Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1992 Feb;447:49–66. doi: 10.1113/jphysiol.1992.sp018990

Electrical behaviour of myenteric neurones in the gastric antrum of the guinea-pig.

J F Tack 1, J D Wood 1
PMCID: PMC1176024  PMID: 1593455

Abstract

1. Intracellular microelectrodes were used to study the electrical behaviour of ganglion cells in the myenteric plexus of the antrum of the guinea-pig stomach. In the absence of any information on antral myenteric neurones, the aim was to characterize the electrical behaviour and identify biophysical properties of the neurones that could be related to specialized organization of the neural microcircuits in this physiologically important division of the stomach. 2. Myenteric neurones in the gastric antrum were classified into four subtypes based on electrophysiological properties. These were gastric I, II, III and AH/type 2 neurones. Gastric I neurones were characterized by repetitive spike discharge during intraneuronal injection of depolarizing current, by higher input resistances and by lower resting membrane potentials than the other cell types. Gastric II neurones did not discharge repetitively. They discharged one or two spikes only at the beginning of depolarizing current pulses. Gastric III neurones did not discharge action potentials in response to depolarizing pulses. These neurones had higher membrane potentials and lower input resistances than the other types. A fourth type of neurone discharged one or more spikes during depolarizing current pulses and had long-lasting hyperpolarizing after-potentials associated with the spikes. The behaviour of these neurones was like AH/type 2 neurones found elsewhere in the enteric nervous system. 3. Action potentials in gastric I and II neurones were abolished by tetrodotoxin. Spikes of the AH/type 2 cells were not abolished by tetrodotoxin due to a calcium component of the inward current. Application of tetraethylammonium broadened the spikes. This was reversed by removal of Ca2+ from the bathing medium. 4. The hyperpolarizing after-potentials of AH/type 2 neurones were suppressed by removal of Ca2+ from the bathing medium. Treatment with 4-aminopyridine decreased the amplitude and duration of the after-hyperpolarization, whereas tetraethylammonium increased the duration and amplitude of the after-potentials. The hyperpolarizing after-potentials were unaffected by apamin. 5. Elevation of cyclic 3',5'-adenosine monophosphate by forskolin resulted in excitation of all AH/type 2 neurones and some of the gastric III cells. Gastric I and II neurones were unaffected. 6. The electrophysiological behaviour of myenteric neurones in the antrum was similar in some respects and different in others from neurones in the gastric corpus and the small and large intestine of the same animal. The differences may reflect distinct organization of the microcircuits for the specialized neural control of the effector functions which characterize the gastric antrum.

Full text

PDF
62

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allescher H. D., Daniel E. E., Dent J., Fox J. E., Kostolanska F. Extrinsic and intrinsic neural control of pyloric sphincter pressure in the dog. J Physiol. 1988 Jul;401:17–38. doi: 10.1113/jphysiol.1988.sp017149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brookes S. J., Ewart W. R., Wingate D. L. Intracellular recordings from myenteric neurones in the human colon. J Physiol. 1987 Sep;390:305–318. doi: 10.1113/jphysiol.1987.sp016702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Deloof S., Rousseau J. P. Neural control of electrical gastric activity in response to inflation of the antrum in the rabbit. J Physiol. 1985 Oct;367:13–25. doi: 10.1113/jphysiol.1985.sp015811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Furukawa K., Taylor G. S., Bywater R. A. An intracellular study of myenteric neurons in the mouse colon. J Neurophysiol. 1986 Jun;55(6):1395–1406. doi: 10.1152/jn.1986.55.6.1395. [DOI] [PubMed] [Google Scholar]
  5. Gershon M. D., Erde S. M. The nervous system of the gut. Gastroenterology. 1981 Jun;80(6):1571–1594. [PubMed] [Google Scholar]
  6. Grafe P., Mayer C. J., Wood J. D. Synaptic modulation of calcium-dependent potassium conductance in myenteric neurones in the guinea-pig. J Physiol. 1980 Aug;305:235–248. doi: 10.1113/jphysiol.1980.sp013360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hirst G. D., Holman M. E., Spence I. Two types of neurones in the myenteric plexus of duodenum in the guinea-pig. J Physiol. 1974 Jan;236(2):303–326. doi: 10.1113/jphysiol.1974.sp010436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hirst G. D., Johnson S. M., van Helden D. F. The calcium current in a myenteric neurone of the guinea-pig ileum. J Physiol. 1985 Apr;361:297–314. doi: 10.1113/jphysiol.1985.sp015647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hirst G. D., Johnson S. M., van Helden D. F. The slow calcium-dependent potassium current in a myenteric neurone of the guinea-pig ileum. J Physiol. 1985 Apr;361:315–337. doi: 10.1113/jphysiol.1985.sp015648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hirst G. D., McKirdy H. C. Synaptic potentials recorded from neurones of the submucous plexus of guinea-pig small intestine. J Physiol. 1975 Jul;249(2):369–385. doi: 10.1113/jphysiol.1975.sp011020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hodgkiss J. P., Lees G. M. Correlated electrophysiological and morphological characteristics of myenteric plexus neurones [proceedings]. J Physiol. 1978 Dec;285:19P–20P. [PubMed] [Google Scholar]
  12. Hodgkiss J. P., Lees G. M. Morphological studies of electrophysiologically-identified myenteric plexus neurons of the guinea-pig ileum. Neuroscience. 1983 Mar;8(3):593–608. doi: 10.1016/0306-4522(83)90201-4. [DOI] [PubMed] [Google Scholar]
  13. Nemeth P. R., Palmer J. M., Wood J. D., Zafirov D. H. Effects of forskolin on electrical behaviour of myenteric neurones in guinea-pig small intestine. J Physiol. 1986 Jul;376:439–450. doi: 10.1113/jphysiol.1986.sp016162. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. North R. A. The calcium-dependent slow after-hyperpolarization in myenteric plexus neurones with tetrodotoxin-resistant action potentials. Br J Pharmacol. 1973 Dec;49(4):709–711. doi: 10.1111/j.1476-5381.1973.tb08550.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Palmer J. M., Wood J. D., Zafirov D. H. Elevation of adenosine 3',5'-phosphate mimics slow synaptic excitation in myenteric neurones of the guinea-pig. J Physiol. 1986 Jul;376:451–460. doi: 10.1113/jphysiol.1986.sp016163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Palmer J. M., Wood J. D., Zafirov D. H. Transduction of aminergic and peptidergic signals in enteric neurones of the guinea-pig. J Physiol. 1987 Jun;387:371–383. doi: 10.1113/jphysiol.1987.sp016578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Schemann M., Wood J. D. Electrical behaviour of myenteric neurones in the gastric corpus of the guinea-pig. J Physiol. 1989 Oct;417:501–518. doi: 10.1113/jphysiol.1989.sp017815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Schemann M., Wood J. D. Synaptic behaviour of myenteric neurones in the gastric corpus of the guinea-pig. J Physiol. 1989 Oct;417:519–535. doi: 10.1113/jphysiol.1989.sp017816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Seamon K. B., Padgett W., Daly J. W. Forskolin: unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3363–3367. doi: 10.1073/pnas.78.6.3363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Tack J. F., Wood J. D. Synaptic behaviour in the myenteric plexus of the guinea-pig gastric antrum. J Physiol. 1992 Jan;445:389–406. doi: 10.1113/jphysiol.1992.sp018930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tamura K., Wood J. D. Electrical and synaptic properties of myenteric plexus neurones in the terminal large intestine of the guinea-pig. J Physiol. 1989 Aug;415:275–298. doi: 10.1113/jphysiol.1989.sp017722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Wade P. R., Wood J. D. Electrical behavior of myenteric neurons in guinea pig distal colon. Am J Physiol. 1988 Apr;254(4 Pt 1):G522–G530. doi: 10.1152/ajpgi.1988.254.4.G522. [DOI] [PubMed] [Google Scholar]
  24. Wade P. R., Wood J. D. Synaptic behavior of myenteric neurons in guinea pig distal colon. Am J Physiol. 1988 Aug;255(2 Pt 1):G184–G190. doi: 10.1152/ajpgi.1988.255.2.G184. [DOI] [PubMed] [Google Scholar]
  25. Wood J. D., Mayer C. J. Intracellular study of electrical activity of Auerbach's plexus in guinea-pig small intestine. Pflugers Arch. 1978 May 31;374(3):265–275. doi: 10.1007/BF00585604. [DOI] [PubMed] [Google Scholar]
  26. Wood J. D. Neurophysiological theory of intestinal motility. Nihon Heikatsukin Gakkai Zasshi. 1987 Jun;23(3):143–186. [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES