Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1989 May;412:493–512. doi: 10.1113/jphysiol.1989.sp017628

Calcium currents in the normal adult rat sympathetic neurone.

O Belluzzi 1, O Sacchi 1
PMCID: PMC1190588  PMID: 2557430

Abstract

1. The calcium currents evoked by membrane depolarization in the mature and intact rat sympathetic neurone have been studied at 37 degrees C using two-electrode voltage-clamp analysis. 2. Under conditions that eliminate Na+ and K+ currents and 5 mM-external Ca2+, inward currents were observed that activated at about -30 mV and reached maximum amplitude between 0 and +10 mV with time-to-peak values (2.7-1.9 ms) decreasing with increasing membrane depolarization. Thereafter, calcium current (ICa) decayed to a virtually zero level with maintained depolarization. Two exponentials were required to describe the total inactivation process. The faster rate (tau = 29.3-17.6 ms) is ten times the slower rate and proved to be only slightly voltage-dependent. Double-pulse experiments gave a similar time course of turn-off. 3. No steady-state inactivation was removed at holding potentials between -40 and -70 mV and indirect data suggest that all the ICa was available at -50 mV. Within the -30 to -50 mV holding potential range no significant modifications either in the final amount of ICa inactivation or in the inactivation time constant values were detected. 4. After an initial 100 ms, recovery from inactivation followed a single-exponential process with a mean time constant value of 1.54 s at -50 mV. 5. The kinetics of ICa observed in this neurone were consistent with the existence of a single class of Ca2+ channels. For times up to 20 ms, ICa is described reasonably well by a Hodgkin-Huxley c2hc scheme. The activation time constant was 0.57 ms close to threshold and 0.29 ms at +30 mV. Deactivation occurred with a similar fast time course. The steady-state value of the variable c was evaluated in the -40 to +20 mV voltage range: 9.9 mV are required to change c infinity e-fold. 6. Following previous analyses, we have formulated a mathematical model which incorporates the present ICa kinetic equations with Hodgkin-Huxley-type gating mechanisms for INa, IA and IK(V) conductances. The Ca2+ load of the neurone proved to be basically an 'off' effect and to be governed by the duration of the action potential falling phase. The model is consistent with the experimental observations indicating that Ca2+ channels probably do not have an important direct electrical function in the sympathetic neurone spike at normal membrane potential levels.(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
497

Selected References

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

  1. Barish M. E. Differentiation of voltage-gated potassium current and modulation of excitability in cultured amphibian spinal neurones. J Physiol. 1986 Jun;375:229–250. doi: 10.1113/jphysiol.1986.sp016114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beam K. G., Knudson C. M. Effect of postnatal development on calcium currents and slow charge movement in mammalian skeletal muscle. J Gen Physiol. 1988 Jun;91(6):799–815. doi: 10.1085/jgp.91.6.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Belluzzi O., Sacchi O. A quantitative description of the sodium current in the rat sympathetic neurone. J Physiol. 1986 Nov;380:275–291. doi: 10.1113/jphysiol.1986.sp016285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Belluzzi O., Sacchi O. The interactions between potassium and sodium currents in generating action potentials in the rat sympathetic neurone. J Physiol. 1988 Mar;397:127–147. doi: 10.1113/jphysiol.1988.sp016992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Belluzzi O., Sacchi O., Wanke E. A fast transient outward current in the rat sympathetic neurone studied under voltage-clamp conditions. J Physiol. 1985 Jan;358:91–108. doi: 10.1113/jphysiol.1985.sp015542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bonifazzi C., Belluzzi O., Sacchi O. Kinetic analysis of incomplete current tracings according to the Hodgkin-Huxley model. J Theor Biol. 1988 Jan 21;130(2):183–190. doi: 10.1016/s0022-5193(88)80093-6. [DOI] [PubMed] [Google Scholar]
  7. Bossu J. L., Feltz A., Thomann J. M. Depolarization elicits two distinct calcium currents in vertebrate sensory neurones. Pflugers Arch. 1985 Apr;403(4):360–368. doi: 10.1007/BF00589247. [DOI] [PubMed] [Google Scholar]
  8. Brown A. M., Morimoto K., Tsuda Y., wilson D. L. Calcium current-dependent and voltage-dependent inactivation of calcium channels in Helix aspersa. J Physiol. 1981 Nov;320:193–218. doi: 10.1113/jphysiol.1981.sp013944. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Carbone E., Lux H. D. A low voltage-activated calcium conductance in embryonic chick sensory neurons. Biophys J. 1984 Sep;46(3):413–418. doi: 10.1016/S0006-3495(84)84037-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Carbone E., Lux H. D. Kinetics and selectivity of a low-voltage-activated calcium current in chick and rat sensory neurones. J Physiol. 1987 May;386:547–570. doi: 10.1113/jphysiol.1987.sp016551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Carbone E., Lux H. D. Single low-voltage-activated calcium channels in chick and rat sensory neurones. J Physiol. 1987 May;386:571–601. doi: 10.1113/jphysiol.1987.sp016552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Eckert R., Chad J. E. Inactivation of Ca channels. Prog Biophys Mol Biol. 1984;44(3):215–267. doi: 10.1016/0079-6107(84)90009-9. [DOI] [PubMed] [Google Scholar]
  13. Eckert R., Tillotson D. L. Calcium-mediated inactivation of the calcium conductance in caesium-loaded giant neurones of Aplysia californica. J Physiol. 1981 May;314:265–280. doi: 10.1113/jphysiol.1981.sp013706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fedulova S. A., Kostyuk P. G., Veselovsky N. S. Two types of calcium channels in the somatic membrane of new-born rat dorsal root ganglion neurones. J Physiol. 1985 Feb;359:431–446. doi: 10.1113/jphysiol.1985.sp015594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fenwick E. M., Marty A., Neher E. Sodium and calcium channels in bovine chromaffin cells. J Physiol. 1982 Oct;331:599–635. doi: 10.1113/jphysiol.1982.sp014394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fox A. P., Nowycky M. C., Tsien R. W. Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J Physiol. 1987 Dec;394:149–172. doi: 10.1113/jphysiol.1987.sp016864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fox A. P., Nowycky M. C., Tsien R. W. Single-channel recordings of three types of calcium channels in chick sensory neurones. J Physiol. 1987 Dec;394:173–200. doi: 10.1113/jphysiol.1987.sp016865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Freschi J. E. Membrane currents of cultured rat sympathetic neurons under voltage clamp. J Neurophysiol. 1983 Dec;50(6):1460–1478. doi: 10.1152/jn.1983.50.6.1460. [DOI] [PubMed] [Google Scholar]
  19. Fukuda J., Kameyama M. Enhancement of Ca spikes in nerve cells of adult mammals during neurite growth in tissue culture. Nature. 1979 Jun 7;279(5713):546–548. doi: 10.1038/279546a0. [DOI] [PubMed] [Google Scholar]
  20. Galvan M., Adams P. R. Control of calcium current in rat sympathetic neurons by norepinephrine. Brain Res. 1982 Jul 22;244(1):135–144. doi: 10.1016/0006-8993(82)90911-8. [DOI] [PubMed] [Google Scholar]
  21. Gillespie J. I., Meves H. The time course of sodium inactivation in squid giant axons. J Physiol. 1980 Feb;299:289–307. doi: 10.1113/jphysiol.1980.sp013125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gonoi T., Hasegawa S. Post-natal disappearance of transient calcium channels in mouse skeletal muscle: effects of denervation and culture. J Physiol. 1988 Jul;401:617–637. doi: 10.1113/jphysiol.1988.sp017183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hagiwara S., Byerly L. Calcium channel. Annu Rev Neurosci. 1981;4:69–125. doi: 10.1146/annurev.ne.04.030181.000441. [DOI] [PubMed] [Google Scholar]
  26. Hirning L. D., Fox A. P., McCleskey E. W., Olivera B. M., Thayer S. A., Miller R. J., Tsien R. W. Dominant role of N-type Ca2+ channels in evoked release of norepinephrine from sympathetic neurons. Science. 1988 Jan 1;239(4835):57–61. doi: 10.1126/science.2447647. [DOI] [PubMed] [Google Scholar]
  27. Kay A. R., Wong R. K. Calcium current activation kinetics in isolated pyramidal neurones of the Ca1 region of the mature guinea-pig hippocampus. J Physiol. 1987 Nov;392:603–616. doi: 10.1113/jphysiol.1987.sp016799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Krishtal O. A., Pidoplichko V. I., Shakhovalov Y. A. Conductance of the calcium channel in the membrane of snail neurones. J Physiol. 1981 Jan;310:423–434. doi: 10.1113/jphysiol.1981.sp013558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Llinás R., Steinberg I. Z., Walton K. Presynaptic calcium currents in squid giant synapse. Biophys J. 1981 Mar;33(3):289–321. doi: 10.1016/S0006-3495(81)84898-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Marrion N. V., Smart T. G., Brown D. A. Membrane currents in adult rat superior cervical ganglia in dissociated tissue culture. Neurosci Lett. 1987 Jun 1;77(1):55–60. doi: 10.1016/0304-3940(87)90606-9. [DOI] [PubMed] [Google Scholar]
  31. Matsuda Y., Yoshida S., Yonezawa T. Tetrodotoxin sensitivity and Ca component of action potentials of mouse dorsal root ganglion cells cultured in vitro. Brain Res. 1978 Oct 6;154(1):69–82. doi: 10.1016/0006-8993(78)91052-1. [DOI] [PubMed] [Google Scholar]
  32. McAfee D. A., Yarowsky P. J. Calcium-dependent potentials in the mammalian sympathetic neurone. J Physiol. 1979 May;290(2):507–523. doi: 10.1113/jphysiol.1979.sp012787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Mitani S. The reduction of calcium current associated with early differentiation of the murine embryo. J Physiol. 1985 Jun;363:71–86. doi: 10.1113/jphysiol.1985.sp015696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Nowycky M. C., Fox A. P., Tsien R. W. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature. 1985 Aug 1;316(6027):440–443. doi: 10.1038/316440a0. [DOI] [PubMed] [Google Scholar]
  35. Schofield G. G., Ikeda S. R. Sodium and calcium currents of acutely isolated adult rat superior cervical ganglion neurons. Pflugers Arch. 1988 May;411(5):481–490. doi: 10.1007/BF00582368. [DOI] [PubMed] [Google Scholar]
  36. Wanke E., Ferroni A., Malgaroli A., Ambrosini A., Pozzan T., Meldolesi J. Activation of a muscarinic receptor selectively inhibits a rapidly inactivated Ca2+ current in rat sympathetic neurons. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4313–4317. doi: 10.1073/pnas.84.12.4313. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES