Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Ionic dependence of electrical activity in small mesenteric arteries of guinea-pigs

  • 19 Accesses

  • 16 Citations

Abstract

The regulation of blood vessel diameter is under the control of the autonomic nervous system (as well as hormones and metabolites), sympathetic nerve stimulation evoking depolarizing post-synaptic potentials. Excitatory junction potentials (EJPs) were recorded from vascular smooth muscle cells of guinea-pig small mesenteric arteries (pressurized) following nerve stimulation. Repetitive stimulation (>5Hz) led to summation of EJPs, which evoked spikes and vasoconstriction. Replacing extracellular Na+ with choline (plus atropine) resulted in a decrease in EJP amplitude, but spike amplitude and maximum rate of rise (+Vmax) were unaffected. Decreasing the extracellular Ca2+ concentration produced decreases in EJP amplitude and spike +Vmax, while increasing extracellular Ca2+ resulted in increased EJP amplitude and spike +Vmax. Verapamil and bepridil, agents that depress Ca2+ influx in vascular and visceral smooth muscle, depolarized the membrane and depressed EJPs and spikes at high concentrations (10−5 M and 5×10−6 M, respectively). The data indicate that EJPs are dependent on external Na+ and Ca2+ ions, and that spikes are dependent on Ca2+. Thus, neuromuscular transmission in this muscle is similar to that in non-vascular smooth muscles, such as intestinal muscle and vas deferens.

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

References

  1. Belardinelli L, Harder D, Sperelakis N, Rubio R, Berne RM (1979) Cardiac glycoside stimulation of inward Ca++ current in vascular smooth muscle of canine coronary artery. J Pharmacol Exp Ther 209:62–66

  2. Blaustein MP, Hodgkin AL (1969) The effect of cyanide on the efflux of calcium from squid axons. J Physiol 200:497–527

  3. Bülbring E, Tomita T (1968) The effects of Ba++ and Mn++ on the smooth muscle of guinea-pig taenia coli. J Physiol 196:137–139

  4. Burnstock G (1979) Autonomic innervation and transmission. Br Med Bull 35:255–262

  5. Burnstock G (1980) Cholinergic and purinergic regulation of blood vessels. In: Bohr DF, Somlyo AD, Sparks HW, Geiger SR (eds) Handbook of physiology, section 2: The cardiovascular system. Vol II, Vascular smooth muscle. American Physiological Society. Waverly Press, Baltimore, pp 567–617

  6. Casteels R, Kitamura K, Kuriyama H, Suzuki H (1977) Excitation-contraction coupling in the smooth muscle cells of the rabbit main pulmonary artery. J Physiol 271:63–79

  7. Devine CE (1978) Vascular smooth muscle morphology and ultrastructure. In: Kaley G, Altura BM (eds) Microcirculation, Vol II. University Park Press, Baltimore, Md. pp 3–39

  8. Droogmans G, Raeymaekers L, Casteels R (1977) Electro- and pharmacomechanical coupling in the smooth muscle cells of the rabbit ear artery. J Gen Physiol 70:129–148

  9. Fleckenstein A, Grun G, Tritthart H, Byon K (1971) Uterus-Relaxation durch hochaktive Ca++-antagonistische Hemmstoffe der elektromechanischen Koppelung wie Isoptin (Verapamil Iproveratril), Substanz D600 ad Segontin (Prenylamin). Klin Wochenschr 49:32–41

  10. Frankenhaeuser B (1957) The effect of calcium on the myelinated nerve fibre. J Physiol 137:245–260

  11. Göthert M, Nawroth P, Neumeyer H (1979) Inhibitory effects of verapamil, prenylamine and D600 on Ca++-dependent noradrenaline release from the sympathetic nerves of isolated rabbit hearts. Naunyn-Schmiedeberg's Arch Pharmacol 310:11–19

  12. Haeusler G (1972) Differential effect of verapamil on excitation-contraction coupling in smooth muscle and on excitation-secretion coupling in adrenergie nerve terminals. J Pharmacol Exp Ther 180:672–682

  13. Harder DR, Sperelakis N (1979) Action potentials induced in guinea-pig arterial smooth muscle by tetraethylammonium. Am J Physiol 237:C75-C80

  14. Hirst GDS (1977) Neuromuscular transmission in arterioles of guinea-pig submucosa. J Physiol 273:263–275

  15. Hirst GDS, Neild TO (1978) An analysis of excitatory junction potentials recorded from arterioles. J Physiol 280:87–104

  16. Hirst GDS, Neild TO (1980a) Evidence for two populations of excitatory receptors for noradrenaline on arteriolar smooth muscle. Nature 283:767–768

  17. Hirst GDS, Neild TO (1980b) Some properties of spontaneous excitatory junction potentials recorded from arterioles of guinea-pigs. J Physiol 303:43–60

  18. Holman ME (1958) Membrane potentials recorded with high-resistance microelectrodes and the effects of changes in ionic environment on the electrical and mechanical activity of the smooth muscle of the taenia coli of the guinea-pig. J Physiol 141:464–488

  19. Holman ME (1969) Electrophysiology of vascular smooth muscle. Ergeb Physiol 61:137–177

  20. Holman ME, Surprenant A (1979) Some properties of the excitatory junction potentials recorded from saphenous arteries of rabbits. J Physiol 287:337–352

  21. Holman ME, Weinrich JP (1975) The effects of calcium and magnesium on inhibitory junction transmission in smooth muscle of guinea-pig small intestine. Pflügers Arch 360:109–119

  22. Horn L, Kumamoto M, Nakajima A (1973) Effects of tetraethylammonium chloride (TEA) on current fluxes: Inconsistencies with toxic hypothesis. Fed Proc 32:405

  23. Katz B, Miledi R (1970) Further study of the role of calcium in synaptic transmission. J Physiol 207:789–801

  24. Keatinge WR (1968a) Ionic requirements for arterial action potential. J Physiol 194:169–182

  25. Keatinge WR (1968b) Sodium flux and electrical activity of arterial smooth muscle. J Physiol 194:183–200

  26. Kuriyama H (1970) Effects of ions and drugs on the electrical activity of smooth muscle. In: Bulbring E, Brading AF, Jones AW, Tomita T (eds) Smooth muscle. Edward Arnold, London, pp 366–395

  27. Mras S, Sperelakis N (1981) Bepridil (CERM-1978) blockade of action potentials in cultured rat aortic smooth muscle cells. Eur J Pharmacol 71:13–19

  28. Nakajima A, Kumamoto M, Horn L (1972) On the mechanism of excitation of vascular smooth muscle. Physiologist 15:225

  29. Narahashi T, Moore JW, Scott WR (1964) Tetrodotoxin blockage of sodium conductance increase in lobster giant axons. J Gen Physiol 47:965–974

  30. Rahamimoff R, Erulkar SD, Alnaes E, Meiri H, Rotshenker S, Rahamimoff H (1975) Modulation of transmitter release by calcium ions and nerve impulses. Cold Spring Harbor Symp XL:107–116

  31. Shigenobu K, Schneider JA, Sperelakis N (1974) Verapamil blockade of slow Na+ and Ca++ response in myocardial cells. J Pharmacol Exp Ther 190:280–288

  32. Somlyo AV (1980) Ultrastructure of vascular smooth muscle. In: Bohr DF, Somlyo AP, Sparks HV (eds) The cardiovascular system, Vol II. Waverly Press Inc., Baltimore, pp 33–67

  33. Speden RN (1964) Electrical activity of single smooth muscle cells of the mesenteric artery produced by splanchnic nerve stimulation in the guinea pig. Nature 202:193–194

  34. Speden RN (1967) Adrenergic transmission in small arteries. Nature 216:289–290

  35. Steedman WM (1966) Microelectrode studies on mammalian vascular muscle. J Physiol 186:382–400

  36. Surprenant A (1980) A comparative study of neuromuscular transmission in several mammalian arteries. Pflügers Arch 386:85–91

  37. Takeuchi N (1963) Effects of calcium on the conductance change of the end-plate membrane during the action of transmitter. J Physiol 167:141–155

  38. Vogel S, Crampton R, Sperelakis N (1979) Blockade of myocardial slow channels by bepridil (CERM-1978). J Pharmacol Exp Ther 210:378–385

  39. Zelcer E (1979) Slow wave activity in rabbit jejunum. Pflügers Arch 381:185–194

  40. Zelcer E, Sperelakis N (1980) Action potential induction by excitatory junction potentials in small pressurized mesenteric arteries. Fed Proc 39:2077

  41. Zelcer E, Sperelakis N (1981) Na and Ca dependence of excitatory junction potentials (EJPs) in vascular smooth muscle. Fed Proc 40:409

Download references

Author information

Correspondence to Nick Sperelakis.

Additional information

Part of this work has been presented to the Biophysical Society (Zelcer and Sperelakis 1980) and to the American Physiological Society (Zelcer and Sperelakis 1981)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Zelcer, E., Sperelakis, N. Ionic dependence of electrical activity in small mesenteric arteries of guinea-pigs. Pflugers Arch. 392, 72–78 (1981). https://doi.org/10.1007/BF00584585

Download citation

Key words

  • Vascular smooth muscle
  • Junction potentials
  • Action potentials
  • Sodium
  • Calcium
  • Verapamil