Br. J. Pharmacol. 75: 311–318, 1982.PubMedGoogle Scholar
  51. 44.
    Daniel, E. E., T. Gonda, T. Domoto, M. Oki, and N. Yanaihara. The effects of substance P and mets-enkephalin in dog ileum. Can. J. Physiol. Pharmacol. 60: 830–840, 1982.PubMedGoogle Scholar
  52. 45.
    Daniel, E. E. and G. S. Taylor. Junction potentials and control of motility of the small intestine. In Proc. Vth Int. Symp. GI Motility. G. Vantrappen, ed. Typoff Press, Leuven, Belgium, pp 142–151, 1975.Google Scholar
  53. 46.
    Daniel, E. E., G. S. Taylor, V. P. Daniel, and M. E. Holman. Can non-adrenergic inhibitory varicosities be identified structurally? Can. J. Physiol. Pharmacol. 55: 243–250, 1977.PubMedGoogle Scholar
  54. 47.
    Daniel, E. E., J. Crankshaw and S. Sarna. Prostaglandins and tetrodotoxin-insensitive relaxation of opossum lower esophageal sphincter. Am. J. Physiol. 236: E153 — E172, 1979.PubMedGoogle Scholar
  55. 48.
    Daniel, E. E., C. Davis, T. R. Jones, and M. S. Kannan. Control of airway smooth muscle. In Airway Reactivity. F. Hargreave, ed. Astra Pharmaceutical, pp 80–107, 1980.Google Scholar
  56. 49.
    Daniel, E. E., A. Helmy-Elkholy, L. P. Jager, and M. S. Kannan. Neither a purine nor VIP is the mediator of inhibitory nerves of opossum esophageal smooth muscle. J. Physiol. (Lond.) 336: 243–260, 1983.Google Scholar
  57. 50.
    Daniel, E. E., M. S., Kannan, C. Davis, and V. Posey-Daniel. Comparative ultra-structural studies in the neuromuscular control of human tracheal and bronchial smooth muscle. Can. J. Physiol. Pharmacol. (submitted).Google Scholar
  58. 51.
    Daniel, E. E. and V. Posey-Daniel. The structural comparison of esophageal lower sphincter (LES) and body circular muscle (BCM) from opossum. Role of interstitial cells of Cajal. Amer. J. Physiol. 246: 305–315, 1984Google Scholar
  59. 52.
    Daniel, E. E. and V. Posey-Daniel. Effects of scorpion venom on structure and function of esophageal lower sphincter (LES) and body circular muscle (BCM) from opossum. Can. J. Physiol. Pharmacol. 62: 360–373, 1984.PubMedGoogle Scholar
  60. 53.
    Davis, C., T. R. Jones and E. E. Daniel. Studies of the mechanism of passive anaphylaxis in human airway smooth muscle. Can. J. Physiol. Pharmacol. Accepted.Google Scholar
  61. 54.
    Den Hertog, G. A. and L. P. Jager. Influxes during the inhibitory junction potentials in the guinea pig taenia coli. J. Physiol. (Lond.) 250: 681–691, 1975.Google Scholar
  62. 55.
    Diamond, L., J. L. Szaren, and M. N. Gillespie. Substance P fails to mimic vagally mediated non-adrenergic bronchodilatation. Peptides 3: 21–29, 1982.Google Scholar
  63. 56.
    Diamond, L. and M. O’Donnell. A non-adrenergic vagal inhibitory pathway to feline airways. Science 208: 185–188, 1980.PubMedGoogle Scholar
  64. 57.
    Dimaline, R. and G. J. Dockray. Molecular variants of vasoactive intestinal polypeptide on the feline lower esophageal sphincter mechanisms of action. Gastroenterology 77: 1001–1007, 1979.Google Scholar
  65. 58.
    Dimaline, R., C. Vaillant and G. J. Dockray. The use of region specific antibodies in the characterization and localization of vasoactive intestinal polypeptide-like substances in the rat gastrointestinal tract. Regulatory Peptides 1: 1–16, 1980.Google Scholar
  66. 59.
    Doidge, J. M. and D. G. Satchell. Adrenergic and non-adrenergic inhibitory nerves in mammalian airways. J. Auton. Nerv. Syst. 5: 83–99, 1982.PubMedGoogle Scholar
  67. 59a.
    Domoto, T., E. E. Daniel, M. Oki, J.E.T. Fox, and N. Yanaihara. Peptidergic nerves (substance P and VIP) in lower esophagus of opossum. Gastroenterology 82 (52): 1044; 1982.Google Scholar
  68. 60.
    Douglas, W. W. Stimulus-secretion coupling: the concept and clues from chromaffin and other cells. Br. J. Pharmacol. 34: 451–474, 1968.PubMedGoogle Scholar
  69. 60a.
    Drury, A. N. and A. Szent-Györgyi. The physiological activity of adenine compounds with especial reference to their action upon the mammalian heart. J. Physiol. (Lond) 68: 213–237, 1929.Google Scholar
  70. 61.
    Edin, R., H. Ahlman, and J. Keventer. The vagal control of the feline pyloric sphincter. Acta Physiol. Scand. 107: 169–174, 1979.PubMedGoogle Scholar
  71. 62.
    Edvinsson, C. and R. Uddman. Immunohistochemical localization and dilatory effect of substance P on human cerebral vessels. Brain Res. 232: 446–471, 1982.Google Scholar
  72. 63.
    Edvinsson, L., J. Fahrenkrug, J. Hanko, C. Owman, F. Sundler, and R.L Uddman. VIP (vasoactive intestinal polypeptide) containing nerves of intra-cranal arteries in mammals. Cell Tissue Res. 208: 135–142, 1980.PubMedGoogle Scholar
  73. 64.
    Eklund, S., J. Fahrenkrug, M. Jodal, O. Lundgren, O. B. Schaffaletzky De Muckadell, and A. Stoqvist. Vasoactive intestinal polypeptide, 5-hydroxytryptamine and reflex hyperaemia in the small intestine of the cat. J. Physiol. (Lond.) 302: 549–557, 1980.Google Scholar
  74. 65.
    Fahrenkrug, J. Vasoactive intestinal polypeptide measurement, distribution and putative neruotransmitter function. Digestion 19: 149–169, 1979.PubMedGoogle Scholar
  75. 66.
    Fahrenkrug, J., H. Galbo, J. J. Holst, and O. B. Schaffaletzky De Muckadell. Influence of the autonomic nervous system on the release of vasoactive intestinal polypeptide from the porcine gastrointestinal tract. J. Physiol. (Lond.) 280: 405–422, 1978b.Google Scholar
  76. 67.
    Fahrenkrug, J., U. Haglund, M. Jodal, O. Lundgren, L. Olbe, and O. B. Schaffaletzky De Muckadell. Nervous release of vasoactive intestinal polypeptide in the gastro-intestinal tract of cats: possible physiological implications. J. Physiol. (Lond.) 284: 291–305, 1978a.Google Scholar
  77. 68.
    Fox, J. E. T., S. J. Said, and E. E. Daniel. Is vasoactive intestinal polypeptide (VIP) an inhibitory neurotransmitter in the lower esophageal sphincter (LES) in the North American opossum? Gastroenterology 76: 11–34, 1979.Google Scholar
  78. 69.
    Fujiwara, M., S. C. Hong, and J. Muramatsu. Effects of Goniopora toxin on non-adrenergic, non-cholinergic response and purine nucleotide release in guinea pig taenia coli. J. Physiol. (Lond.) 326: 515–526, 1982.Google Scholar
  79. 70.
    Franco, R., M. Costa, and J. B. Furness. Evidence that axons containing substance P are of intrinsic origin. Naunyn-Schmiedeberg’s Arch. Pharmacol. 307: 57–63, 1979b.Google Scholar
  80. 71.
    Franco, R., M. Costa and J. B. Furness. Evidence for the release of endogenous substance P from intestinal nerves. Naunyn Schmiedeberg’s Arch. Pharmacol. 306: 185–201, 1979a.Google Scholar
  81. 72.
    Frew, R. and P. M. Landry. Effect of arylazidoaminopropionyl ATP (ANAPP3), a putative ATP antogonist, on ATP responses of isolated guinea pig smooth muscle. Life Sciences 30: 259–267, 1980.Google Scholar
  82. 73.
    Furness, J. B., R. E. Papka, N. G. Della, M. Costa, and R. L. Eskay. Substance P-like immunoreactivity in nerves associated with the vascular system of guinea pigs. Neuroscience 7: 447–459, 1982.PubMedGoogle Scholar
  83. 74.
    Furness, J. B. An electrophysiological study of the smooth muscle of the colon. J. Physiol. (Lond.) 205: 549–562, 1969.Google Scholar
  84. 75.
    Furness, J. B. and M. Costa. Identification of gastrointestinal neurotransmitters. In Handbook of Experimental Pharmacology. Bertaccini, ed. Springer Verlag, Berlin, pp 383–460, 1982.Google Scholar
  85. 76.
    Furness, J. B. and M. Costa. Projections of intestinal neurones showing immunoreactivity for vasoactive intestinal polypeptide are consistent with these neurones being the enteric inhibitory neurones. Neuroscience Letters 15: 199–204, 1979.PubMedGoogle Scholar
  86. 77.
    Furness, J. B., M. Costa, and J. H. Walsh. Evidence for and significance of the projection of VIP neurons from the myenteric plexus to the taenia colin in the guinea pig. Gastroenterology 80: 1557–1561, 1981.PubMedGoogle Scholar
  87. 78.
    Gaginella, T. S., H. S. Mekhjian, and T. M. O’Dorisio. Vasoactive intestinal peptide: quantification by radioimmunoassay in isolated cells, mucosa and muscle of the hamster intestine. Gastroenterolgy 74: 718–721, 1978.Google Scholar
  88. 79.
    Gaginella, T. S., T. M. O’Dorisio, and K. A. Hubel. Release of vasoactive intestinal polypeptide by electrical field stimulation of rabbit ileum. Regulatory Peptides 2: 165–174, 1981.PubMedGoogle Scholar
  89. 80.
    Gershon, M. D. The enteric nervous sytems. Am. Rev. Neurosc. 4: 227–272, 1981.Google Scholar
  90. 81.
    Ghater, M. G., M. N. Sheppard, D. J. O’Shaughnessy, T. E. Adriaan, G. P. McGregor, J. M. Polak and S. R. Bloom. Regulatory peptides in the mammalian respiratory tract. Endocrinology 111: 1248–1254, 1982.Google Scholar
  91. 82.
    Gibbins, I. L. Lack of correlation between ultrastructural and pharmacological types of non-adrenergic autonomic nerves. Cell Tissue Res. 221: 551–581, 1982.PubMedGoogle Scholar
  92. 83.
    Gibson, A. and J. F. Tucker. The effects of vasoactive intestinal polypeptide and of adenosine-5’-triphosphate on the isolated anococcygeus muscle of the mouse. Br. J. Pharmacol. 77: 97–104, 1982.PubMedGoogle Scholar
  93. 83a.
    Gillespie, J. H. The biological significance of the linkages in adenosine triphosphoric acid. J. Physiol. (Lond.) 80: 345–359, 1934.Google Scholar
  94. 84.
    Gillespie, J. S. Non-adrenergic, non-cholinergic inhibitory control of gastrointestinal motility. In Motility of the Digestive Tract. M. Wienbeck, ed. Raven Press, New York, pp 51–66, 1982.Google Scholar
  95. 85.
    Gillespie, J. S. The rat anococcygeus muscle and its response to nerve stimulation and to some drugs. Br. J. Pharmacol. 45: 404–416, 1972.PubMedGoogle Scholar
  96. 86.
    Gillespie, J. S. and J. C. McGrath. The response of the cat anococcygeus muscle to nerve or drug stimulation and a comparison with the rat anococcygeus. Br. J. Pharmacol. 50: 109–118, 1974.PubMedGoogle Scholar
  97. 87.
    Goyal, R. K. and S. Rattan. VIP as a possible neurotransmitter of non-cholinergic, non-adrenergic inhibitory neurons. Nature 288: 378–380, 1980.PubMedGoogle Scholar
  98. 88.
    Goyal, R. K. and S. Rattan. Neurohumoral and drug receptors for the lower esophageal sphincter. Gastroenterology 74: 598–619, 1978.PubMedGoogle Scholar
  99. 89.
    Hirst, G. D. S., M. E. Holman and H. C. McKirdy. Two descending nerve pathways activated by distention of guinea pig small intestine. J. Physiol. (Lond.) 244: 113–127, 1975.Google Scholar
  100. 90.
    Holman, M. E. and J. Hughes. Inhibition of intestinal smooth muscle. Aust. J. Exp. Biol. Med. Sci. 43: 277–290, 1965.PubMedGoogle Scholar
  101. 91.
    Holman, M. E. and J. P. Weinreich. The effects of calcium and magnesium on inhibitory junctional transmission in smooth muscle of guinea pig small intestine. Pflueger’s Arch. 360: 109–119, 1975.Google Scholar
  102. 92.
    Huizinga, J. D. and A. Den Hertog. Inhibition of fundic strips from guinea pig stomach: the effect of theophylline on responses to adenosine, ATP and intramural nerve stimulation. Eur. J. Pharmacol. 63: 259–265, 1980.PubMedGoogle Scholar
  103. 93.
    Hulme, M. E. and Weston, A. H. Some effects of dipyridamole, hexobendine and lidoflazine on inhibitory processes in rabbit duodenum. Br. J. Pharmacol. 50: 609–611, 1974.PubMedGoogle Scholar
  104. 94.
    Hunt, W. B., D. G. Parsons, A. Wahid and J. Wilkinson. Influence of 2–2’-pyridylisatogen to sylate on responses by ATP and by neural stimulation on the rat gastric corpus. Br. J. Pharmacol. 63: 378–379p, 1978.Google Scholar
  105. 95.
    Imaizumi, M. and K. Hama. An electron miscropic study on the interstitial cells of the gizzard of the Love Bird (Uronloncha domestica). Z. Zellforsch. Mikrosk. Anat. 97: 351–357, 1969.Google Scholar
  106. 96.
    Irvin, C. G. R., R. Boileau, J. Tremblay, R. Martin, and P. T. Macklem. Bronchodilation: non-cholinergic, non-adrenergic mediation demonstrated in vivo in the cat. Science 207: 791–792, 1979.Google Scholar
  107. 97.
    Israel, M. and F. M. Meunier. The release of ATP triggered by transmitter action and its possible physiological significance retrograde transmission. J. Physiol. (Paris) 74: 485–490, 1978.Google Scholar
  108. 98.
    Ito, Y. and K. Takeda. Non-adrenergic inhibitory nerves and putative transmitters in the smooth muscle of cat trachea. J. Physiol. (Lond.) 330: 497–511, 1982.Google Scholar
  109. 99.
    Jaffer, S. S., J. T. Farrar, W. M. You, and G. M. Makhlouf. Mode of action and interplay of vasoactive intestinal peptide (VIP), secretin and octapeptide of cholecystokinin (Octa- CCK) on duodenal and ileal muscle in vitro. Gastroenterology, 66 (4): 716, 1974.Google Scholar
  110. 100.
    Jager, L. P. Effects of purinergic compounds on excitable membranes. In Physiological and Regulatory Functions of Adenosine and Adenosine Nucleotides. H. P. Baer and G. I. Drummond, eds. Raven Press, New York, pp 369–376, 1979.Google Scholar
  111. 101.
    Jager, L. P. and J. A. M. Shevers. A comparison of effects evoked in guinea pig taenia coli by purine nucleotides and by purinergic nerve stimulation. J. Physiol. (Lond.) 299: 75–83, 1980.Google Scholar
  112. 102.
    Johns, A. The effect of indomethacin and substance P on the guinea pig urinary bladder. Life Sci. 29: 1803–1809, 1981.PubMedGoogle Scholar
  113. 103.
    Johns, A. The effect of magnesium-free solutions on the responses of the guinea pig urinary bladder to adenosine 5’-triphosphate and nerve stimulation. Can. J. Physiol. Pharmacol. 57: 1320–1323, 1979.PubMedGoogle Scholar
  114. 104.
    Jones, T. R., M. S. Kannan, and E. E. Daniel. Ultrastructural study of guinea pig tracheal smooth muscle and its innervation. Can. J. Physiol. Pharmacol. 581 (8): 974–983, 1982.Google Scholar
  115. 105.
    Kachelhoffer, J., C. Mendel, J. Dachel, D. Hohmatter, and J. F. Grenier. The effect of VIP on intestinal motility. Study on ex vivo perfused isolated canine jejund loops. Am. J. Digest. Dis. 21: 957–962, 1976.PubMedGoogle Scholar
  116. 106.
    Kuchii, M. J. T. Miyahara, and S. Shibata. [3H]-adenine nucleotide and [3H]-noradrenaline release evoked by electrical field stimulation, perivascular nerve stimulation and nicotine from the taenia of the guinea pig caecum. Br. J. Pharmacol. 49: 258–267, 1973a.PubMedGoogle Scholar
  117. 107a.
    Kuchii, M., J. T. Miyahara and S. Shibata. [3H]-adenosine nucleotide and [3H]-nonadrenaline uptake by cold stored guinea pig taenia caecum; mechanical effects and release of [3H]-adenosine nucleotide by noradrenaline, papaverine and nitroglycerine. Br. J. Pharmacol. 49: 642–650, 1973b.PubMedGoogle Scholar
  118. 107.
    Kuriyama, H., T., Osa and N. Toida. Nervous factors influencing the membrane activity of intestinal smooth muscle. J. Physiol. (Lond) 191: 257–270, 1967.Google Scholar
  119. 108.
    Kuroda, Y. and H. Mcilwain. Uptake and release of [14C]- adenine derivative at beds of mammalian cortical synaplosomes in a superfusion system. J. Neurochem. 22: 691–699, 1974.PubMedGoogle Scholar
  120. 109.
    Langley, J. N. and R. Magnus. Some observations of the movements of the intestine before and after degenerative section of the mesenteric nerves. J. Physiol. (Lond.) 33: 34–51, 1905.Google Scholar
  121. 110.
    Larsson, L. J. Ultrastructural localization of a new neuronal peptide (VIP). Histochemistry 54: 173–176, 1977.PubMedGoogle Scholar
  122. 111.
    Larsson, L. J., L. Edvinsson, J. Fahrenkrug, R. Hakanson, C. Owman, O. Shaffaletzky De Muckadell, and F. Sundler. Immunohistochemical localization of a vasodilatory polypeptide (VIP) in cerebrovascular nerves. Brain Res. 113: 440–404, 1976a.Google Scholar
  123. 112.
    Lee, T. J. F., W. R. Hume, C. Su, and J. A. Bevan. Neurogenic vasodilation of cat cerebral arteries. Circ. Res. 42: 535–542, 1978.PubMedGoogle Scholar
  124. 113.
    Lee, T. J. F. Cholinergic mechanism in the large cat cerebral artery. Circ. Res. 50: 870–879, 1982.PubMedGoogle Scholar
  125. 114.
    Luchelli-Fortis, M. A., B. B. Fredholm, and S. Z. Langer. Release of radioactive purines from cat nictitating membrane labelled with 3H-adenine. Eur. J. Pharmacol. 58: 389–392, 1979.PubMedGoogle Scholar
  126. 115.
    Lundberg, J. M. Evidence for occurrence of vasoactive intestinal polypeptide (VIP) in neurons of cat exocrine glands. Morphological, biochemical and functional studies. Acta Physiol. Scand. Suppl. 496: 1–57, 1981a.PubMedGoogle Scholar
  127. 116.
    Lundberg, J. M. Evidence for coexistence of vasoactive intestinal polypeptide (VIP) and acetylcholine in neurons of cat exocrine glands; morphological, biochemical and functional studies. Acta Physiol. Scand. Suppl. 496: 81–101, 1981b.Google Scholar
  128. 117.
    Lundberg, J. M., A. Anggard, P. Emson, J. Fahrenkrug, and J. Hokfelt. Vasoactive intestinal polypeptide and cholinergic mechanism in cat nasal mucosa: studies on choline acetyltransferase and release of vasoactive intestinal polypeptide. Proc. Natl. Acad. Sci. USA 78: 5255–5259, 1981a.PubMedGoogle Scholar
  129. 118.
    Lundberg, J. M., A. Anggard, and J. Fahrenkrug. Complementary role of vasoactive intestinal polypeptide (VIP) and acetylcholine for cat submandibular gland blood flow ana secretion. I. VIP release. Acta Physiol. Scand. 113: 317–327, 1981b.PubMedGoogle Scholar
  130. 119.
    Maas, A. J. J. The effect of apamin on responses evoked by field stimulation in guinea pig taenia coli. Eur. J. Pharmacol. 73: 1–9, 1981.PubMedGoogle Scholar
  131. 120.
    Maas, A. J. J. and A. Den Hertog. The effect of apamin on the smooth muscle cells of the guinea pig taenia coli. Eur. J. Pharmacol. 58: 151–156, 1979.PubMedGoogle Scholar
  132. 121.
    Mackenzie, J. and G. Burnstock. Evidence against vasoactive intestinal polypeptide being the non-adrenergic, non-cholinergic inhibitory transmitter released from nerves supplying the smooth muscle of the guinea pig taenia coli. Eur. J. Pharmacol. 67: 255–267, 1980.PubMedGoogle Scholar
  133. 122.
    Martinson, J. Studies on the efferent vagal control of the stomach. Acta Physiol. Scand. (Suppl. 255 ): 1–65, 1965.Google Scholar
  134. 123.
    Martinson, J. Nervous control of gastroduodenal motility and emptying. Scand. J. Gastroenterology (Suppl. 10 ): 31–44, 1975.Google Scholar
  135. 123a.
    Matsuzaki, Y., Y. Hamasaki, and S. I. Said. Vasoactive intestinal peptide: a possible transmitter of non-adrenergic relaxation of guinea pig airways. Science 210: 1252–1253, 1980.PubMedGoogle Scholar
  136. 124.
    McCullock, J. T. and L. Edvinsson. The effects of vasoactive intestinal polypeptide in trial arteriolar calibre, cerebral blood flow, cerebral oxygen consumption and the electroencephalogram. Am. J. Physiol. 238: 449–456, 1980.Google Scholar
  137. 125.
    McKay, D. and H. C. McKirdy. Effect of vasopressin and of adenosine triphosphate in the fleet preparation of rabbit rectum. Br. J. Pharmacol. 44: 366–367P, 1972.Google Scholar
  138. 126.
    McKirdy, H. C. Functional relationship of longitudinal and circular layers of the muscularis externa of the rabbit large intestine. J. Physiol. (Lond.) 227: 839–853, 1972.Google Scholar
  139. 126a.
    Morgan, K. G., P. F. Schmalz, J. H. Szursweski. The inhibitory effects of vasoactive intestinal polypeptide on the mechanical and electrical activity of canine antral smooth muscle. J. Physiol. (Lond.)282:437–450, 1978.Google Scholar
  140. 127.
    Muller, M. J. and H. P. Baer. Apamin, a non-specific antagonist of smooth muscle relaxants. Naunyn-Schmiedeberg’s Arch. Pharmacol. 311: 105–107, 1980.Google Scholar
  141. 128.
    Mutt, V. and S. J. Said. Structure of the porcine vasoactive intestinal octocosapeptide. Eur. J. Biochem. 42: 581–589, 1974.PubMedGoogle Scholar
  142. 129.
    Neya, T., T. Yamasato, M. Tokaki, M. Mizutami and S. Nakayama. Excitatory and inhibitory effects of vasoactive intestinal polypeptide (VIP) on the isolated jejunum and internal anal sphincter in the guinea pig. Biomed. Res. 2: 398–403, 1981.Google Scholar
  143. 130.
    Nilsson, G., K. Dahlberg, E. Brodir, F. Sundler, and K. Strandberg. Distribution and constrictor effect of substance P in guinea pig tracheo-bronchial tissue. In Substance P. U. S. Von Euler and B. Pernow, eds. Raven Press, New York, pp 75–81, 1977.Google Scholar
  144. 131.
    Northway, M. N. and T. F. Burks. Stimulation of cholinergic nerves in dog intestine by adenine nucleotides. Eur. J Pharmacol. 65: 11–19, 1980.PubMedGoogle Scholar
  145. 132.
    Ohga, A. and T. Taneike. Dissimilarity between the responses to adenosine triphosphate or its related compounds and nonadrenergic inhibitory nerve stimulation in the longitudinal smooth muscle of pig stomach. Br. J. Pharmacol. 60: 221–231, 1977.PubMedGoogle Scholar
  146. 133.
    Okwuasaba, F. K., J. T. Hamilton, and M. A. Cook. Relaxations of guinea pig fundic strip by adenosine, adenine nucleotides and electrical stimulation; antagonism by theophylline and desensitization to adenosine and its derivatives. Eur. J. Pharmacol. 46: 181–198, 1977.PubMedGoogle Scholar
  147. 134.
    Paton, W. D. M. and M. A. Zar. Mechanism of acetylcholine release from parasympathetic nerves. J. Physiol. (Lond.) 194: 13–33, 1968.Google Scholar
  148. 135.
    Rattan, S. and R. K. Goyal. Neural control of the lower esophageal sphincter. Influence of the vagus nerves. J. Clin. Invest. 54: 899–906, 1974.PubMedGoogle Scholar
  149. 136.
    Rattan, S. and R. K. Goyal. Evidence against purinergic inhibitory nerves in the vagal pathway to the opossum lower esophageal sphincter. Gastroenterology 78: 898–904, 1980.PubMedGoogle Scholar
  150. 137.
    Rattan, S., M. Grey, and R. K. Goyal. Vasoactive intestinal peptide causes peristaltic contractions in the esophageal body. Life Sciences 30: 1557–1563, 1982.PubMedGoogle Scholar
  151. 138.
    Richardson, J. B. Nerve supply to the lungs. Am. Rev. Resp. Dis. 119: 785–809, 1979.PubMedGoogle Scholar
  152. 139.
    Richardson, J. and J. Beland. Non-adrenergic inhibitory nervous system in human airways. J. Appl. Physiol. 4: 764–771, 1976.Google Scholar
  153. 140.
    Rikimaru, A., Y. Fukushi and T. Suzuki. Effects of imidazole and phentolamine on the relaxant responses of guinea pig taenia coli to transmural stimulation and to adenosine triphosphate. Tokoku Med. J. 105: 199–200, 1971.Google Scholar
  154. 141.
    Roman, C. Nervous control of esophageal and gastric motility. In Mediators and Drugs in Gastrointestinal Motility. I. Handbook of Experimental Pharmacology. Vol. 59/I. G. C. Bertaccini, ed. Springer Verlag, Berlin, pp 223–228, 1982.Google Scholar
  155. 142.
    Rosell, S., L. Olgart, B. Gazelius, P. Panopoulos, K. Folkers, and J. Honig. Inhibition of antidromic and substance P-induced vasodilation by a substance P antagonist. Acta Physiol. Scand. 111: 381–382, 1981.PubMedGoogle Scholar
  156. 143.
    Roth, J., M. Bendayan, and L. Orci. Utrastructural localization of intracellular antigens by use of protein A gold complex. J. Histochem. Cytochem. 26: 1074–1081, 1978.Google Scholar
  157. 144.
    Rumesson, J. J. and L. Thuneberg. Plexus muscularis profondus and associated interstitial cells. I. Light microscopical studies of mouse small intestine. The Anat. Res. 203: 115–129, 1982a.Google Scholar
  158. 145.
    Rumesson, J. J., L. Thuneberg and H. B. Mikkelsen. Plexus muscularis profundus and associated interstitial cells. II. Ultrastructural studies of mouse small intestine. The Anat. Res. 203: 125–146, 1982b.Google Scholar
  159. 146.
    Rutherfold, A. and G. Burnstock. Neuronal and non-neuronal components in the overflow of labelled adenyl compounds from guinea pig taenia coli. Eur. J. Pharmacol. 48: 195–202, 1978.Google Scholar
  160. 146a.
    Ryan, J. P. and S. Ryave. Effect of vasoactive intestinal polypeptide on gall bladder smooth muscle in vitro. Am. J. Physiol. 234: E44–46, 1978.PubMedGoogle Scholar
  161. 147.
    Saito, K. Effects of extracellularly applied ATP and its related nucleotides on the membrane potential of the guinea pig taenia coli. Jap. J. Smooth Muscle Res. 8: 32–39, 1972.Google Scholar
  162. 149.
    Satchell, D. G. and G. Burnstock. Comparison of the inhibitory effects of the guinea pig taenia coli of adenine nucleotides and adenosine in the presence and absence of dipyridamole. Eur. J. Pharmacol. 32: 324–328, 1975.PubMedGoogle Scholar
  163. 150.
    Satchell, D. G., A. Lunch, P. M. Bourke, and G. Burnstock. Potentiation of the effects of exogenously applied ATP and purinergic nerve stimulation on the guinea pig taenia coli by dipyridamole and hexobendine. Eur. J. Pharmacol. 19: 343–350, 1972.PubMedGoogle Scholar
  164. 151.
    Schaffaletzky De Muckadell, O. B., J. Fahrenkrug, J. Holst and K. B. Lauritsen. Release of vasoactive intestinal polypeptide (VIP) by intraduodenal stimuli. Scand. J. Gastroent. 12: 793–799, 1977.Google Scholar
  165. 152.
    Schultzberg, M., T. Hokfelt, G. Nilsson, L. Terenius, J. F. Rehfeld, M. Brown, R. Elder, M. Goldstein, and S. Said. Distribution of peptide and catecholamine neurons in the gastrointestinal tract of rat and guinea pig: immunohistochemical studies with antisera to substance P, VIP, enkephalins, somatostatin, gastrin, neurotensin and dopamine beta-hyroxylase. Neuroscience 5: 689–744, 1980.PubMedGoogle Scholar
  166. 153.
    Shuba, M. F. and I. A. Vladimirova. Effect of apamin on the electrical responses of smooth muscle to adenosine 5’-triphosphate and to non-adrenergic, non-cholinergic nerve stimulation. Neuroscience 5: 853–859, 1980.PubMedGoogle Scholar
  167. 154.
    Silinsky, E. M. On the association between transmitter secretion and the release of adenine nucleotides from mammalian motor nerve terminals. J. Physiol. (Lond.) 247: 145–162, 1975.Google Scholar
  168. 155.
    Small, R. C. Electrical slow waves and tone of guinea pig isolated trachealis muscle. Effects of drugs and temperature changes. Br. J. Pharmacol. 77: 45–54, 1982.PubMedGoogle Scholar
  169. 156.
    Small, R. C. and A. H. Weston. Intramural inhibition in rabbit and guinea pig intestine. In Physiological and Regulatory Functions of Adenosine and Adenine Nucleotides. H. P. Baer and G. J. Drummond, eds. Raven Press, New York, pp 45–61, 1979.Google Scholar
  170. 157.
    Spedding, M. and D. F. Weetman. Identification of separate receptors for adenosine and adenosine-5’-triphosphate in causing relaxations of the isolated taenia of the guinea pig ceacum. Br. J. Pharmacol. 57: 305–310, 1976.PubMedGoogle Scholar
  171. 158.
    Spedding, M., A. Sweetman and D. F. Weetman. Antagonism of adenosine-5’-triphosphate-induced relaxation by 2–2’-pyridylisatogen in the taenia of guinea pig ceacum. Br. J. Pharmacol. 53: 575–583, 1975.PubMedGoogle Scholar
  172. 159.
    Stockley, H. C. 2–2’-pyridylisatogen antagonizes adenosine 5’-triphosphate but not nerve-mediated relaxations in human isolated taenia coli. In Gastrointestinal Motility in Health and Disease (H. L. Duthie, ed.) University Park Press, Baltimore, pp 145–150, 1978.Google Scholar
  173. 160.
    Su, C., J. Bevan and G. Burnstock. [3H]-adenosine triphosphate: release during stimulation of enteric nerves. Science 173: 336–338, 1971.PubMedGoogle Scholar
  174. 161.
    Sundler, F., R. Hakanson, L. D. Larsson, E. Brodin, and G. Nilsson. Substance P in the gut: an immunochemical and immunohistochemical study of its distribution and development. In Substance P. U. S. Von Euler and B. Pernow, eds. Raven Press, New York, pp 59–65, 1977.Google Scholar
  175. 162.
    Suzuki, T., Y. Fukushi, and A. Rikimaru. Relaxant effect of adenosine triphosphate and its related nucleotides on the guinea pig taenia coli. Jap. J. Smooth Muscle Res. 7: 207–212, 1971.Google Scholar
  176. 163.
    Thuneberg, L. The interstitial cells of Cajal: intestinal pacemaker cells? In Advances in Anatomy, Embryology and Cell Biology. Springer Verlag, Berlin, pp 1–30, 1982.Google Scholar
  177. 164.
    Tomita, J. Conductance change during the inhibitory potential in the guinea pig taenia coli. J. Physiol. (Lond.) 225: 693–703, 1972.Google Scholar
  178. 165.
    Tomita, J. and H. Watanabe. A comparison of the effects of adenosine triphosphate with noradrenaline and with the inhibitory potential of the guinea pig taenia coli. J. Physiol. (Lond.) 231: 167–177, 1973.Google Scholar
  179. 166.
    Tonini, M., L. Onori, G. M. Grigo, S. Lecchini, L. D’Angelo, and A. Crema. Non-adrenergic inhibition of the longitudinal muscle of rabbit distal colon may not be mediated by purinergic nerves. J. Pharin. Pharmacol. 33: 536–537, 1981.Google Scholar
  180. 167.
    Uddman, R., J. Alumets, L. Edvinsson, R. Hakanson, and F. Sundler. Occurrences and distribtuion of VIP nerves in the nasal mucosa and tracheobronchial wall. Acta Otolaryngol. (Stockholm) 86: 443–448, 1978a.Google Scholar
  181. 168.
    Uddman, R., J. Alumets, L. Edvinsson, R. Hakanson and F. Sundler. Peptidergic (VIP) innervation of the esophagus. Gastroenterology 75: 5–8, 1978b.PubMedGoogle Scholar
  182. 169.
    Uddman, R., J. Fahrenkrug, L. Malm, J. Alumets, R. Hakanson, and F. Sundler. Neuronal VIP in salivary glands: distribution and release. Acta Physiol. Scand. 110: 31–38, 1980.PubMedGoogle Scholar
  183. 170.
    Uddman, R., J. Alumets, L. Edvinsson, R. Hakanson and F. Sundler. VIP nerve fibers around peripheral blood vessels. Acta Physiol. Scand. 112: 65–70, 1981.PubMedGoogle Scholar
  184. 171.
    Vladimirova, J. A. and M. F. Shuba. The effect of strychnine, hydras-tin and apamin on synaptic transmission in smooth muscle cells. Neirofiziologiya, Kiev 10: 295–299, 1978.Google Scholar
  185. 172.
    Wei, E. P., H. A. Kontos, and S. I. Said. Mechanism of action of vasoactive intestinal polypeptide on cerebral blood flow. Am. J. Physiol. 239: 765–768, 1980.Google Scholar
  186. 173.
    Weston, A. H. The effect of desensitization to adenosine triphosphate on the peristaltic reflex in guinea pig ileum. Br. J. Pharmacol. 47: 606–608, 1973.PubMedGoogle Scholar
  187. 174.
    White J. D. Direct detection of depolarization induced release of ATP from a synaptosomal preparation. Nature (Lond.) 267: 67–68, 1977.Google Scholar
  188. 175.
    White, T., P. Potter, C. Moody and G. Burnstock. Tetrodotoxin resistant release of ATP from guinea pig taenia coli and vas deferens during electrical field stimulation in the presence of luciferinluciferase. Can. J. Physiol. Pharmacol. 59: 1094–1100, 1981.PubMedGoogle Scholar
  189. 176.
    Yip, P., B. Polembini, and R. F. Coburn. Inhibitory innervation to the guinea pig trachealis muscle. J. Appl. Physiol. 50: 374–382, 1981.PubMedGoogle Scholar
  190. 177.
    Zimmerman, H. and V.P. Whittaker. Effect of electrical stimulation in the yield and composition of synaptic vesicles from the cholinergic synapsis of the electric organ of Torpedo: a combined biochemical, electrophysiological and morphological study. J. Neurochem. 22: 435–450, 1974.Google Scholar
  191. 178.
    Zimmerman, H. and C. R. Denston. Adenosine triphosphate in cholinergic vesicles isolated from the electric organ of Electrophorus electricus. Brain Res. 111: 365–376, 1976.Google Scholar

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