Skip to main content
Log in

Charybdotoxin and iberiotoxin but not apamin abolish the slow after-hyperpolarization in myenteric plexus neurons

  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

Myenteric neurons of guinea-pig ileum were studied with intracellular microelectrodes. The specific toxins charybdotoxin, iberiotoxin and apamin were used to characterize the prolonged after-hyperpolarizations of AH neurons in this preparation. Charybdotoxin and iberiotoxin blocked prolonged after-hyperpolarizations in 23 of 24 AH neurons, but apamin had no effect on 5 of 5 AH neurons. Abolition of the after-hyperpolarizations was accompanied by depolarization and increases in input resistances of those AH neurons affected, but the shapes of action potentials were unchanged. The excitability of the AH neurons was enhanced as shown by an increase in the number of action potentials evoked by a 500-ms depolarizing current pulse or by a train of 15 ms depolarizing current pulses (10Hz). The other class of myenteric neurons, S neurons, was also investigated. The 19 S neurons studied fired action potentials only at the start of a 500 ms depolarization, but the toxins had no effect on this behaviour or on their other properties. Intracellular injection of Neurobiotin into the neurons studied and subsequent immunohistochemical staining to localise the calcium-binding protein, calretinin, indicated that all major classes of S neurons were included in the sample. Thus, the prolonged after-hyperpolarizations in AH neurons may be due to opening of a large-conductance (BK) calcium-dependent potassium channel, but similar channels play little or no role in regulation of the excitability of S neurons.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Blatz AL, Magleby KL (1987) Calcium-activated potassium channels. Trends Neurosci 10:463–467

    Google Scholar 

  2. Bornstein JC, Furness JB, Smith TK, Trussell DC (1991) Synaptic responses evoked by mechanical stimulation of the mucosa in morphologically characterized myenteric neurons of the guinea pig ileum. J Neurosci 11:505–518

    Google Scholar 

  3. Bornstein JC, Hendriks R, Furness JB, Trussell DC (1991) Ramifications of the axons of AH-neurons injected with the intracellular marker biocytin in the myenteric plexus of the guinea pig small intestine. J Comp Neurol 314:437–451

    Google Scholar 

  4. Bornstein JC, Furness JB, Kunze WAA (1994) Electrophysiological characterization of myenteric neurons, how do classifications schemes relate? J Auton Nerv Syst (in press)

  5. Brewster BS, Strong PN (1992) Naturally-occuring potassium channel blockers. In: Weston AH, Hamilton TC (eds) Potassium channel modulators. Blackwell, Oxford, pp 272–304

    Google Scholar 

  6. Brookes SJH, Steele PA, Costa M (1991) Calretinin immunoreactivity in cholinergic motor neurones, interneurones and vasomotor neurones in the guinea-pig small intestine. Cell Tissue Res 263:471–481

    Google Scholar 

  7. Castle NA, Haylett DG, Jenkinson DH (1989) Toxins in the characterization of potassium channels. Trends Neurosci 12:59–65

    Google Scholar 

  8. Furness JB, Bornstein JC (1991) The enteric nervous system and its extrinsic connections. In: Yamada T (ed) Textbook of gastroenterology. Lippincott, Philadelphia, pp 2–24

    Google Scholar 

  9. Furness JB, Costa M (1987) The enteric nervous system. Churchill Livingstone, Edinburgh London Melbourne New York

    Google Scholar 

  10. Furness JB, Bornstein JC, Trussell DC (1988) Shapes of nerve cells in the myenteric plexus of the guinea-pig small intestine revealed by the intracellular injection of dye. Cell Tissue Res 254:561–571

    Google Scholar 

  11. Galligan JJ, North RA, Tokimasa T (1989) Muscarinic agonists and potassium currents in guinea-pig myenteric neurones. Br J Pharmacol 96:193–203

    Google Scholar 

  12. Garcia ML, Kaczorowski GJ (1992) High conductance calcium-activated potassium channels: molecular pharmacology, purification and regulation. In: Weston AH, Hamilton TC (eds) Potassium channel modulators. Blackwell, Oxford, pp 76–109

    Google Scholar 

  13. Grafe P, Mayer CJ, Wood JD (1980) Synaptic modulation of calciumdependent potassium conductance in myenteric neurones in the guinea-pig. J Physiol (Lond) 305:235–248

    Google Scholar 

  14. Harvey AL, Anderson AJ, Rowan EG (1993) Toxins affecting ion channels. In: Harvey AL (ed) Natural and synthetic neurotoxins. Academic Press, London, pp 129–185

    Google Scholar 

  15. Hill R, Matsushima T, Schotland J, Grillner S (1992) Apamin blocks the slow AHP in lamprey and delays termination of locomotor bursts. NeuroRep 3:943–945

    Google Scholar 

  16. Hirst GDS, Holman ME, Spence I (1974) Two types of neurones in the myenteric plexus of duodenum in the guinea-pig. J Physiol (Lond) 236:303–326

    Google Scholar 

  17. Hirst GDS, Johnson SM, Helden DF van (1985) The slow calciumdependent potassium current in a myenteric neurone of the guinea-pig ileum. J Physiol (Lond) 361:315–337

    Google Scholar 

  18. Hirst GDS, Johnson SM, Helden DF van (1985) The calcium current in a myenteric neurone of the guinea-pig ileum. J Physiol (Lond) 361:297–314

    Google Scholar 

  19. Iyer V, Bornstein JC, Costa M, Furness JB, Takahashi Y, Iwanaga T (1988) Electrophysiology of guinea-pig myenteric neurons correlated with immunoreactivity for calcium binding proteins. J Auton Nerv Syst 22:141–150

    Google Scholar 

  20. Kunze WAA, Furness JB, Bornstein JC (1993) Simultaneous intracellular recordings from enteric neurons reveals that myenteric AH neurons transmit via slow excitatory post-synaptic potentials. Neuroscience 55:685–694

    Google Scholar 

  21. Mawe GM (1990) Intracellular recording from neurons of the guinea-pig gall bladder. J Physiol (Lond) 429:323–338

    Google Scholar 

  22. Messenger JP, Bornstein JC, Furness JB (1994) Electrophysiological and morphological classification of myenteric neurons in the proximal colon of the guinea-pig. Neuroscience (in press)

  23. Meves H (1992) Potassium channel toxins. In: Herken H, Hucho F (eds) Selective neurotoxicity. Springer, Berlin Heidelberg-New York, pp 739–774

    Google Scholar 

  24. Miles R, Wong RKS (1986) Excitatory synaptic interactions between CA3 neurones in the guineapi g hippocampus. J Physiol (Lond) 373:397–418

    Google Scholar 

  25. Moczydlowski E, Lucchesi K, Ravindran A (1988) An emerging pharmacology of peptide toxins targeted against potassium channels. J Membr Biol 105:95–111

    Google Scholar 

  26. Morita K, Katayama Y (1992) Substance P inhibits activation of calciumdependent potassium conductances in guinea-pig myenteric neurones. J Physiol (Lond) 447:293–308

    Google Scholar 

  27. Morita K, North RA, Tokimasa T (1982) The calcium-activated potassium conductance in guinea-pig myenteric neurones. J Physiol (Lond) 329:341–354

    Google Scholar 

  28. North RA, Nishi S (1974) Properties of the ganglion cells of the myenteric plexus of the guinea-pig ileum determined by intracellular recording. In: Daniel EE (ed) Proceedings of the 4th International Symposium on Gastrointestinal Motility. Mitchell Press, Vancouver, pp 667–676

    Google Scholar 

  29. North RA, Tokimasa T (1987) Persistent calcium-sensitive potassium current and the resting properties of guinea-pig myenteric neurones. J Physiol (Lond) 386:333–353

    Google Scholar 

  30. Pineda JC, Ggalarraga E, Bargas J, Cristancho M, Aceves J (1992) Charybdotoxin and apamin sensitivity of the calciumdependent repolarization and the afterhyperpolarization in neostriatal neurons. J Neurophysiol 68:287–294

    Google Scholar 

  31. Pompolo S, Furness JB (1988) Ultrastructure and synaptic relationships of calbindin reactive, Dogiel type II neurons, in myenteric ganglia of guinea-pig small intestine. J Neurocytol 17:771–782

    Google Scholar 

  32. Pompolo S, Furness JB (1993) Origins of synaptic inputs to calretinin immunoreactive neurons in the guinea-pig small intestine. J Neurocytol 22:531–546

    Google Scholar 

  33. Pompolo S, Furness JB, Bornstein JC, Hendriks R, Trussell DC (1989) Dogiel type II neurons in the guinea-pig small intestine: ultrastructure in relation to other characteristics. In: Singer MV, Goebell H (eds) Nerves in the gastrointestinal tract. Kluwer, Lancaster, pp 57–67

    Google Scholar 

  34. Rudy B (1988) Diversity and ubiquity of K channels. Neuroscience 25:729–749

    Google Scholar 

  35. Sah P, McLachlan EM (1992) Potassium currents contributing to action potential repolarization and the afterhyperpolarization in rat vagal motoneurons. J Neurophysiol 68:1834–1841

    Google Scholar 

  36. Smith TK, Bornstein JC, Furness JB (1992) Convergence of reflex pathways excited by distension and mechanically deforming the mucosa onto morphologically characterized myenteric neurons of the guinea-pig small intestine. J Neurosci 12:1502–1510

    Google Scholar 

  37. Song ZM, Brookes SJH, Costa M (1991) Identification of myenteric neurons which project to the mucosa of the guinea-pig small intestine. Neurosci Lett 129:294–298

    Google Scholar 

  38. Stach W (1989) A revised morphological classification of neurons in the enteric nervous system. In: Singer MV, Goebell H (eds) Nerves and the Gastrointestinal Tract. Kluwer, Lancaster, pp 29–45

    Google Scholar 

  39. Tamura K (1992) Morphology of electrophysiologically identified myenteric neurons in the guinea pig rectum. Am J Physiol 262: G545-G552

    Google Scholar 

  40. Wood JD (1989) Electrical and synaptic behavior of enteric neurons. In: Wood JD (ed) Handbook of physiology. Sect 6. The gastrointestinal system. vol I. Motility and circulation. American Physiological Society, Washington, DC, pp 465–517

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kunze, W.A.A., Bornstein, J.C., Furness, J.B. et al. Charybdotoxin and iberiotoxin but not apamin abolish the slow after-hyperpolarization in myenteric plexus neurons. Pflügers Arch. 428, 300–306 (1994). https://doi.org/10.1007/BF00724511

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00724511

Key words

Navigation