Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Neurotransmitter release in the enteric nervous system

William M. Yau

10.1002/cphy.cp060112

Source: Supplement 16: Handbook of Physiology, The Gastrointestinal System, Motility and Circulation

Originally published: 1989

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Neurotransmitter Versus Neuromodulator
2 Mechanism of Release
2.1 Vesicular Release Mechanism
2.2 Nonvesicular Hypothesis
2.3 Nonsynaptic Transmitter Release
3 Modulation of Transmitter Release
3.1 Presynaptic Modulation
3.2 Activation of Intracellular Control Systems
4 Enteric Cholinergic System
4.1 Factors Regulating Acetylcholine Release
5 Neuro Active Peptides and their Modulation of Acetylcholine Release
5.1 Vasoactive Intestinal Peptide
5.2 Substance P
5.3 Somatostatin
5.4 Cholecystokinin
5.5 Dynorphins and Enkephalins
5.6 Other Neuropeptides
6 General Neuropeptide‐Degrading Enzymes
6.1 Endopeptidase
6.2 Peptidyl Dipeptidase A
6.3 Aminopeptidase
6.4 Dipeptidyl Peptidase IV
6.5 Acetylcholinesterase
7 Adrenergic System
7.1 Factors Regulating Norepinephrine Release
8 Enteric Synaptosomes
8.1 Release of Acetylcholine
8.2 Serotonergic Synaptosomes
8.3 Noradrenergic Synaptosomes
8.4 Release of ATP
8.5 Neuropeptide Synaptic Vesicles
Figure 1. Figure 1.

Presynaptic autoreceptor inhibitory feedback mechanism. Transmitter substance release by presynaptic neuron can depress further transmitter release by interacting with receptor sites at its own axon terminals.
Figure 2. Figure 2.

Presynaptic heteroreceptor inhibitory feedback mechanism. Transmitter substance released from one neuron (A) can depress transmitter release from another neuron (B) by activating receptor sites at terminals of target neuron.
Figure 3. Figure 3.

Transsynaptic modulation of transmitter release. Chemical substance released by innervated tissue may inhibit further release of neurotransmitter from innervating neuron by activating receptors at axon terminals.
Figure 4. Figure 4.

Metabolism of inositol phospholipids and signal transduction. When extracellular signal (A) activates membrane receptor (R), cascade of reactions occurs within plasma membrane, starting from hydrolysis by phospholipase C of phosphatidylinositol (PI) to formation of 1,2‐diacylglycerol (DG), with phosphatidylinositol 4‐monophosphate (PIP) and phosphatidylinositol 4,5‐bisphosphate (PIPP) as intermediates. In each hydrolysis step, ATP is required. In conversion of PIPP to DG, D‐myo‐inositol 1,4,5‐trisphosphate (IPPP) is generated. IPPP triggers mobilization of Ca2+ but is also recycled back to inositol (I) with inositol 1,4‐bisphosphate (IPP) and inositol 1‐phosphate (IP) as intermediates. DG is phosphorylated by diglyceride kinase to phosphatidic acid (PA). PA can form phosphatidyl‐cytidine 5'‐monophosphate (CMP‐PA) in the presence of cytidine 5'‐triphosphate. When CMP‐PA is combined with I, resynthesis of PI occurs. Ca2+ mobilization, which leads to physiological responses, is thought to be enhanced by PA, IPPP, or occupation of R by A. PA is converted to arachidonic acid (AA) by diglyceride lipase. Synthesis of prostaglandins (PG) from AA is catalyzed by cyclooxygenase. Both AA and PG are capable of activating guanylate cyclase, enzyme responsible for formation of cGMP from GTP. DG may also activate Ca2+‐ and phospholipid‐dependent protein kinase, leading to phosphorylation of membrane proteins. Both protein phosphorylation and increase in Ca2+ can elicit cellular responses such as neurotransmitter release 31,107,265.
Figure 5. Figure 5.

Summary of possible interactions between different neurons in myenteric plexus of guinea pig small intestine. Substance P (SP), vasoactive intestinal peptide (VIP), and cholecystokinin‐octapeptide (CCK) are stimulant (+) neuropeptides, whereas somatostatin (SOMA) and opioids (OPI) are depressant (−) neuropeptides on release of acetylcholine (ACh) from cholinergic neurons. Other chemical substances that are capable of enhancing ACh release include bradykinin, histamine, γ‐aminobutyric acid (GABA), gastrin‐releasing peptide (GRP)/bombesin, neurotensin, serotonin (5‐HT), and prostaglandins. Neurotransmitter substances that may inhibit ACh release include norepinephrine (NOR), galanin, neuropeptide Y (NPY), and ATP.


Figure 1.

Presynaptic autoreceptor inhibitory feedback mechanism. Transmitter substance release by presynaptic neuron can depress further transmitter release by interacting with receptor sites at its own axon terminals.



Figure 2.

Presynaptic heteroreceptor inhibitory feedback mechanism. Transmitter substance released from one neuron (A) can depress transmitter release from another neuron (B) by activating receptor sites at terminals of target neuron.



Figure 3.

Transsynaptic modulation of transmitter release. Chemical substance released by innervated tissue may inhibit further release of neurotransmitter from innervating neuron by activating receptors at axon terminals.



Figure 4.

Metabolism of inositol phospholipids and signal transduction. When extracellular signal (A) activates membrane receptor (R), cascade of reactions occurs within plasma membrane, starting from hydrolysis by phospholipase C of phosphatidylinositol (PI) to formation of 1,2‐diacylglycerol (DG), with phosphatidylinositol 4‐monophosphate (PIP) and phosphatidylinositol 4,5‐bisphosphate (PIPP) as intermediates. In each hydrolysis step, ATP is required. In conversion of PIPP to DG, D‐myo‐inositol 1,4,5‐trisphosphate (IPPP) is generated. IPPP triggers mobilization of Ca2+ but is also recycled back to inositol (I) with inositol 1,4‐bisphosphate (IPP) and inositol 1‐phosphate (IP) as intermediates. DG is phosphorylated by diglyceride kinase to phosphatidic acid (PA). PA can form phosphatidyl‐cytidine 5'‐monophosphate (CMP‐PA) in the presence of cytidine 5'‐triphosphate. When CMP‐PA is combined with I, resynthesis of PI occurs. Ca2+ mobilization, which leads to physiological responses, is thought to be enhanced by PA, IPPP, or occupation of R by A. PA is converted to arachidonic acid (AA) by diglyceride lipase. Synthesis of prostaglandins (PG) from AA is catalyzed by cyclooxygenase. Both AA and PG are capable of activating guanylate cyclase, enzyme responsible for formation of cGMP from GTP. DG may also activate Ca2+‐ and phospholipid‐dependent protein kinase, leading to phosphorylation of membrane proteins. Both protein phosphorylation and increase in Ca2+ can elicit cellular responses such as neurotransmitter release 31,107,265.



Figure 5.

Summary of possible interactions between different neurons in myenteric plexus of guinea pig small intestine. Substance P (SP), vasoactive intestinal peptide (VIP), and cholecystokinin‐octapeptide (CCK) are stimulant (+) neuropeptides, whereas somatostatin (SOMA) and opioids (OPI) are depressant (−) neuropeptides on release of acetylcholine (ACh) from cholinergic neurons. Other chemical substances that are capable of enhancing ACh release include bradykinin, histamine, γ‐aminobutyric acid (GABA), gastrin‐releasing peptide (GRP)/bombesin, neurotensin, serotonin (5‐HT), and prostaglandins. Neurotransmitter substances that may inhibit ACh release include norepinephrine (NOR), galanin, neuropeptide Y (NPY), and ATP.

References
 1. Abood, L. G., K. Koketsu, and S. Miyamoto. Outflux of various phosphates during membrane depolarization of excitable tissues. Am. J. Physiol. 202: 469–474, 1962.
 2. Adam‐Vizi, V., and E. S. Vizi. Direct evidence of acetylcholine releasing effect of serotonin in the Auerbach plexus. J. Neural Transm. 42: 127–138, 1978.
 3. Adler‐Graschinsky, E., and S. Z. Langer. Possible role of a β‐adrenoceptor in the regulation of noradrenaline release by nerve stimulation through a positive feedback mechanism. Br. J. Pharmacol. 53: 43–50, 1975.
 4. Ágoston, D. V., M. Ballmann, J. M. Conlon, G. H. C. Dowe, and V. P. Whittaker. Isolation of neuropeptide‐containing vesicles from the guinea pig ileum. J. Neurochem. 45: 398–406, 1985.
 5. D. V. Ágoston,, J. W. Kosh, J. Lisziewicz, and V. P. Whittaker. Separation of recycling and reserve synaptic vesicles from cholinergic nerve terminals of the myenteric plexus of guinea pig ileum. J. Neurochem. 44: 299–305, 1985.
 6. Akubue, P. I. The site of action of drugs on the isolated taenia caeci from the guinea‐pig. Br. J. Pharmacol. 27: 347–365, 1966.
 7. Alberts, P., T. Bartfai, and L. Stjärne. The effects of atropine on [3H]acetylcholine secretion from guinea‐pig myenteric plexus evoked electrically or by high potassium. J. Physiol. Lond. 329: 93–112, 1982.
 8. Alberts, P., V. R. Ogren, and A. I. Sellstrom Role of adenosine 3',5'‐cyclic monophosphate in adrenoceptor‐mediated control of 3H‐noradrenaline secretion in guinea‐pig ileum myenteric nerve terminals. Naunyn‐Schmiedeberg's Arch. Pharmacol. 330: 114–120, 1985.
 9. Alberts, P., and L. Stjärne. Secretion of 3H‐acetylcholine from guinea‐pig ileum myenteric plexus is enhanced by 8‐Br adenosine 3',5'‐cyclic monophosphate but not changed by 8‐Br guanosine 3',5' ‐cyclic monophosphate. Acta Physiol. Scand. 115: 269–272, 1982.
 10. Alberts, P., and L. Stjärne. Role of calcium in muscarinic auto‐inhibition of 3H‐acetylcholine secretion in guinea‐pig ileum myenteric plexus. Acta Physiol. Scand. 115: 487–491, 1982.
 11. Alberts, P., and L. Stjärne. Facilitation, and muscarinic and α‐adrenergic inhibition of the secretion of 3H‐acetylcholine and 3H‐noradrenaline from guinea‐pig ileum myenteric nerve terminals. Acta Physiol. Scand. 116: 83–92, 1982.
 12. Al‐Humayyd, M., and T. D. White. Adrenergic and possible noradrenergic sources of adenosine 5'‐triphosphate release from nerve varicosities isolated from ileal myenteric plexus. J. Pharmacol. Exp. Ther. 233: 796–800, 1985.
 13. Al‐Humayyd, M., and T. D. White. 5‐Hydroxytryptamine releases adenosine 5'‐triphosphate from nerve varicosities isolated from myenteric plexus of guinea‐pig ileum. Br. J. Pharmacol. 84: 27–34, 1985.
 14. Almenoff, J., and M. Orlowski. Biochemical and immunological properties of a membrane‐bound brain metalloen‐dopeptidase: comparison with thermolysin‐like kidney neutral metalloendopeptidase. J. Neurochem. 42: 151–157, 1984.
 15. Ambache, N., and M. A. Freeman. Atropine‐resistant longitudinal muscle spasms due to excitation of non‐cholinergic neurones in Auerbach's plexus. J. Physiol. Lond. 199: 705–727, 1968.
 16. Angel, F., V. L. W. Go, P. F. Schmalz, and J. H. Szurszewski Vasoactive intestinal polypeptide: a putative transmitter in the canine gastric muscularis mucosa. J. Physiol. Lond. 341: 641–654, 1983.
 17. Angel, F., V. L. W. Go, and J. H. Szurszewski. Innervation of the muscularis mucosae of canine proximal colon. J. Physiol. Lond. 357: 93–108, 1984.
 18. Angus, J. A., and P. I. Korner. Evidence against presynaptic α‐adrenoceptor modulation of cardiac sympathetic transmission. Nature Lond. 286: 288–291, 1980.
 19. Anthony, M. Serotonin antagonists. Aust. NZ J. Med. 14: 888–895, 1984.
 20. Arregui, A., P. C. Emson, and E. G. Spokes. Angiotensinconverting enzyme in substantia nigra: reduction of activity in Huntington's disease and after intrastriatal kainic acid in rats. Eur. J. Pharmacol. 52: 121–124, 1978.
 21. Astrom, A. Anti‐sympathetic action of sympathomimetic amines. Acta Physiol. Scand. 18: 295–307, 1949.
 22. Baker, P. F., and M. P. Blaustein. Sodium‐dependent uptake of calcium by crab nerve. Biochim. Biophys. Acta 150: 167–170, 1968.
 23. Baron, S. A., B. M. Jaffe, and A. R. Gintzler. Release of substance P from the enteric nervous system: direct quantitation and characterization. J. Pharmacol. Exp. Ther. 227: 365–368, 1983.
 24. Bartfai, T. Cyclic nucleotides in the central nervous system. Curr. Top. Cell. Regul. 16: 225–269, 1980.
 25. Bartho, L., and P. Holzer. Search for a physiological role of substance P in gastrointestinal motility. Neuroscience 16: 1–32, 1985.
 26. Bartho, L., P. Holzer, and F. Lembeck. Sympathetic control of substance P releasing enteric neurones in the guinea pig ileum. Neurosci. Lett. 38: 291–296, 1983.
 27. Beani, L., C. Bianchi, and A. Crema. The effect of catecholamines and sympathetic stimulation on the release of acetylcholine from the guinea‐pig colon. Br. J. Pharmacol. 36: 1–17, 1969.
 28. Beani, L., C. Bianchi, A. Siniscalchi, L. Sivilotti, S. Tanganelli, and E. Veratti. Different approaches to study acetylcholine release: endogenous ACh versus tritium efflux. Naunyn‐Schmiedeberg's Arch. Pharmacol. 328: 119–126, 1984.
 29. Bennett, A., K. G. Eley, and H. L. Stockley. The effects of prostaglandins on guinea‐pig isolated intestine and their possible contribution to muscle activity and tone. Br. J. Pharmacol. 54: 197–204, 1975.
 30. Benuck, M., and N. Marks. Co‐identity of brain angiotensin converting enzyme with a membrane bound dipeptidyl carboxypeptidase inactivating met‐enkephalin. Biochem. Biophys. Res. Commun. 88: 215–221, 1979.
 31. Berridge, M. J. Electrophysiology of intestinal smooth muscle. In: Chemical Neurotransmission 75 Years, edited by L. Stjärne, P. Hedqvist, H. Lagercrantz, and A. Wennmalm. New York: Academic, 1981, p. 385–397.
 32. Besson, J., W. Rostene, A.‐M. Lhiaubet, B. Poussin, and G. Rosselin. Release of vasoactive intestinal peptide from rat jejunoileum in vitro. Effect of various depolarizing agents. Experientia 39: 732–733, 1983.
 33. Bitar, K. N., and G. M. Makhlouf. Receptors on smooth muscle cells: characterization by contraction and specific antagonists. Am. J. Physiol. 242 (Gastrointest. Liver Physiol. 5): G400–G407, 1982.
 34. Bitar, K. N., and G. M. Makhlouf. Relaxation of isolated gastric smooth muscle cells by vasoactive intestinal peptide. Science Wash. DC 216: 531–533, 1982.
 35. Bitar, K. N., and G. M. Makhlouf. Specific opiate receptors on isolated mammalian gastric muscle cells. Nature Lond. 297: 72–74, 1982.
 36. Bitar, K. N., S. I. Said, G. C. Weir, B. Saffouri, and G. M. Makhlouf. Neural release of vasoactive intestinal peptide from the gut. Gastroenterology 79: 1288–1294, 1980.
 37. Bjorklund, A., and O. Lindvall. Dopamine in dendrites of substantia nigra neurons: suggestions for a role in dendritic terminals. Brain Res. 83: 531–537, 1975.
 38. Bligh, J. The level of free choline in plasma. J. Physiol. Lond. 117: 234–240, 1952.
 39. Botting, J. H., and R. Salzmann. The effect of indomethacin on the release of prostaglandin E2 and acetylcholine from guinea‐pig isolated ileum at rest and during field stimulation. Br. J. Pharmacol. 50: 119–124, 1974.
 40. Briggs, C. A., and J. R. Cooper. A synaptosomal preparation from the guinea pig ileum myenteric plexus. J. Neurochem. 36: 1097–1108, 1981.
 41. Briggs, C. A., and J. R. Cooper. Cholinergic modulation of the release of [3H]acetylcholine from synaptosomes of the myenteric plexus. J. Neurochem. 38: 501–508, 1982.
 42. Brown, D. R., and R. J. Miller. Neurotensin. Br Med. Bull. 38: 239–245, 1982.
 43. Brown, G. L., B. N. Davies, and J. S. Gillespie. The release of chemical transmitter from the sympathetic nerves of the intestine of the cat. J. Physiol. Lond. 143: 41–54, 1958.
 44. Brown, G. L., and J. S. Gillespie. The output of sympathetic transmitter from the spleen of the cat. J. Physiol. Lond. 138: 81–102, 1957.
 45. Browning, M. D., R. Huganir, and P. Greengard. Protein phosphorylation and neuronal function. J. Neurochem. 45: 11–23, 1985.
 46. Buck, S. H., E. Burcher, C. W. Shults, W. Lovenberg, and T. L. O'Donohue. Novel pharmacology of substance K‐binding sites: a third type of tachykinin receptor. Science Wash. DC 226: 987–989, 1984.
 47. Bulbring, E., and M. D. Gershon. 5‐Hydroxytryptamine participation in the vagal inhibitory innervation of the stomach. J. Physiol. Lond. 192: 823–846, 1967.
 48. Burnstock, G. Autonomic innervation and transmission. Br. Med. Bull. 35: 255–262, 1979.
 49. Burnstock, G. Electrophysiology of intestinal smooth muscle. In: Physiological and Regulatory Functions of Adenosine and Adenine Nucleotides, edited by H. P. Baer and G. I. Drummond. New York: Raven, 1979, p. 3–32.
 50. Burnstock, G. The ultrastructure of autonomic cholinergic nerves and junctions. Prog. Brain Res. 49: 3–21, 1979.
 51. Burnstock, G. Neurotransmitters and trophic factors in the autonomic nervous system. J. Physiol. Lond. 313: 1–35, 1981.
 52. Burnstock, G. Electrophysiology of intestinal smooth muscle. In: Cotransmission, edited by A. C. Cuello London: Macmillan, 1982, p. 151–163.
 53. Burnstock, G., and M. Costa. Adrenergic Neurons: Their Organization, Function and Development in the Peripheral Nervous System. New York: Wiley, 1975.
 54. Burnstock, G., and P. Sneddon. Evidence of ATP and noradrenaline as cotransmitters in sympathetic nerves. Clin. Sci. Lond. 68, Suppl. 10: 89s–92s, 1985.
 55. Catalan, R. E., A. M. Martinez, M. D. Aragones, B. G. Miguel, A. Robles, and J. E. Godoy. Effects of substance P on acetylcholinesterase activity. Biochem. Int. 8: 203–208, 1984.
 56. Catterall, W. A. The molecular basis of neuronal excitability. Science Wash. DC 223: 653–661, 1984.
 57. Ceccarelli, B., and W. P. Hurlbut. Vesicle hypothesis of the release of quanta of acetylcholine. Physiol. Rev. 60: 396–441, 1980.
 58. Chavkin, C., and A. Goldstein. Demonstration of a specific dynorphin receptor in guinea pig ileum myenteric plexus. Nature Lond. 291: 591–593, 1981.
 59. Checler, F., J.‐P. Vincent, and P. Kitabgi. Degradation of neurotensin by rat brain synaptic membranes: involvement of a thermolysin‐like metalloendopeptidase (enkephalinase), angiotensin‐converting enzyme, and other unidentified peptidases. J. Neurochem. 41: 375–384, 1983.
 60. Cheung, W. Y. Calmodulin: an overview. Federation Proc. 41: 2253–2257, 1982.
 61. Chubb, I. W., A. J. Hodgson, and G. H. White. Acetylcholinesterase hydrolyzes substance P. Neuroscience 5: 2065–2072, 1980.
 62. Clark, S. J., and T. W. Smith. Peristalsis abolishes the release of methionine‐enkephalin from guinea‐pig ileum in vitro. Eur. J. Pharmacol. 70: 421–424, 1981.
 63. Clark, S. J., and T. W. Smith. The release of met‐enkephalin from the guinea‐pig ileum at rest and during peristaltic activity. Life Sci. 33: 465–468, 1983.
 64. Cohen, M. L., and A. S. Landry. Vasoactive intestinal polypeptide: increased tone, enhancement of acetylcholine release, and stimulation of adenylate cyclase in intestinal smooth muscle. Life Sci. 26: 811–822, 1980.
 65. Collier, B. The preferential release of newly synthesized transmitter by a sympathetic ganglion. J. Physiol. Lond. 205: 341–352, 1969.
 66. Comb, M., P. H. Seeburg, J. Adelman, L. Eiden, and E. Hebert. Primary structure of the human Met‐ and Leuenkephalin precursor and its mRNA. Nature Lond. 295: 663–666, 1982.
 67. Cooper, J. R., and E. M. Meyer. Possible mechanisms involved in the release and modulation of release of neuroactive agents. Neurochem. Int. 6: 419–433, 1984.
 68. Correa, F. M. A., R. B. Innis, G. R. Uhl, and S. H. Snyder. Bradykinin‐like immunoreactive neuronal systems localized histochemically in rat brain. Proc. Natl. Acad. Sci. USA 76: 1489–1493, 1979.
 69. Costa, M., and J. B. Furness. Somatostatin is present in a subpopulation of noradrenergic nerve fibres supplying the intestine. Neuroscience 13: 911–919, 1984.
 70. Costa, M., J. B. Furness, R. Franco, I. Llewellyn‐Smith, R. Murphy, and A. M. Beardsley. Substance P in nerve tissue in the gut. In: Substance P in the Nervous System. London: Pitman, 1982, p. 129–144.
 71. Costa, M., J. B. Furness, and G. Gabella. Catecholamine containing nerve cells in the mammalian myenteric plexus. Histochemie 25: 103–106, 1971.
 72. Costa, M., J. B. Furness, I. J. Llewellyn‐Smith, and A. C. Cuello. Projections of substance P‐containing neurons within the guinea‐pig small intestine. Neuroscience 6: 411–424, 1981.
 73. Costa, M., J. B. Furness, I. J. Llewellyn‐Smith, B. Davies, and J. Oliver. An immunohistochemical study of the projections of somatostatin‐containing neurons in the guinea‐pig intestine. Neuroscience 5: 841–852, 1980.
 74. Costa, M., J. B. Furness, C. O. Pullin, and J. Bornstein. Substance P enteric neurons mediate non‐cholinergic transmission to the circular muscle of the guinea‐pig intestine. Naunyn‐Schmiedeberg's Arch. Pharmacol. 328: 446–453, 1985.
 75. Costa, M., J. B. Furness, N. Yanaihara, C. Yanaihara, and T. W. Moody. Distribution and projections of neurons with immunoreactivity for both gastrin‐releasing peptide and bombesin in the guinea‐pig small intestine. Cell Tissue Res. 235: 285–293, 1984.
 76. Costa, M., and G. Gabella. Adrenergic innervation of the alimentary canal. Z. Zellforsch. Mikrosk. Anat. 122: 357–377, 1971.
 77. Cowie, A. L., H. W. Kosterlitz, and A. A. Waterfield. Factors influencing the release of acetylcholine from the myenteric plexus of the ileum of the guinea‐pig and rabbit. Br. J. Pharmacol. 64: 565–580, 1978.
 78. Cowie, A. L., H. W. Kosterlitz, and A. J. Watt. Mode of action of morphine‐like drugs on autonomic neuro‐effectors. Nature Lond. 220: 1040–1042, 1968.
 79. Cox, B., and S. E. Hecker. Investigation of the mechanism of action of oxotremorine on the guinea‐pig isolated ileum preparation. Br. J. Pharmacol. 41: 19–25, 1971.
 80. Cox, B. M., and M. Weinstock. The effect of analgesic drugs on the release of acetylcholine from electrically stimulated guinea‐pig ileum. Br. J. Pharmacol. 27: 81–92, 1966.
 81. Cunnane, T. C., and L. Stjärne. Secretion of transmitter from individual varicosities of guinea‐pig and mouse vas deferens: all‐or‐none and extremely intermittent. Neuroscience 7: 2565–2576, 1982.
 82. Cunnane, T. C., and L. Stjärne. Transmitter secretion from individual varicosities of guinea‐pig and mouse vas deferens: highly intermittent and monoquantal. Neuroscience 13: 1–20, 1984.
 83. Dahlstrom, A., and J. Häggendal. Some quantitative studies on the noradrenaline contents in the cell bodies and terminals of a sympathetic adrenergic neuron system. Acta Physiol. Scand. 67: 271–277, 1966.
 84. Dale, H. H., and W. Feldberg. The chemical transmitter of vagus effects to the stomach. J. Physiol. Lond. 81: 320–334, 1934.
 85. Decamilli, P., R. Cameron, and P. Greengard. Synapsin I (protein I), a nerve terminal‐specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections. J. Cell Biol. 96: 1337–1354, 1983.
 86. Decamilli, P., S. M. Harris, W. B. Huttner, and P. Greengard. Synapsin I (protein I), a nerve terminal‐specific phosphoprotein: II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agarose‐embedded synaptosomes. J. Cell Biol. 96: 1355–1373, 1983.
 87. Del Castillo, J., and B. Katz. Biophysical aspects of neuromuscular transmission. Progr. Biophys. Biophys. Chem. 6: 121–170, 1956.
 88. DeLorenzo, R. J. Calmodulin in neurotransmitter release and synaptic function. Federation Proc. 41: 2265–2272, 1982.
 89. Del Tacca, M., G. Soldani, M. Selli, and A. Crema. Action of catecholamines on release of acetylcholine from human taenia coli. Eur. J. Pharmacol. 9: 80–84, 1970.
 90. Descarries, L., A. Beaudet, and K. C. Watkins. Serotonin nerve terminals in adult rat neocortex. Brain Res. 100: 563–588, 1975.
 91. Descarries, L., K. C. Watkins, and Y. Lapierre. Noradrenergic axon terminals in the cerebral cortex of rat. III. Topometric ultrastructural analysis. Brain Res. 133: 197–222, 1977.
 92. Deschodt‐Lanckmann, M., and N. D. Bui. Proglumide inhibits the degradation of cholecystokinin octapeptide and leucine‐enkephalin by brain enzymes. Biomed. Res. 3: 517–524, 1982.
 93. Deschodt‐Lanckmann, M., D. Koueischer, S. Przedborski, and M. Louwerays. Cholecystokinin octa‐ and tetrapeptide degradation by synaptic membranes. III. Inactivation of CCK‐8 by a phosphoramidon‐sensitive endopeptidase. Peptides 5: 649–951, 1984.
 94. Deschodt‐Lanckmann, M., and A. D. Strosberg. In vitro degradation of the C‐terminal octapeptide of cholecystokinin by ‘enkephalinase A’. FEBS Lett. 152: 109–113, 1983.
 95. Dingledine, R., and A. Goldstein. Effect of synaptic transmission blockade on morphine action in the guinea‐pig myenteric plexus. J. Pharmacol. Exp. Ther. 196: 97–106, 1976.
 96. Dingledine, R., A. Goldstein, and J. Kendig. Effects of narcotic opiates and serotonin on the electrical behavior of neurons in the guinea pig myenteric plexus. Life Sci. 14: 2299–2309, 1974.
 97. Dismukes, R. K. New concepts of molecular communication among neurons. Behav. Brain Sci. 2: 409–448, 1979.
 98. Dockray, G. J. Immunochemical evidence of cholecystokinin‐like peptides in brain. Nature Lond. 264: 568–570, 1976.
 99. Dockray, G. J. The physiology of cholecystokinin in brain and gut. Br. Med. Bull. 38: 253–258, 1982.
 100. Dodd, P. R., J. A. Edwardson, and G. Dockray. The depolarization‐induced release of cholecystokinin C‐terminal octapeptide (CCK‐8) from rat synaptosomes and brain slices. Regul. Pept. 1: 17–29, 1980.
 101. Domoto, T., J. Jury, I. Berezin, J. E. T. Fox, and E. E. Daniel. Does substance P comediate with acetylcholine in nerves of opossum esophageal muscularis mucosa? Am. J. Physiol. 245 (Gastrointest. Liver Physiol. 8): G19–G28, 1983.
 102. Donnerer, J., L. Bartho, P. Holzer, and L. Lembeck. Intestinal peristalsis associated with release of immunoreactive substance P. Neuroscience 11: 913–918, 1984.
 103. Donnerer, J., P. Holzer, and F. Lembeck. Release of dynorphin, somatostatin and substance P from the vascularly perfused small intestine of the guinea‐pig during peristalsis. Br. J. Pharmacol. 83: 919–925, 1984.
 104. Donnerer, J., D. K. Meyer, P. Holzer, and F. Lembeck. Release of cholecystokinin‐immunoreactivity into the vascular bed of guinea‐pig small intestine during peristalsis. Naunyn‐Schmiedeberg's Arch. Pharmacol. 328: 324–326, 1985.
 105. Dowe, G. H. C., H. Kilbinger, and V. P. Whittaker. Isolation of cholinergic synaptic vesicles from the myenteric plexus of guinea‐pig small intestine. J. Neurochem. 35: 993–1003, 1980.
 106. Down, J. A., and J. C. Szerb. Kinetics of morphine‐sensitive [3H]acetylcholine release from the guinea‐pig myenteric plexus. Br. J. Pharmacol. 68: 47–55, 1980.
 107. Downes, C. P. Inositol phospholipids and neurotransmitter‐receptor signalling mechanisms. Trends Neurosci. 6: 313–316, 1983.
 108. Dunant, Y. Electrophysiology of intestinal smooth muscle. In: Chemical Transmission 75 Years, edited by L. Stjärne, P. Hedqvist, H. Lagercrantz, and A. Wennmalm. New York: Academic, 1981, p. 165–178.
 109. Ekblad, E., R. Ekman, R. Håkanson, and F. Sundler. GRP neurones in the rat small intestine issue long anal projections. Regul. Pept. 9: 279–287, 1984.
 110. Ekblad, E., R. Håkanson, F. Sundler, and C. Wahlestedt. Galanin: neuromodulatory and direct contractile effects on smooth muscle preparations. Br. J. Pharmacol. 86: 241–246, 1985.
 111. Ekblad, E., A. Rokaeus, R. Håkanson, and F. Sundler. Galanin nerve fibers in the rat gut: distribution, origin and projections. Neuroscience 16: 355–363, 1985.
 112. Emson, P. C., and M. E. De Quidt NPY—a new member of the pancreatic polypeptide family. Trends Neurosci. 7: 31–35, 1984.
 113. Emson, P. C., C. M. Lee, and J. F. Rehfeld. Cholecystokinin octapeptide: vesicular localization and calcium dependent release from rat brain in vivo. Life Sci. 26: 2157–2162, 1980.
 114. Engel, G., M. Göthert, E. Muller‐Schweinitzer, E. Schlicker, L. Sistonen, and P. A. Stadler. Evidence for common pharmacological properties of [3H]5‐hydroxytrypta‐mine binding sites, presynaptic 5‐hydroxytryptamine autoreceptors in CNS and inhibitory presynaptic 5‐hydroxytryptamine receptors on sympathetic nerves. Naunyn‐Schmiedeberg's Arch. Pharmacol. 324: 116–124, 1983.
 115. Engel, G., D. Hoyer, H. O. Kalkman, and M. B. Wick. Identification of 5HT2‐receptors on longitudinal muscle of the guinea pig ileum. J. Recept. Res. 4: 113–126, 1984.
 116. Erdos, E. G., A. R. Johnson, and N. T. Boyden. Hydrolysis of enkephalin by cultured human endothelial cells and by purified peptidyl dipeptidases. Biochem. Pharmacol. 27: 843–848, 1978.
 117. Erulkar, S. D. The modulation of neurotransmitter release at synaptic junctions. Rev. Physiol. Biochem. Pharmacol. 98: 63–175, 1983.
 118. Euler, U. S. von, and J. H. Gaddum. An unidentified depressor substance in certain tissue extracts. J. Physiol. Lond. 72: 74–87, 1931.
 119. Fahrenkrug, J. Electrophysiology of intestinal smooth muscle. In: Vasoactive Intestinal Peptide, edited by S. I. Said New York: Raven, 1982, p. 361–372.
 120. Fahrenkrug, J., U. Haglund, M. Jodal, O. Lundgren, L. Olbe, and O. B. Schaffalitzky de Muckadell Nervous release of vasoactive intestinal polypeptide in the gastrointestinal tract of cats: possible physiological implications. J. Physiol. Lond. 284: 291–305, 1978.
 121. Finkleman, B. On the nature of inhibition in the intestine. J. Physiol. Lond. 70: 145–157, 1930.
 122. Floor, E. Substance P release from K+‐depolarized rat brain synaptosomes at one‐second resolution. Brain Res. 279: 321–324, 1983.
 123. Floor, E., O. Grad, and S. E. Leeman. Synaptic vesicles containing substance P purified by chromatography on controlled pore glass. Neuroscience 7: 1647–1655, 1982.
 124. Florey, E. Electrophysiology of intestinal smooth muscle. In: Inhibition in the Nervous System and Gamma‐Aminobutyric Acid, edited by E. Roberts, C. F. Baxter, A. van Harreveld, C. A. G. Wiersma, W. R. Adey, and K. F. Killiam. London: Pergamon, 1960, p. 72–84.
 125. Florey, E. Neurotransmitters and modulators in the animal kingdom. Federation Proc. 26: 1164–1178, 1967.
 126. Fosbraey, P., R. L. Featherstone, and I. K. M. Morton. Comparison of potency of substance P and related peptides on [3H]acetylcholine release, and contractile actions, in the guinea‐pig ileum. Naunyn‐Schmiedeberg's Arch. Pharmacol. 326: 111–115, 1984.
 127. Fosbraey, P., and E. S. Johnson. Electrophysiology of intestinal smooth muscle. In: Presynaptic Receptors, edited by J. de Belleroche. Chichester, UK: Horwood, 1982, p. 75–102.
 128. Fox, J., S. I. 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: 1134, 1979.
 129. Fozard, J. R. Neuronal 5‐HT receptors in the periphery. Neuropharmacology 23: 1473–1486, 1984.
 130. Franco, R., M. Costa, and J. B. Furness. Evidence for the release of endogenous substrate P from intestinal nerves. Naunyn‐Schmiedeberg's Arch. Pharmacol. 306: 195–201, 1979.
 131. Fredholm, B. B. Modulation of transmitter release—with special reference to adenosine: In: Chemical Neurotransmission 75 Years, edited by L. Stjärne, P. Hedqvist, H. Lagercrantz, and A. Wennmalm. New York: Academic, 1981, p. 211–222.
 132. Fredholm, B. B., and P. Hedqvist. Modulation of neurotransmission by purine nucleotides and nucleosides. Biochem. Pharmacol. 29: 1635–1643, 1980.
 133. Fried, G., L. Terenius, T. Hokfelt, and M. Goldstein. Evidence for differential localization of noradrenaline and neuropeptide Y in neuronal storage vesicles isolated from rat vas deferens. J. Neurosci. 5: 450–458, 1985.
 134. Fujisawa, H., T. Yamauchi, H. Nakata, and S. Okuno. Role of calmodulin in neurotransmitter synthesis. Federation Proc. 43: 3011–3014, 1984.
 135. Furness, J. B., and M. Costa. The nervous release and the action of substances which affect intestinal muscle through neither adrenoreceptors nor cholinoreceptors. Philos. Trans. R. Soc. Lond. B Biol. Sci. 265: 123–133, 1973.
 136. Furness, J. B., and M. Costa. The adrenergic innervation of the gastrointestinal tract. Rev. Physiol. Biochem. Exp. Pharmacol. 69: 1–51, 1974.
 137. Furness, J. B., and M. Costa. Actions of somatostatin on excitatory and inhibitory nerves in the intestine. Europ. J. Pharmacol. 56: 69–74, 1979.
 138. Furness, J. B., and M. Costa. Types of nerves in the enteric nervous system. Neuroscience 5: 1–20, 1980.
 139. Furness, J. B., and M. Costa. Electrophysiology of intestinal smooth muscle. In: Vasoactive Intestinal Peptide, edited by S. I. Said. New York: Raven, 1982, p. 391–406.
 140. Furness, J. B., and M. Costa. Electrophysiology of intestinal smooth muscle. In: Mediators and Drug in Gastrointestinal Motility, edited by G. Bertaccini. New York: Springer‐Verlag, 1982, p. 383–442.
 141. Furness, J. B., M. Costa, P. C. Emson, R. Håkanson, E. Moghimzadeh, F. Sundler, I. L. Taylor, and R. E. Chance. Distribution, pathways and reactions to drug treatment of nerves with neuropeptide Y‐ and pancreatic polypeptide‐like immunoreactivity in the guinea‐pig digestive tract. Cell Tissue Res. 234: 71–92, 1983.
 142. Furness, J. B., M. Costa, R. Franco, and I. J. Llewellyn‐Smith. Electrophysiology of intestinal smooth muscle. In: Neural Peptides and Neuronal Communication, edited by E. Costa and M. Trabucchi. New York: Raven, 1980, p. 601–617.
 143. Furness, J. B., M. Costa, and R. J. Miller. Distribution and projections of nerves with enkephalin‐like immunoreactivity in the guinea pig small intestine. Neuroscience 8: 653–664, 1983.
 144. Gaddum, J. H., and Z. P. Picarelli. Two kinds of tryptamine receptor. Br. J. Pharmacol. Chemother. 12: 323–328, 1957.
 145. Gaginella, T. S., T. M. O'Doriso, and K. A. Hubel. Release of vasoactive intestinal polypeptide by electrical field stimulation of rabbit ileum. Regul. Pept. 2: 165–174, 1981.
 146. Geary, L. E., K. S. Wiley, W. L. Scott, and M. L. Cohen. Degradation of exogenous enkephalin in the guinea‐pig ileum: relative importance of aminopeptidase, enkephalinase and angiotensin converting enzyme activity. J. Pharmacol. Exp. Ther. 221: 104–111, 1982.
 147. Gershon, M. The enteric nervous system. Annu. Rev. Neurosci. 4: 227–272, 1981.
 148. Gershon, M. D., and S. M. Erde. The nervous system of the gut. Gastroenterology 80: 1571–1594, 1981.
 149. Gillespie, J. S., and B. R. McKenna. The inhibitory action of the sympathetic nerves on the smooth muscle of the rabbit gut, its reversal by reserpine and restoration by catecholamines and by dopa. J. Physiol. Lond. 156: 17–34, 1961.
 150. Gintzler, A. R. Substance P involvement in the expression of gut dependence on opiates. Brain Res. 182: 224–228, 1980.
 151. Gintzler, A. R., and J. A. Scalisi. Effects of opioids on noncholinergic excitatory responses of the guinea‐pig isolated ileum: inhibition of release of enteric substance P. Br. J. Pharmacol. 75: 199–205, 1982.
 152. Giotti, A., S. Luzzi, S. Spagnesi, and L. Zilletti. GABAa and GABAb receptor‐mediated effects in guinea‐pig ileum. Br. J. Pharmacol. 78: 469–478, 1983.
 153. Giraud, A., A.‐C. Jonsson, and G. Dockray. Pro‐enkephalin gene derived peptides in the porcine stomach: cellular distribution and molecular forms. Peptides 5: 757–763, 1984.
 154. Goltermann, N. R., J. F. Rehfeld, and H. Roigaardpetersen. In vivo biosynthesis of cholecystokinin in rat cerebral cortex. J. Biol. Chem. 255: 6181–6185, 1980.
 155. Gordon‐Weeks, P. R. Noradrenergic and non‐noradrenergic nerves containing small granular vesicles in Auerbach's plexus of the guinea‐pig: evidence against the presence of noradrenergic synapses. Neuroscience 7: 2925–2936, 1982.
 156. Göthert, M. Serotonin‐receptor‐mediated modulation of Ca2+‐dependent 5‐hydroxytryptamine release from neurones of the rat brain cortex. Naunyn‐Schmiedeberg's Arch. Pharmacol. 314: 223–230, 1980.
 157. Göthert, M. Modulation of serotonin release in the brain via presynaptic receptors. Trends Pharmacol. Sci. 3: 437–440, 1982.
 158. Goyal, R. K., S. Rattan, and S. I. Said. VIP as a possible neurotransmitter of non‐cholinergic, non‐adrenergic inhibitory neurons. Nature Lond. 288: 378–380, 1980.
 159. Greengard, P. Electrophysiology of intestinal smooth muscle. In: Chemical Neurotransmission 75 Years, edited by L. Stjärne, P. Hedqvist, H. Lagercrantz, and A. Wennmalm. New York: Academic, 1981, p. 377–384.
 160. Grider, J. R., M. B. Cable, S. I. Said, and G. M. Makhlouf. Vasoactive intestinal peptide as a neural mediator of gastric relaxation. Am. J. Physiol. 248 (Gastrointest. Liver Physiol. 11): G73–G78, 1985.
 161. Gubler, U., P. Seeburg, B. J. Hoffman, L. P. Gage, and S. Udenfriend. Molecular cloning establishes proenkephalin as precursor of enkephalin‐containing peptides. Nature Lond. 295: 206–209, 1982.
 162. Gustafsson, L. Influence of adenosine on responses to vagal nerve stimulation in the anesthetized rabbit. Acta Physiol. Scand. 111: 263–268, 1981.
 163. Gustafsson, L., B. B. Fredholm, and P. Hedqvist. Theophylline interferes with the modulatory role of endogenous adenosine on cholinergic neurotransmission in guinea‐pig ileum. Acta Physiol. Scand. 111: 269–280, 1981.
 164. Gustafsson, L., P. Hedqvist, B. B. Fredholm, and G. Lundgren. Inhibition of acetylcholine release in guinea pig ileum by adenosine. Acta Physiol. Scand. 104: 469–478, 1978.
 165. Hadhazy, P., and J. C. Szerb. The effect of cholinergic drugs on 3H‐acetylcholine release from slices of rat hippocampus, striatum and cortex. Brain Res. 123: 311–322, 1977.
 166. Haggendal, J. Electrophysiology of intestinal smooth muscle. In: New Aspects of Storage and Release Mechanisms of Catecholamines, edited by H. J. Schümann and G. Kroneberg. Berlin: Springer‐Verlag, 1970, p. 100–109.
 167. Hayashi, E., M. Mori, S. Yamada, and M. Kunitomo. Effects of purine compounds on cholinergic nerves. Specificity of adenosine and related compounds on acetylcholine release in electrically stimulated guinea‐pig ileum. Eur. J. Pharmacol. 48: 297–307, 1978.
 168. Hedqvist, P. Electrophysiology of intestinal smooth muscle. In: Chemical Neurotransmission 75 Years, edited by L. Stjärne, P. Hedqvist, H. Lagercrantz, and A. Wennmalm. New York: Academic, 1981, p. 223–233.
 169. Hellstrom, P., O. Olerup, and K. Tatemoto. Neuropeptide Y may mediate effects of sympathetic nerve stimulation on colonic motility and blood flow in the cat. Acta Physiol. Scand. 124: 613–624, 1985.
 170. Hersh, L. B. Solubilization and characterization of two rat brain membrane‐bound aminopeptidases active on met‐enkephalin. Biochemistry 20: 2345–2350, 1981.
 171. Hertting, A., J. Axelrod, and L. G. Whitby. Effect of drugs on the uptake and metabolism of 3H‐norepinephrine. J. Pharmacol. Exp. Ther. 134: 146–153, 1961.
 172. Heuser, J. E., and T. S. Reese. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57: 315–344, 1973.
 173. Heuser, J. E., and T. S. Reese. Electrophysiology of intestinal smooth muscle. In: Handbook of Physiology. The Nervous System. Cellular Biology of Neurons, edited by E. R. Kandel. Bethesda, MD: Am. Physiol. Soc, 1977, vol. I, chapt. 8, p. 261–294.
 174. Heymann, E., and R. Mentlein. Liver dipeptidyl aminopeptidase IV hydrolyzes substance P. FEBS Lett. 91: 360–364, 1978.
 175. Holtzman, E. The origin and fate of secretory packages, especially synaptic vesicles. Neuroscience 2: 327–355, 1977.
 176. Holzer, P. Characterization of the stimulus‐induced release of immunoreactive substance P from the myenteric plexus of the guinea‐pig small intestine. Brain Res. 297: 127–136, 1984.
 177. Holzer, P., and F. Lembeck. Neurally mediated contraction of ileal longitudinal muscle by substance P. Neurosci. Lett. 17: 101–105, 1980.
 178. Hotta, Y. Some properties of the junctional and extrajunctional receptors in the vas deferens of the guinea‐pig. Agents Actions 1: 69–77, 1969.
 179. Hughes, J. Biogenesis, release and inactivation of enkephalins and dynorphins. Br. Med. Bull. 39: 17–24, 1983.
 180. Hughes, J., H. W. Kosterlitz, and T. W. Smith. The distribution of methionine‐enkephalin and leucine‐enkephalin in the brain and peripheral tissues. Br. J. Pharmacol. 61: 639–647, 1977.
 181. Hui, K.‐S., and A. Lajtha. Neuropeptidases. In: Handbook of Neurochemistry ( 2nd ed.), edited by A. Lajtha. New York: Plenum, 1983, vol. 4, p. 1–19.
 182. Humphrey, P. P. A. Peripheral 5‐hydroxytryptamine receptors and their classification. Neuropharmacology 23: 1503–1510, 1984.
 183. Huttner, W. B., W. Scheibler, P. Greengard, and P. Decamilli. Synapsin I (protein I), a nerve terminal‐specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell Biol. 96: 1374–1388, 1983.
 184. Innis, R. B., D. C. Manning, J. M. Stewart, and S. H. Snyder. [3H]Bradykinin receptor binding in mammalian tissue membranes. Proc. Natl. Acad. Sci. USA 78: 2630–2634, 1981.
 185. Israel, M., Y. Dunant, and R. Manaranche. The present status of the vesicular hypothesis. Prog. Neurobiol. 13: 237–275, 1979.
 186. Israel, M., B. Lesbats, F. M. Meunier, and J. Stinnakre. Postsynaptic release of adenosine triphosphate induced by single impulse transmitter action. Proc. R. Soc. Lond. Biol. Sci. B 193: 461–468, 1976.
 187. Iversen, L. L. Electrophysiology of intestinal smooth muscle. In: Neuroscience Third Study Program, edited by F. O. Schmitt and F. G. Worden. Cambridge, MA: MIT Press, 1974, p. 905–915.
 188. Iversen, L. L. Substance P. Br. Med. Bull. 38: 277–282, 1982.
 189. Iversen, L. L., T. Jessell, and I. Kanazawa. Release and metabolism of substance P in rat hypothalamus. Nature Lond. 264: 81–83, 1976.
 190. Iversen, L. L., and S. Z. Langer. Effects of phenoxybenzamine on the uptake and metabolism of noradrenaline in the rat heart and vas deferens. Br. J. Pharmacol. 37: 627–637, 1969.
 191. Jonakait, G. M., A. R. Gintzler, and M. D. Gershon. Isolation of axonal varicosities (autonomic synaptosomes) from the enteric nervous system. J. Neurochem. 32: 1387–1400, 1979.
 192. Jonakait, G. M., H. Tamir, A. R. Gintzler, and M. D. Gershon Release of [3H]serotonin and its binding protein from enteric neurons. Brain Res. 174: 55–69, 1979.
 193. Jonakait, G. M., H. Tamir, M. M. Rapport, and M. D. Gershon. Detection of a soluble serotonin‐binding protein in the mammalian myenteric plexus and other peripheral sites of serotonin storage. J. Neurochem. 28: 277–284, 1977.
 194. Kalsner, S. Single pulse stimulation of guinea‐pig vas deferens and the presynaptic receptor hypothesis. Br. J. Pharmacol. 66: 343–349, 1979.
 195. Kalsner, S. Limitation of presynaptic adrenoceptor theory:—the characteristics of the effects of noradrenaline and phenoxybenzamine on stimulation‐induced efflux of [3H]noradrenaline in vas deferens. J. Pharmacol. Exp. Ther. 212: 232–239, 1980.
 196. Kalsner, S. Evidence against the unitary hypothesis of agonist and antagonist action at presynaptic adrenoceptors. Br. J. Pharmacol. 77: 375–380, 1982.
 197. Kalsner, S. Is there feedback regulation of neurotransmitter release by autoreceptors? Biochem. Pharmacol. 34: 4085–4097, 1985.
 198. Kamikawa, Y., and Y. Shimo. Indirect action of 5‐hydroxytryptamine on the isolated muscularis mucosae of the guinea‐pig esophagus. Br. J. Pharmacol. 78: 103–110, 1983.
 199. Katayama, Y., and R. A. North. The action of somatostatin on neurones of the myenteric plexus of the guinea‐pig ileum. J. Physiol. Lond. 303: 315–323, 1980.
 200. Kato, T., T. Nagatsu, K. Fukasawa, K. Harada, I. Nagatsu, and S. Sakakibara. Successive cleavage of N‐terminal Arg1‐Pro2 and Lys3‐Pro4 from substance P but no release of Arg1‐Pro2 from bradykinin, by X‐Pro dipeptidyl‐aminopeptidase. Biochim. Biophys. Acta 525: 417–422, 1978.
 201. Katz, B. The transmission of impulses from nerve to muscle, and the subcellular unit of synaptic action. Proc. R. Soc. Lond. B Biol. Sci. 155: 455–477, 1962.
 202. Katz, B. The Release of Neural Transmitter Substances. Liverpool, UK: Liverpool Univ. Press, 1969.
 203. Kazic, T. Effect of adrenergic factors on peristalsis and acetylcholine release. Eur. J. Pharmacol. 16: 367–373, 1971.
 204. Keast, J. R., J. B. Furness, and M. Costa. Somatostatin in human enteric nerves. Distribution and characterization. Cell Tissue Res. 237: 299–308, 1984.
 205. Keast, J. R., J. B. Furness, and M. Costa. Different substance P receptors are found on muscosal epithelial cells and submucous neurons of the guinea‐pig small intestine. Naunyn‐Schmiedeberg's Arch. Pharmacol. 329: 382–387, 1985.
 206. Kelly, R. S., J. W. Deutsch, S. S. Carlson, and J. A. Wagner. Biochemistry of neurotransmitter release. Annu. Rev. Neurosci. 2: 399–446, 1979.
 207. Kerr, D. I. B., and A. Krantis. Uptake and stimulus‐evoked release of [3H]‐γ‐aminobutyric acid by myenteric nerves of guinea‐pig intestine. Br. J. Pharmacol. 78: 271–276, 1983.
 208. Kilbinger, H. Modulation of oxotremorine and atropine of acetylcholine release evoked by electrical stimulation of the myenteric plexus of the guinea‐pig ileum. Naunyn‐Schmiedeberg's Arch. Pharmacol. 300: 145–151, 1977.
 209. Kilbinger, H. Facilitation and inhibition by muscarinic agonists of acetylcholine release from guinea‐pig myenteric neurones: mediation through different types of neuronal muscarinic receptors. Trends Pharmacol. Sci. Suppl. Jan: 49–52, 1984.
 210. Kilbinger, H., and M. Nafziger. Two types of neuronal muscarine receptors modulating acetylcholine release from guinea‐pig myenteric plexus. Naunyn‐Schmiedeberg's Arch. Pharmacol. 328: 304–309, 1985.
 211. Kilbinger, H., and I. Pfeuffer‐Friederich. Two types of receptors for 5‐hydroxytryptamine on the cholinergic nerves of the guinea‐pig myenteric plexus. Br. J. Pharmacol. 85: 529–539, 1985.
 212. Kilbinger, H., and P. Wagner. Inhibition of oxotremorine of acetylcholine resting release from guinea‐pig ileum longitudinal muscle strips. Naunyn‐Schmiedeberg's Arch. Pharmacol. 287: 47–60, 1975.
 213. Kilbinger, H., and I. Wessler. Increase by α‐adrenolytic drugs of acetylcholine release evoked by field stimulation of the guinea‐pig ileum. Naunyn‐Schmiedeberg's Arch. Pharmacol. 309: 255–257, 1979.
 214. Kilbinger, H., and I. Wessler. Inhibition by acetylcholine of the stimulation‐evoked release of 3H‐acetylcholine from the guinea‐pig myenteric plexus. Neuroscience 5: 1331–1340, 1980.
 215. Kishimoto, S., R. Kato, T. Mukai, A. Kanbara, K. Okamoto, S. Shimizu, K. Daitoku, and G. Kajiyama. Distribution and endocrine morphology of polypeptide YY (PYY) containing cells in the human gut. Hiroshima J. Med. Sci. 34: 155–160, 1985.
 216. Klaff, L. J., A. M. Hudson, M. Paul, and R. P. Miller. A method for studying synaptosomal release of neurotransmitter candidates, as evaluated by studies on cortical cholecystokinin octapeptide release. Peptides 3: 155–161, 1982.
 217. Kleinrok, A., and H. Kilbinger. γ‐Aminobutyric acid and cholinergic transmission in the guinea‐pig ileum. Naunyn‐Schmiedeberg's Arch. Pharmacol. 322: 216–220, 1983.
 218. Knoll, J., and E. S. Vizi. Presynaptic inhibition of acetylcholine release by endogenous and exogenous noradrenaline at high rate stimulation. Br. J. Pharmacol. 40: 554P–555P, 1970.
 219. Krantis, A., M. Costa, J. B. Furness, and J. Orbach. γ‐Aminobutyric acid stimulates intrinsic inhibitory and excitatory nerves in the guinea‐pig intestine. Eur. J. Pharmacol. 67: 461–468, 1980.
 220. Krnjevi, K. Chemical nature of synaptic transmission in vertebrates. Physiol. Rev. 54: 418–540, 1974.
 221. Kromer, W., V. Hollt, H. Schmidt, and A. Herz. Release of immunoreactive‐dynorphin from the isolated guinea‐pig small intestine is reduced during peristaltic activity. Neurosci. Lett. 25: 53–56, 1981.
 222. Kromer, W., and W. Pretzlaff. In vitro evidence for the participation of intestinal opioids in the control of peristalsis in the guinea pig small intestine. Naunyn‐Schmiedeberg's Arch. Pharmacol. 309: 153–157, 1979.
 223. Kromer, W., W. Pretzlaff, and R. Woinoff. Opioids modulate periodicity rather than efficacy of peristaltic waves in the guinea pig ileum in vitro. Life Sci. 26: 1857–1865, 1980.
 224. Kromer, W., E. Scheiblhuber, and P. Illes. Functional antagonism by calcium of an intrinsic opioid mechanism in the guinea‐pig isolated ileum. Neuropharmacology 19: 839–843, 1980.
 225. Kromer, W., and H. Schmidt. Opioids modulate intestinal peristalsis at a site of action additional to that modulating acetylcholine release. J. Pharmacol. Exp. Ther. 223: 271–274, 1982.
 226. Kupfermann, I. Modulatory actions of neurotransmitters. Annu. Rev. Neurosci. 2: 447–465, 1979.
 227. Kuwahara, A., T. Ishikawa, S.‐I. Mikami, and N. Yanaihara. Distribution of neurons containing immunoreactivity for gastrin‐releasing peptide (GRP), substance P, and vasoactive intestinal polypeptide (VIP) in the rat gastric wall. Biomed. Res. 4: 473–478, 1983.
 228. Laduron, P. M. Presynaptic heteroreceptors in regulation of neuronal transmission. Biochem. Pharmacol. 34: 467–470, 1985.
 229. Landmesser, L., and G. Pilar. The onset and development of transmission in the chick ciliary ganglion. J. Physiol. Lond. 222: 691–713, 1972.
 230. Langer, S. Z. Presynaptic receptors and their role in the regulation of transmitter release. Br. J. Pharmacol. 60: 481–497, 1977.
 231. Larsson, L.‐I., S. Childers, and S. H. Snyder. Met‐ and Leu‐enkephalin immunoreactivity in separate neurones. Nature Lond. 282: 407–410, 1979.
 232. Larsson, L.‐I., and J. F. Rehfeld. Localization and molecular heterogeneity of cholecystokinin in the central and peripheral nervous system. Brain Res. 165: 201–218, 1979.
 233. Leander, S., R. Ekman, R. Uddman, F. Sundler, and R. Håkanson. Neuronal cholecystokinin, gastrin‐releasing peptide, neurotensin, and β‐endorphin in the intestine of the guinea pig. Distribution and possible motor functions. Cell Tissue Res. 235: 521–531, 1984.
 234. Legay, C., M. J. Saffrey, and G. Burnstock. Coexistence of immunoreactive substance P and serotonin in neurones of the gut. Brain Res. 302: 379–382, 1984.
 235. Llinas, R. R., and J. E. Heuser. Depolarization‐release coupling systems in neurons. Neurosci. Res. Program Bull 15: 557–687, 1978.
 236. Lundberg, J. M. Evidence for coexistence of vasoactive intestinal polypeptide (VIP) and acetylcholine in neurons of cat exocrine glands. Acta Physiol. Scand. Suppl. 496: 1–57, 1981.
 237. Lundberg, J. M., A. Anggard, J. Fahrenkrug, O. Johansson, and T. Hokfelt. Vasoactive intestinal polypeptide in cholinergic neurons of exocrine glands. In: Vasoactive Intestinal Peptide, edited by S. I. Said. New York: Raven, 1982, p. 373–389.
 238. Lundberg, J. M., A. Saria, A. Franco‐Cereceda, T. Hokfelt, L. Terenius, and M. Goldstein. Differential effects of reserpine and 6‐hydroxydopamine on neuropeptide Y (NPY) and noradrenaline in peripheral neurons. Naunyn‐Schmiedeberg's Arch. Pharmacol. 328: 331–340, 1985.
 239. Macintosh, F. C., and P. E. Oborin. Release of acetylcholine from intact cerebral cortex. Proc. Int. Congr. Physiol. Sci., 19th, Montreal, 1953, p. 580–581.
 240. Maeda, M., H. Takagi, Y. Kubota, Y. Morishima, F. Akai, S. Hashimoto, and S. Mori. The synaptic relationship between vasoactive intestinal polypeptide (VIP)‐like immunoreactive neurons and their axon terminals in the rat small intestine: light and electron microscopic study. Brain Res. 329: 356–359, 1985.
 241. Makhlouf, G. M. Electrophysiology of intestinal smooth muscle. In: The Gastroenterology Annual, edited by F. Kern and A. L. Blum. Amsterdam: Elsevier, 1983, vol. 1, p. 181–197.
 242. Makhlouf, G. M. Electrophysiology of intestinal smooth muscle. In: The Gastroenterology Annual, edited by F. Kern and A. L. Blum. Amsterdam: Elsevier, 1984, vol. 2, p. 177–189.
 243. Makhlouf, G. M. Enteric neuropeptides: role in neuromuscular activity of the gut. Trends Pharmacol. Sci. 6: 214–218, 1985.
 244. Malfroy, B., J. P. Swerts, A. Guyon, B. P. Roques, and J.‐C. Schwartz. High‐affinity enkephalin‐degrading peptidase in brain is increased after morphine. Nature Lond. 276: 523–526, 1978.
 245. Manber, L., and M. D. Gershon. A reciprocal adrenergic‐cholinergic axoaxonic synapse in the mammalian gut. Am. J. Physiol. 236 (Endocrinol. Metab. Gastrointest. Physiol. 5): E738–E745, 1979.
 246. Matsas, R., I. S. Fulcher, A. J. Kenny, and A. J. Turner. Substance P and [Leu]enkephalin are hydrolysed by an enzyme in pig caudate synaptic membranes that is identical with the endopeptidase of kidney microvilli. Proc. Natl. Acad. Sci. USA 80: 3111–3115, 1983.
 247. Matsas, R., A. J. Turner, and A. J. Kenny. Endopeptidase‐24:11 and aminopeptidase activity in brain synaptic membranes are jointly responsible for the hydrolysis of cholecystokinin octapeptide (CCK‐8). FEBS Lett. 175: 124–128, 1984.
 248. Mayer, E. A., J. Elashoff, J. H. Walsh Characterization of bombesin effects on canine gastric muscle. Am. J. Physiol. 243 (Gastrointest. Liver Physiol. 6): G141–G147, 1982.
 249. McKnight, A. T., R. P. Sosa, J. Hughes, and H. W. Kosterlitz. Electrophysiology of intestinal smooth muscle. In: Characteristics and Function of Opioids, edited by J. M. van Ree and L. Terenius. Amsterdam: Elsevier/North‐Holland, 1978, p. 259–269.
 250. Melander, T., T. Hokfelt, A. Rokaeus, J. Fahrenkrug, K. Tatemoto, and V. Mutt. Distribution of galanin‐like immunoreactivity in the gastro‐intestinal tract of several mammalian species. Cell Tissue Res. 239: 253–270, 1985.
 251. Meyer, E. M., and D. H. Otero. Pharmacological and ionic characterizations of the muscarinic receptors modulating [3H]acetylcholine release from rat cortical synaptosomes. Neuroscience 5: 1202–1207, 1985.
 252. Miller, R. J. PHI and GRF: two new members of the glucagon/secretin family. Med. Biol. Helsinki 61: 159–162, 1984.
 253. Mitchell, R. H. Inositol phospholipids and cell surface receptor functions. Biochim. Biophys. Acta 415: 81–147, 1975.
 254. Mitchell, R. H. Is phosphatidylinositol really out of the calcium gate? Nature Lond. 296: 492–493, 1982.
 255. Mo, N., R. Ammari, and N. J. Dun. Prostaglandin E1 inhibits calcium‐dependent potentials in mammalian sympathetic neurons. Brain Res. 334: 325–349, 1985.
 256. Moghimzadeh, E., R. Ekman, R. Håkanson, N. Yanaihara, and F. Sundler. Neuronal gastrin‐releasing peptide in the mammalian gut and pancreas. Neuroscience 10: 553–563, 1983.
 257. Morgan, K. G., P. F. Schmalz, V. L. W. Go, and J. H. Szurszewski. Electrical and mechanical effects of molecular variants of CCK on antral smooth muscle. Am. J. Physiol. 235 (Endocrinol. Metab. Gastrointest. Physiol. 4): E324–E329, 1978.
 258. Morgan, K. G., P. F. Schmalz, and J. H. Szurszewski. 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.
 259. Moritoki, H., T. Kanbe, M. Maruoka, M. Ohara, and Y. Ishida. Potentiation by dipyridamole of the inhibition of guinea‐pig ileum twitch response caused by adenine derivatives. J. Pharmacol. Exp. Ther. 204: 343–350, 1978.
 260. Moritoki, H., M. Morita, and T. Kanbe. Effects of methylxanthines and imidazole on the contractions of guinea‐pig ileum induced by transmural stimulation. Eur. J. Pharmacol. 35: 185–198, 1976.
 261. Narahashi, T., J. W. Moore, and W. R. Scott. Tetrodotoxin blockage of sodium conductance increase in lobster giant axons. J. Gen. Physiol. 47: 965–974, 1964.
 262. Nemeth, P. R., C. A. Ort, and J. D. Wood. Intracellular study of effects of histamine on electrical behavior of myenteric neurones in guinea‐pig small intestine. J. Physiol. Lond. 355: 411–425, 1984.
 263. Nestler, E. J., S. I. Walaas, and P. Greengard. Neuronal phosphoproteins: physiological and clinical implications. Science Wash. DC 225: 1357–1364, 1984.
 264. Nicoll, R. A., C. Schenker, and S. E. Leeman. Substance P as a transmitter candidate. Annu. Rev. Neurosci. 3: 227–268, 1980.
 265. Nishizuka, Y. Turnover of inositol phospholipids and signal transduction. Science Wash. DC 225: 1365–1370, 1984.
 266. Noda, M., Y. Furutani, H. Takahashi, M. Toyasato, T. Hirose, S. Inayama, S. Nakanishi, and S. Numa. Cloning and sequence analysis of cDNA for bovine adrenal preproenkephalin. Nature Lond. 295: 202–206, 1982.
 267. North, R. A. Electrophysiology of the enteric nervous system. Neuroscience 7: 315–325, 1982.
 268. North, R. A., G. Henderson, Y. Katayama, and S. M. Johnson. Electrophysiological evidence for presynaptic inhibition of acetylcholine release by 5‐hydroxytryptamine in the enteric nervous system. Neuroscience 5: 581–586, 1980.
 269. O'Donohue, T. L., B. M. Chronwall, R. M. Pruss, E. Mezey, J. Z. Kiss, L. E. Eiden, V. J. Massari, R. E. Tessel, V. M. Pickel, D. A. Dimaggio, A. J. Hotchkiss, W. R. Crowley, and Z. Zukowska‐Grojec. Neuropeptide Y and peptide YY neuronal and endocrine systems. Peptides 6: 755–768, 1985.
 270. Orlowski, M. Proteinases. In: Handbook of Neurochemistry ( 2nd ed.), edited by A. Lajtha. New York: Plenum, 1983, vol. 4, p. 21–66.
 271. Osborne, N. N. Communication between neurons: current concepts. Neurochem. Int. 3: 3–16, 1981.
 272. Otsuka, M., S. Konishi, and T. Takahashi. A further study of the motoneuron depolarizing peptide extracted from dorsal roots of bovine spinal nerves. Proc. Jpn. Acad. 48: 747–752, 1972.
 273. Palade, G. E. Intracellular aspects of the process of protein synthesis. Science Wash. DC 189: 347–357, 1975.
 274. Paton, W. D. M., and E. S. Vizi. The inhibitory action of noradrenaline and adrenaline on acetylcholine output by guinea‐pig longitudinal muscle strip. Br. J. Pharmacol. 35: 10–28, 1969.
 275. Paton, W. D. M., E. S. Vizi, and M. A. Zar. The mechanism of acetylcholine release from parasympathetic nerves. J. Physiol. Lond. 215: 819–848, 1971.
 276. Paton, W. D. M., and M. A. Zar. The origin of acetylcholine released from guinea‐pig intestine and longitudinal muscle strips. J. Physiol. Lond. 194: 13–33, 1968.
 277. Patterson, S. J., L. E. Robson, and H. W. Kosterlitz. Classification of opioid receptors. Br. Med. Bull. 39: 31–36, 1983.
 278. Peper, K., F. Dreyer, C. Sandri, K. Akert, and H. Moor. Structure and ultrastructure of the frog motor endplate. A freeze‐etch study. Cell Tissue Res. 149: 437–455, 1974.
 279. Pert, C. B., and S. H. Snyder. High affinity transport of choline into the myenteric plexus of guinea‐pig intestine. J. Pharmacol. Exp. Ther. 191: 102–108, 1974.
 280. Phillis, J. W., and R. A. Barraco. Electrophysiology of intestinal smooth muscle. In: Advances in Cyclic Nucleotide and Protein Phosphorylation Research, edited by D. M. F. Cooper and K. B. Seamon. New York: Raven, 1985, vol. 19, p. 257.
 281. Potter, L. T. Synthesis, storage and release of [14C]acetylcholine in isolated rat diaphragm muscles. J. Physiol. Lond. 206: 145–166, 1970.
 282. Powis, D. A. Does Na,K‐ATPase play a role in the regulation of neurotransmitter release by prejunctional α‐adrenoceptors? Biochem. Pharmacol. 30: 2389–2397, 1981.
 283. Quirion, R. Multiple tachykinin receptors. Trends Neurosci. 8: 183–185, 1985.
 284. Reese, J. H., and J. R. Cooper. Modulation of the release of acetylcholine from ileal synaptosomes by adenosine and adenosine 5'‐triphosphate. J. Pharmacol. Exp. Ther. 223: 612–616, 1982.
 285. Reese, J. H., and J. R. Cooper. Stimulation of acetylcholine release from guinea‐pig ileal synaptosomes by cyclic nucleotides and forskolin. Biochem. Pharmacol. 33: 3007–3011, 1984.
 286. Rehfeld, J. F. Neuronal cholecystokinin: one or multiple transmitters? J. Neurochem. 44: 1–10, 1985.
 287. Reichlin, S. N. Engl. J. Med. 309: 1495–1501, 1556–1563, 1983.
 288. Ribeiro, J. A. ATP; related nucleotides and adenosine on neurotransmission. Life Sci. 22: 1373–1380, 1978.
 289. Ribeiro, J. A. Purinergic modulation of transmitter release. J. Theor. Biol. 80: 259–270, 1979.
 290. Robinson, J. D., and M. S. Flashner. The Na+ + K+‐activated ATPase enzymatic and transport properties. Biochim. Biophys. Acta 549: 145–176, 1979.
 291. Robinson, P. J., and P. R. Dunkley. Depolarisation‐dependent protein phosphorylation in rat cortical synaptosomes: factors determining the magnitude of the response. J. Neurochem. 41: 909–918, 1983.
 292. Rodnight, R. Protein kinases and phosphatases. In: Handbook of Neurochemistry ( 2nd ed.), edited by A. Lajtha. New York: Plenum, 1983, vol. 4, p. 195–217.
 293. Rosell, S., A. Al‐Saffar, and K. Thor. The role of neurotensin in gut motility. Scand. J. Gastroenterol. Suppl. 19: 69–75, 1984.
 294. Rubinstein, R., and S. Cohen. Histamine‐mediated acetylcholine release in the guinea‐pig ileum. Eur. J. Pharmacol. 111: 245–250, 1985.
 295. Rutledge, C. O. Effect of metabolic inhibitors and ouabain on amphetamine‐ and potassium‐induced release of biogenic amines from isolated brain tissue. Biochem. Pharmacol. 27: 511–516, 1978.
 296. Ryan, L. J., J. M. Tepper, and S. F. Sawyer. Autoreceptor activation in central monoamine neurons: modulation of neurotransmitter release is not mediated by intermittent axonal conduction. Neuroscience 4: 925–931, 1985.
 297. Said, S. I. Vasoactive intestinal polypeptide (VIP): current status. Peptides 5: 143–150, 1984.
 298. Sato, T., I. Takayanagi, and K. Takagi. Pharmacological properties of electrical activities obtained from neurons in Auerbach's plexus. Jpn. J. Pharmacol. 23: 665–671, 1973.
 299. Sato, T., I. Takayanagi, and K. Takagi. Effects of acetylcholine releasing drugs on electrical activities obtained from Auerbach's plexus in the guinea‐pig ileum. Jpn. J. Pharmacol. 24: 447–451, 1974.
 300. Sawynok, J., and K. H. Jhamandas. Inhibition of acetylcholine release from cholinergic nerves by adenosine, adenine nucleotides and morphine: antagonism by theophylline. J. Pharmacol. Exp. Ther. 197: 379–390, 1976.
 301. Schaffalitzky de Muckadell, O. B., J. Fahrenkrug, and J. J. Holst. Release of vasoactive intestinal polypeptide (VIP) by electrical stimulation of the vagal nerves. Gastroenterology 72: 373–375, 1977.
 302. Scheuermann, D. W., and W. Stach. A simultaneous demonstration of particular enteric neuronal cell types with the NADH:nitro BT‐dehydrogenase reaction and of nerve fibers containing enkephalin‐like immunoreactivity in the myenteric plexus of the porcine small intestine. Histochemistry 82: 269–273, 1985.
 303. Schultzberg, M., M. Hökfelt, G. Nilsson, L. Terenius, J. F. Rehfeld, M. Brown, R. Elde, M. Goldstein, and S. Said. Distribution of peptide‐ and catecholamine‐containing neurons in the gastrointestinal tract of rat and guinea‐pig: immunohistochemical studies with antisera to substance P, vasoactive intestinal polypeptide, enkephalins, somatostatin, gastrin/cholecystokinin, neurotensin and dopamine β‐hydroxylase. Neuroscience 5: 689–744, 1980.
 304. Schwartz, A., G. E. Lindenmayer, and J. C. Allen. The sodium‐potassium adenosine triphosphatase: pharmacological, physiological and biochemical aspects. Pharmacol. Rev. 27: 3–134, 1975.
 305. Schwartz, J.‐C., B. Malfroy, and S. De La Baume Biological inactivation of enkephalins and the role of enkephalin‐dipeptidyl‐carboxypeptidase (“enkephalinase”) as neuropeptidase. Life Sci. 29: 1715–1740, 1981.
 306. Seamon, K. B., and J. W. Daly. Forskolin: a unique diterpene activator of cyclic AMP‐generating systems. J. Cyclic Nucleotide Res. 7: 201–224, 1981.
 307. Seamon, K. B., and J. W. Daly. Forskolin, cyclic AMP and cellular physiology. Trends Pharmacol. Sci. 4: 120–123, 1983.
 308. Segawa, T., Y. Nakata, H. Yajima, and K. Kitagawa. Further observation on the lack of active uptake system for substance P in the central nervous system. Jpn. J. Pharmacol. 27: 573–580, 1977.
 309. Shain, W., and D. O. Carpenter. Mechanisms of synaptic modulation. Int. Rev. Neurobiol. 22: 205–250, 1981.
 310. Siegelbaum, S. A., and R. W. Tsien. Modulation of gated ion channels as a mode of transmitter action. Trends Neurosci. 6: 307–313, 1983.
 311. Silbergeld, E. K. Na+‐levels regulate Ca2+‐efflux from synaptosomal mitochondria. Biochem. Biophys. Res. Commun. 77: 464–469, 1977.
 312. Skou, J. C. Enzymatic basis for active transport of Na+ and K+ across cell membrane. Physiol. Rev. 45: 596–617, 1965.
 313. Sneddon, P., and D. P. Westfall. Pharmacological evidence that adenosine triphosphate and noradrenaline are co‐transmitters in the guinea‐pig vas deferens. J. Physiol. Lond. 347: 561–580, 1984.
 314. Snyder, S. H., H. I. Yamamura, C. B. Pert, W. J. Logan, and J. P. Bennet. Electrophysiology of intestinal smooth muscle. In: New Concepts in Neurotransmitter Regulation, edited by A. J. Mandell, New York: Plenum, 1973, p. 195–222.
 315. Sosa, R. P., A. T. McKnight, J. Hughes, and H. W. Kosterlitz. Incorporation of labelled amino acids into the enkephalins. FEBS Lett. 84: 195–198, 1977.
 316. Starke, K. Alpha sympathomimetic inhibition of adrenergic and cholinergic transmission in the rabbit heart. Naunyn‐Schmiedeberg's Arch. Pharmacol 274: 18–45, 1972.
 317. Starke, K. Regulation of noradrenaline release by presynaptic receptor systems. Rev. Physiol. Biochem. Pharmacol. 77: 1–124, 1977.
 318. Starke, K. Electrophysiology of intestinal smooth muscle. In: Chemical Neurotransmission 75 Years, edited by L. Stjärne, P. Hedqvist, H. Lagercrantz, and A. Wennmalm. New York: Academic, 1981, p. 189–200.
 319. Starke, K. Presynaptic receptors. Annu. Rev. Pharmacol. Toxicol. 21: 7–30, 1981.
 320. Starke, K., T. Endo, and H. D. Taube. Relative pre‐ and postsynaptic potencies of α‐adrenoceptor agonists in the rabbit pulmonary artery. Naunyn‐Schmiedeberg's Arch. Pharmacol. 291: 55–78, 1975.
 321. Steardo, L., M. Knight, C. A. Tamminga, P. Barone, A. M. Kask, and T. N. Chase. CCK26–33 degrading activity in brain and nonneural tissue: a metalloendopeptidase. J. Neurochem. 45: 784–790, 1985.
 322. Stjärne, L. Presynaptic alpha‐receptors do not depress the secretion of [3H]noradrenaline induced by veratridine. Acta Physiol. Scand. 106: 379–380, 1979.
 323. Stjärne, L. Electrophysiology of intestinal smooth muscle. In: Chemical Transmission 75 Years, edited by L. Stjärne, P. Hedqvist, H. Lagercrantz, and A. Wennmalm. New York: Academic, 1981, p. 257–284.
 324. Stjärne, L. Scope and mechanisms of control of stimulus‐secretion coupling in single varicosities of sympathetic nerves. Clin. Sci. 68, Suppl. 10: 77s–81s, 1985.
 325. Stjärne, L., P. Alberts, and T. Bartfai. Electrophysiology of intestinal smooth muscle. In: Catecholamines, Basic and Clinical Frontiers, edited by E. Usdin, I. J. Kopkin, and J. Barchas. New York: Pergamon, 1979, p. 292–297.
 326. Stoclet, J. C. Calmodulin An ubiquitous protein which regulates calcium‐dependent cellular functions and calcium movements. Biochem. Pharmacol. 30: 1723–1729, 1981.
 327. Stone, T. W. Physiological roles for adenosine and adenosine 5'‐triphosphate in the nervous system. Neuroscience 6: 523–555, 1981.
 328. Sundler, F., E. Moghimzadeh, R. Håkanson, M. Ekelund, and P. Emson. Nerve fibers in the gut and pancreas of the rat displaying neuropeptide‐Y immunoreactivity. Cell Tissue Res. 230: 487–493, 1983.
 329. Suszkiw, J. B., and M. E. O'Leary. Differential labeling of depot and active acetylcholine pools in nondepolarized and potassium‐depolarized rat brain synaptosomes. J. Neurochem. 38: 1668–1675, 1982.
 330. Szentagothai, J. Electrophysiology of intestinal smooth muscle. In: Structure and Function of Inhibitory Neuronal Mechanisms, edited by C. von Euler, S. Skoglund, and U. Soderberg. Oxford, UK: Pergamon, 1968, p. 15–31.
 331. Szerb, J. C. Endogenous acetylcholine release and labelled acetylcholine formation from [3H]choline in the myenteric plexus of the guinea‐pig ileum. Can. J. Physiol. Pharmacol. 53: 566–574, 1975.
 332. Szerb, J. C. Storage and release of labelled acetylcholine in the myenteric plexus of the guinea‐pig ileum. Can. J. Physiol. Pharmacol. 54: 12–22, 1976.
 333. Szerb, J. C. Correlation between acetylcholine release and neuronal activity in the guinea‐pig ileum myenteric plexus; effect of morphine. Neuroscience 7: 327–340, 1982.
 334. Takagi, K., and I. Takayanagi. Effect of N6, 2'‐O‐dibutyryl 3',5'‐cyclic adenosine monophosphate and adenosine triphosphate on acetylcholine output from cholinergic nerves in guinea‐pig ileum. Jpn. J. Pharmacol. 22: 33–36, 1972.
 335. Tanaka, C., and K. Taniyama. Substance P provoked γ‐aminobutyric acid release from the myenteric plexus of the guinea‐pig small intestine. J. Physiol. Lond. 362: 319–329, 1985.
 336. Taniyama, K., M. Kusunoki, N. Saito, and C. Tanaka. Release of γ‐aminobutyric acid from cat colon. Science Wash. DC 217: 1038–1040, 1982.
 337. Taniyama, K., M. Kusunoki, N. Saito, and C. Tanaka. GABA evoked ACh release from isolated guinea pig ileum. Life Sci. 32: 2349–2353, 1983.
 338. Taniyama, K., Y. Miki, M. Kusunoki, N. Saito, and C. Tanaka. Release of endogenous and labeled GABA from isolated guinea pig ileum. Am. J. Physiol. 245 (Gastrointest. Liver Physiol. 8): G717–G721, 1983.
 339. Tatemoto, K., M. Carlquist, T. J. McDonald, and V. Mutt. Isolation of a brain peptide identical to the intestinal PHI (peptide HI). FEBS Lett. 153: 248–252, 1983.
 340. Tatemoto, K., and V. Mutt. Isolation of two novel candidate hormones using a chemical method for finding naturally occurring polypeptides. Nature Lond. 285: 417–419, 1980.
 341. Tatemoto, K., and V. Mutt. Isolation and characterization of the intestinal peptide porcine PHI, a new member of the glucagon/secretin family. Proc. Natl. Acad. Sci. USA 78: 6603–6607, 1981.
 342. Tatemoto, K., A. Rokaeus, H. Jornvall, T. J. McDonald, and V. Mutt. Galanin—a novel biologically active peptide from porcine intestine. FEBS Lett. 164: 124–128, 1983.
 343. Tatemoto, K., S. Siimesmaa, H. Jornvall, J. M. Polak, S. R. Bloom, and V. Mutt. Isolation and characterization of neuropeptide Y from porcine intestine. FEBS Lett. 179: 181–184, 1985.
 344. Tauc, L. Nonvesicular release of neurotransmitter. Physiol. Rev. 62: 857–893, 1982.
 345. Teitelbaum, D. H., T. M. O'Dorisio, W. E. Perkins, and T. S. Gaginella. Somatostatin modulation of peptide‐induced acetylcholine release in guinea pig ileum. Am. J. Physiol. 246 (Gastrointest. Liver Physiol. 9): G509–G514, 1984.
 346. Tomita, T., and H. Watanabe. A comparison of the effects of ATP with noradrenaline and with the inhibitory potential of the guinea‐pig taenia coli. J. Physiol. Lond. 231: 167–177, 1973.
 347. Turner, A. J., R. Matsas, and A. J. Kenny. Are there neuropeptide‐specific peptidases? Biochem. Pharmacol. 34: 1347–1356, 1985.
 348. Uddman, R., E. Ekblad, L. Edvinsson, R. Håkanson, and F. Sundler. Neuropeptide Y‐like immunoreactivity in perivascular nerve fibres of the guinea‐pig. Regul. Pept. 10: 243–257, 1985.
 349. Uvnas‐Wallensten, K. Release of substance P‐like immunoreactivity into the antral lumen of cats. Acta Physiol. Scand. 104: 464–468, 1978.
 350. Vincent, S. R., C.‐J. Dalsgaard, M. Schultzberg, T. Hokfelt, I. Christensson, and L. Terenius. Dynorphin‐immunoreactive neurons in the autonomic nervous system. Neuroscience 11: 973–987, 1984.
 351. Vizi, E. S. Interaction between adrenergic and cholinergic systems: presynaptic inhibitory effect of noradrenaline on acetylcholine release. J. Neural Transm. Suppl. 11: 61–78, 1974.
 352. Vizi, E. S. Electrophysiology of intestinal smooth muscle. In: Cholinergic Mechanisms, edited by P. G. Waser. New York: Raven, 1975, p. 199–211.
 353. Vizi, E. S. Presynaptic modulation of neurochemical transmission. Prog. Neurobiol. Oxf. 12: 181–290, 1979.
 354. Vizi, E. S. Electrophysiology of intestinal smooth muscle. In: Cholinergic Mechanisms: Phylogenetic Aspects, Central and Peripheral Synapses, and Clinical Significance, edited by G. Pepeu and H. Ladinsky. New York: Plenum, 1981, p. 187–195.
 355. Vizi, E. S. Non‐Synaptic Interactions Between Neurons: Modulation of Neurochemical Transmission, Pharmacological and Clinical Agents. New York: Wiley, 1984.
 356. Vizi, E. S., M. D. Bertaccini, M. Impicciatorre, and J. Knoll. Evidence that acetylcholine released by gastrin and related polypeptides contributes to their effect on gastrointestinal motility. Gastroenterology 64: 268–277, 1973.
 357. Vizi, E. S., and J. Knoll. The effects of sympathetic nerve stimulation and guanethidine on parasympathetic neuroeffector transmission: the inhibition of acetylcholine release. J. Pharm. Pharmacol. 23: 918–925, 1971.
 358. Vizi, E. S., and J. Knoll. The inhibitory effect of adenosine and related nucleotides on the release of acetylcholine. Neuroscience 1: 391–398, 1976.
 359. Vizi, E. S., K. Ono, V. Adam‐Vizi, D. Duncalf, and F. F. Foldes. Presynaptic inhibitory effect of met‐enkephalin on [14C]acetylcholine release from the myenteric plexus and its interaction with muscarinic negative feedback inhibition. J. Pharmacol. Exp. Ther. 230: 493–499, 1984.
 360. Wallis, D. Neuronal 5‐hydroxytryptamine receptors outside the central nervous system. Life Sci. 29: 2345–2355, 1981.
 361. Waterfield, A. A., and H. W. Kosterlitz. Release of acetylcholine from the myenteric plexus of the guinea‐pig ileum. In: Proceedings of the Fourth International Symposium on Gastrointestinal Motility, edited by E. E. Daniel. Vancouver, Canada: Mitchell, 1974, p. 659–666.
 362. Waterfield, A. A., R. W. J. Smokcum, J. Hughes, H. W. Kosterlitz, and G. Henderson. In vitro pharmacology of the opioid peptides, enkephalins and endorphins. Eur. J. Pharmacol. 43: 107–116, 1977.
 363. Weight, F. F. Electrophysiology of intestinal smooth muscle. In: Neuroscience Third Study Program, edited by F. O. Schmitt and F. G. Worden. Cambridge, MA: MIT Press, 1974, p. 929–941.
 364. Weiler, M. H., C. B. Gundersen, and D. J. Jenden. Choline uptake and acetylcholine synthesis in synaptosomes: investigations using two different labeled variants of choline. J. Neurochem. 36: 1802–1812, 1981.
 365. Westfall, T. C. Local regulation of adrenergic neurotransmission. Physiol. Rev. 57: 659–728, 1977.
 366. White, T. D. Release of ATP from isolated myenteric varicosities by nicotinic agonists. Eur. J. Pharmacol. 79: 333–334, 1982.
 367. White, T. D., and M. Al‐Humayyd. Acetylcholine releases ATP from varicosities isolated from guinea pig myenteric plexus. J. Neurochem. 40: 1069–1075, 1983.
 368. White, T. D., and R. A. Leslie. Depolarization‐induced release of adenosine 5'‐triphosphate from isolated varicosities derived from the myenteric plexus of the guinea pig small intestine. J. Neurosci. 2: 206–215, 1982.
 369. White, J. D., K. D. Stewart, J. E. Krause, and J. F. McKelvy. Biochemistry of peptide‐secreting neurons. Physiol. Rev. 65: 553–606, 1985.
 370. Whittaker, V. P. Electrophysiology of intestinal smooth muscle. In: Methods of Neurochemistry, edited by R. Fried. New York: Dekker, 1972, vol. 2, p. 1–52.
 371. Wikberg, J. Release of [3H]acetylcholine from isolated guinea‐pig ileum. A radiochemical method for studying the release of the cholinergic neurotransmitter in the intestine. Acta Physiol. Scand. 101: 302–317, 1977.
 372. Wikberg, J. Differentiation between pre‐ and postjunctional α‐receptors in guinea pig ileum and rabbit aorta. Acta Physiol. Scand. 103: 225–239, 1978.
 373. Wikberg, J. E. S. The pharmacological classification of adrenergic α1 and α2 receptors and their mechanisms of action. Acta Physiol. Scand. Suppl. 468: 1–99, 1979.
 374. Wikberg, J. E. S., and R. J. Lefkowitz. Alpha2 adrenergic receptors are located prejunctionally in the Auerbach's plexus of the guinea pig small intestine: direct demonstration by radioligand binding. Life Sci. 31: 2899–2905, 1982.
 375. Williams, J. T., and R. A. North. Inhibition of firing of myenteric neurones by somatostatin. Brain Res. 155: 165–168, 1978.
 376. Williams, J. T., and R. A. North. Effects of endorphins on single myenteric neurons. Brain Res. 165: 57–65, 1979.
 377. Wood, J. D. Intracellular study of effects of morphine on electrical activity of myenteric neurons in cat small intestine. Gastroenterology 79: 1222–1230, 1980.
 378. Wood, J. D. Electrophysiology of intestinal smooth muscle. In: Autonomic Ganglia, edited by L.‐G. Elfvin. New York: Wiley, 1983, p. 367–398.
 379. Wood, J. D. Enteric neurophysiology. Am. J. Physiol. 247 (Gastrointest. Liver Physiol. 10): G585–G598, 1984.
 380. Wood, J. D., and C. J. Mayer. Serotonergic activation of tonic‐type enteric neurons in guinea pig small bowel. J. Neurophysiol. 42: 582–593, 1979.
 381. Wu, Z.‐A. C., and T. S. Gaginella. Functional properties of noradrenergic nervous system in rat colonic mucosa: uptake of [3H]norepinephrine. Am. J. Physiol. 241 (Gastrointest. Liver Physiol. 4): G137–G142, 1981.
 382. Yagasaki, O., H. Funaki, and I. Yanagiya. Contribution of endogenous prostaglandins to excitation of the myenteric plexus of guinea‐pig ileum: are adrenergic factors involved. Eur. J. Pharmacol. 103: 1–8, 1984.
 383. Yamaguchi, T. Effects of 5‐hydroxytryptamine on isolated strips of the guinea‐pig stomach. Br. J. Pharmacol. 44: 100–108, 1972.
 384. Yau, W. M. Electrophysiology of intestinal smooth muscle. In: Handbook of Endocrinology, edited by G. H. Gass and H. M. Kaplan. Boca Raton, FL: CRC, 1987, vol. II, pt. A, p. 93–105.
 385. Yau, W. M., J. A. Dorsett, and M. L. Youther. Evidence for cyclic AMP as the physiologic mediator for acetylcholine release from myenteric plexus (Abstract). Dig. Dis. Sci. 30: 801, 1985.
 386. Yau, W. M., J. A. Dorsett, and M. L. Youther. Inhibitory peptidergic neurons: functional difference between somatostatin and enkephalin in myenteric plexus. Am. J. Physiol. 250 (Gastrointest. Liver Physiol. 13): G60–G63, 1986.
 387. Yau, W. M., J. A. Dorsett, and M. L. Youther. Calcium‐dependent stimulation of acetylcholine release by substance P and vasoactive intestinal polypeptide. Eur. J. Pharmacol. 120: 241–243, 1986.
 388. Yau, W. M., J. A. Dorsett, and M. L. Youther. Bradykinin releases acetylcholine from myenteric plexus by a prostaglan‐din‐mediated mechanism. Peptides 7: 289–292, 1986.
 389. Yau, W. M., P. F. Lingle, and M. L. Youther. Modulation of cholinergic neurotransmitter release from myenteric plexus by somatostatin. Peptides 4: 49–53, 1983.
 390. Yau, W. M., P. F. Lingle, and M. L. Youther. Interaction of enkephalin and caerulein on guinea pig small intestine. Am. J. Physiol. 244 (Gastrointest. Liver Physiol. 7): G65–G70, 1983.
 391. Yau, W. M., G. M. Makhlouf, L. E. Edwards, and J. T. Farrar. The action of cholecystokinin and related peptides on guinea pig small intestine. Can. J. Physiol. Pharmacol. 52: 298–303, 1974.
 392. Yau, W. M., and P. R. Verdun. Release of γ‐aminobutyric acid from guinea pig myenteric plexus synaptosomes. Brain Res. 278: 271–273, 1983.
 393. Yau, W. M., P. R. Verdun, and M. L. Youther. Neurotensin: a modulator of enteric cholinergic neurons in the guinea pig small intestine. Eur. J. Pharmacol. 95: 253–258, 1983.
 394. Yau, W. M., and M. L. Youther. Direct evidence for a release of acetylcholine from the myenteric plexus of guinea‐pig small intestine by substance P. Eur. J. Pharmacol. 81: 665–668, 1982.
 395. Yau, W. M., and M. L. Youther. Substance K: a stimulant of myenteric cholinergic neurons in the small intestine (Abstract). Gastroenterology 88: 1638, 1985.
 396. Yau, W. M., M. L. Youther, and P. R. Verdun. A presynaptic site of action of substance P and vasoactive intestinal polypeptide on myenteric neurons. Brain Res. 330: 382–385, 1985.
 397. Zafirov, D. H., J. M. Palmer, P. R. Nemeth, and J. D. Wood. Bombesin, gastrin releasing peptide and vasoactive intestinal peptide excite myenteric neurons. Eur. J. Pharmacol. 115: 103–107, 1985.
 398. Zavecz, J. H., and T. O. Yellin. Histamine receptors in the myenteric plexus‐longitudinal muscle of the guinea‐pig ileum: H1‐and H2‐receptor‐mediated potentiation of the contractile response to electrical stimulation. J. Pharmacol. Exp. Ther. 223: 177–182, 1982.
 399. Zimmermann, H. Vesicle recycling and transmitter release. Neuroscience 4: 1773–1804, 1979.
 400. Zimmermann, H., and C. R. Denston. Recycling of synaptic vesicles in the cholinergic synapses of the Torpedo electric organ during induced transmitter release. Neuroscience 2: 695–714, 1977.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Neurotransmitter release in the enteric nervous system
 

How to Cite

William M. Yau. Neurotransmitter release in the enteric nervous system. Compr Physiol 2011, Supplement 16: Handbook of Physiology, The Gastrointestinal System, Motility and Circulation: 403-433. First published in print 1989. doi: 10.1002/cphy.cp060112