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. 1993 Feb;461:387–402. doi: 10.1113/jphysiol.1993.sp019519

Noradrenaline as a presynaptic inhibitory neurotransmitter in ganglia of the guinea-pig gall-bladder.

G M Mawe 1
PMCID: PMC1175263  PMID: 8102400

Abstract

1. The effects of noradrenaline on guinea-pig gall-bladder ganglia were investigated with intracellular recording techniques. 2. Noradrenaline (0.01-100 microM) decreased the amplitude of the fast excitatory postsynaptic potential (EPSP) that was evoked by stimulation of interganglionic fibre tracts. High concentrations of noradrenaline (10-100 microM) caused an inhibition ranging from 93-100%. The noradrenaline concentration that resulted in half-maximal inhibition (EC50) of the EPSP was 280 nM. 3. Experiments with selective agonists and antagonists indicated that the alpha 2-adrenoreceptor was involved in the inhibition of the EPSP. Clonidine (0.001-100 microM) reduced the EPSP in a concentration-dependent manner with an EC50 of 30 nM. Yohimbine (100-300 nM) caused a rightward shift of the noradrenaline concentration-effect relationship, with a dissociation equilibrium constant of 1.4 nM. 4. Release of endogenous catecholamines by tyramine (100 microM) in the presence of desipramine (1.0 microM), caused a yohimbine-sensitive decrease in the amplitude of the EPSP. Treatment with tyramine did not affect the amplitude of the EPSP in tissue that had undergone prior chemical sympathectomy with 6-hydroxydopamine. 5. Electrical stimulation of the vascular plexus (1-3 s; 10-20 Hz; 10 mA) decreased the amplitude of the EPSP. In some cases suprathreshold responses were reduced to subthreshold EPSPs following stimulation of the vascular plexus. Yohimbine (300 nM) reversibly inhibited the effects of vascular plexus stimulation. 6. Noradrenaline did not modify the responses of gall-bladder neurones to exogenously applied acetylcholine. Also, application of noradrenaline, by superfusion (0.001-100 microM) or by pressure microejection (1.0 mM), had no effect on the resting membrane potential, membrane conductance, or action potential characteristics of gall-bladder neurones. 7. Immunoreactivity for type A monoamine oxidase (MAO-A) was found in the vascular plexus and the ganglionated plexus of the gall-bladder. 8. These results show that noradrenaline has an alpha 2-adrenoreceptor-mediated presynaptic inhibitory effect on fast synaptic transmission in the ganglia of the guinea-pig gall-bladder. It is proposed that vagal terminals may be an important target of this adrenergic inhibitory input to the gall-bladder.

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Selected References

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  1. Bauer A. J., Hanani M., Muir T. C., Szurszewski J. H. Intracellular recordings from gallbladder ganglia of opossums. Am J Physiol. 1991 Feb;260(2 Pt 1):G299–G306. doi: 10.1152/ajpgi.1991.260.2.G299. [DOI] [PubMed] [Google Scholar]
  2. Baumgarten H. G., Lange W. Extrinsic adrenergic innervation of the extrahepatic biliary duct system in guinea-pigs, cats and rhesus monkeys. Z Zellforsch Mikrosk Anat. 1969 Sep 22;100(4):606–615. doi: 10.1007/BF00344379. [DOI] [PubMed] [Google Scholar]
  3. Cai W. Q., Gabella G. Catecholamine-containing cells in the nerve plexus of the guinea pig gallbladder. Acta Anat (Basel) 1984;119(1):10–17. doi: 10.1159/000145856. [DOI] [PubMed] [Google Scholar]
  4. Cornbrooks E. B., Pouliot W. A., Mawe G. M. Structure of neurons and ganglia of the guinea pig gallbladder: light and electron microscopic studies. J Comp Neurol. 1992 Mar 1;317(1):31–44. doi: 10.1002/cne.903170103. [DOI] [PubMed] [Google Scholar]
  5. Dahlstrand C., Dahlström A., Ahlman H. Adrenergic and VIP-ergic relaxatory mechanisms of the feline extrahepatic biliary tree. J Auton Nerv Syst. 1989 Mar;26(2):97–106. doi: 10.1016/0165-1838(89)90157-4. [DOI] [PubMed] [Google Scholar]
  6. Doggrell S. A., Scott G. W. The occurrence of postsynaptic alpha- and beta-adrenoceptors in the guinea-pig gall bladder. Br J Pharmacol. 1980;71(1):185–189. doi: 10.1111/j.1476-5381.1980.tb10924.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hanyu N., Dodds W. J., Layman R. D., Hogan W. J., Chey W. Y., Takahashi I. Mechanism of cholecystokinin-induced contraction of the opossum gallbladder. Gastroenterology. 1990 May;98(5 Pt 1):1299–1306. doi: 10.1016/0016-5085(90)90348-5. [DOI] [PubMed] [Google Scholar]
  8. Hirst G. D., McKirdy H. C. Presynaptic inhibition at mammalian peripheral synapse? Nature. 1974 Aug 2;250(465):430–431. doi: 10.1038/250430a0. [DOI] [PubMed] [Google Scholar]
  9. Hirst G. D., Silinsky E. M. Some effects of 5-hydroxytryptamine, dopamine and noradrenaline on neurones in the submucous plexus of guinea-pig small intestine. J Physiol. 1975 Oct;251(3):817–832. doi: 10.1113/jphysiol.1975.sp011124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kirchgessner A. L., Pintar J. E. Guinea pig pancreatic ganglia: projections, transmitter content, and the type-specific localization of monoamine oxidase. J Comp Neurol. 1991 Mar 22;305(4):613–631. doi: 10.1002/cne.903050407. [DOI] [PubMed] [Google Scholar]
  11. Mawe G. M., Gershon M. D. Structure, afferent innervation, and transmitter content of ganglia of the guinea pig gallbladder: relationship to the enteric nervous system. J Comp Neurol. 1989 May 15;283(3):374–390. doi: 10.1002/cne.902830306. [DOI] [PubMed] [Google Scholar]
  12. Mawe G. M. Intracellular recording from neurones of the guinea-pig gall-bladder. J Physiol. 1990 Oct;429:323–338. doi: 10.1113/jphysiol.1990.sp018259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mawe G. M. The role of cholecystokinin in ganglionic transmission in the guinea-pig gall-bladder. J Physiol. 1991 Aug;439:89–102. doi: 10.1113/jphysiol.1991.sp018658. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nakamura T., Yoshimura M., Shinnick-Gallagher P., Gallagher J. P., Akasu T. alpha 2 and alpha 1-Adrenoceptors mediate opposing actions on parasympathetic neurons. Brain Res. 1984 Dec 10;323(2):349–353. doi: 10.1016/0006-8993(84)90312-3. [DOI] [PubMed] [Google Scholar]
  15. Nishi S., North R. A. Intracellular recording from the myenteric plexus of the guinea-pig ileum. J Physiol. 1973 Jun;231(3):471–491. doi: 10.1113/jphysiol.1973.sp010244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. North R. A., Surprenant A. Inhibitory synaptic potentials resulting from alpha 2-adrenoceptor activation in guinea-pig submucous plexus neurones. J Physiol. 1985 Jan;358:17–33. doi: 10.1113/jphysiol.1985.sp015537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. PALLIN B., SKOGLUND S. NEURAL AND HUMORAL CONTROL OF THE GALLBLADDER-EMPTYING MECHANISM IN THE CAT. Acta Physiol Scand. 1964 Apr;60:358–362. doi: 10.1111/j.1748-1716.1964.tb02898.x. [DOI] [PubMed] [Google Scholar]
  18. Persson C. G. Adrenergic, cholecystokinetic and morphine-induced effects on extra-hepatic biliary motility. Acta Physiol Scand Suppl. 1972;383:1–32. [PubMed] [Google Scholar]
  19. Persson C. G. Dual effects on the sphincter of Oddi and gallbladder induced by stimulation of the right great splanchnic nerve. Acta Physiol Scand. 1973 Mar;87(3):334–343. doi: 10.1111/j.1748-1716.1973.tb05397.x. [DOI] [PubMed] [Google Scholar]
  20. Schemann M. Excitatory and inhibitory effects of norepinephrine on myenteric neurons of the guinea-pig gastric corpus. Pflugers Arch. 1991 Jul;418(6):575–580. doi: 10.1007/BF00370574. [DOI] [PubMed] [Google Scholar]
  21. Shen K. Z., Surprenant A. Mechanisms underlying presynaptic inhibition through alpha 2-adrenoceptors in guinea-pig submucosal neurones. J Physiol. 1990 Dec;431:609–628. doi: 10.1113/jphysiol.1990.sp018350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Surprenant A., Shen K. Z., North R. A., Tatsumi H. Inhibition of calcium currents by noradrenaline, somatostatin and opioids in guinea-pig submucosal neurones. J Physiol. 1990 Dec;431:585–608. doi: 10.1113/jphysiol.1990.sp018349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Talmage E. K., Pouliot W. A., Cornbrooks E. B., Mawe G. M. Transmitter diversity in ganglion cells of the guinea pig gallbladder: an immunohistochemical study. J Comp Neurol. 1992 Mar 1;317(1):45–56. doi: 10.1002/cne.903170104. [DOI] [PubMed] [Google Scholar]
  24. Wood J. D., Mayer C. J. Adrenergic inhibition of serotonin release from neurons in guinea pig Auerback's plexus. J Neurophysiol. 1979 Mar;42(2):594–603. doi: 10.1152/jn.1979.42.2.594. [DOI] [PubMed] [Google Scholar]
  25. Yamasato T., Nakayama S. Participation of the parasympathetic and sympathetic nerves in regulation of gallbladder motility in the dog. Acta Med Okayama. 1990 Apr;44(2):79–86. doi: 10.18926/AMO/30441. [DOI] [PubMed] [Google Scholar]
  26. de Groat W. C., Booth A. M. Inhibition and facilitation in parasympathetic ganglia of the urinary bladder. Fed Proc. 1980 Oct;39(12):2990–2996. [PubMed] [Google Scholar]

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