Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1981 Feb;311:23–55. doi: 10.1113/jphysiol.1981.sp013571

The characteristics of synaptic currents and responses to acetylcholine of rat submandibular ganglion cells

H P Rang 1
PMCID: PMC1275396  PMID: 6267251

Abstract

1. Synaptic currents and responses to acetylcholine (ACh) have been recorded at 20°C from rat submandibular ganglion cells by a two micro-electrode volatage-clamp technique.

2. The peak amplitude (ap) of excitatory synaptic currents (e.s.c.s) was linearly related to membrane potential (Em), with a reversal potential close to - 10 mV. E.s.c.s decayed with a bi-exponential time course, the fast phase comprising just over half the total amplitude. The time constant (τf) of the fast phase was 5-9 msec, while that of the slow phase (τs) was 27-45 msec. The relative amplitudes of the two components remained constant at different membrane potentials, showing that the reversal potential was the same for both.

3. Both τf and τs increased as the cell was hyperpolarized, the ratio τ(-80)/τ(-40) being about 1.6 for both fast and slow components.

4. Increasing the calcium concentration from 2.5 to 7.5 mm increased the amplitude of both components by about 40% and also prolonged the synaptic currents 30-50%, its effect being slightly greater on τs than on τf.

5. In contrast to e.s.c.s, spontaneous or potassium-evoked miniature synaptic currents (m.s.c.s) showed a simple exponential decay with a time constant (τm.s.c.) very similar to τf. τm.s.c. showed the same sensitivity to membrane potential and calcium concentration as τf.

6. In the presence of neostigmine (10 μm) e.s.c.s were prolonged, τf about 3.5-fold and τs about 2.5-fold. The decay remained bi-exponential, with little change in the relative amplitude or voltage-dependence of the two components. M.s.c.s were prolonged to a lesser extent (1.5-2-fold) and the voltage dependence of τm.s.c. was unaffected by neostigmine.

7. Reduction of the quantal content of the e.s.c. by low calcium—high magnesium solution did not affect the time course. The relative amplitudes, and the time constants of the two components were unchanged even with a 90% reduction of ap.

8. Voltage-jump studies, in which the cell was abruptly hyperpolarized by 20-40 mV during a response to ionophoretically applied ACh, showed a relaxation pattern consisting of two distinct exponential components, whose relative amplitudes varied considerably in different cells. The two rate constants τf.rel and τs.rel were somewhat shorter than τf and τs for e.s.c.s, the difference being generally less than two-fold.

9. Measurements of ACh noise also revealed two kinetic components, the time constants of which corresponded closely to τf and τs for e.s.c.s. On the assumption that the two components represent channels of equal conductance, the single channel conductance, γ, was calculated to be 31±3 pS, similar to that of endplate channels.

10. It is concluded that the two kinetic components of e.s.c.s and ACh responses probably represent two distinct classes of ACh-operated ionic channels, whose mean lifetime differs about fivefold. The two types of channel show the same ionic selectivity and their mean lifetime varies in the same way with the membrane potential. The absence of a slow component in m.s.c.s suggests that the two types of channel are spatially separate in the membrane.

Full text

PDF
23

Selected References

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

  1. Adams P. R. Kinetics of agonist conductance changes during hyperolarization at frog endplates. Br J Pharmacol. 1975 Feb;53(2):308–310. doi: 10.1111/j.1476-5381.1975.tb07364.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson C. R., Stevens C. F. Voltage clamp analysis of acetylcholine produced end-plate current fluctuations at frog neuromuscular junction. J Physiol. 1973 Dec;235(3):655–691. doi: 10.1113/jphysiol.1973.sp010410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ascher P., Large W. A., Rang H. P. Studies on the mechanism of action of acetylcholine antagonists on rat parasympathetic ganglion cells. J Physiol. 1979 Oct;295:139–170. doi: 10.1113/jphysiol.1979.sp012958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ascher P., Marty A., Neild T. O. Life time and elementary conductance of the channels mediating the excitatory effects of acetylcholine in Aplysia neurones. J Physiol. 1978 May;278:177–206. doi: 10.1113/jphysiol.1978.sp012299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. BLACKMAN J. G., GINSBORG B. L., RAY C. On the quantal release of the transmitter at a sympathetic synapse. J Physiol. 1963 Jul;167:402–415. doi: 10.1113/jphysiol.1963.sp007158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. BLACKMAN J. G., GINSBORG B. L., RAY C. Spontaneous synaptic activity in sympathetic ganglion cells of the frog. J Physiol. 1963 Jul;167:389–401. doi: 10.1113/jphysiol.1963.sp007157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. BLACKMAN J. G., GINSBORG B. L., RAY C. Synaptic transmission in the sympathetic ganglion of the frog. J Physiol. 1963 Jul;167:355–373. doi: 10.1113/jphysiol.1963.sp007155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Blackman J. G., Purves R. D. Intracellular recordings from ganglia of the thoracic sympathetic chain of the guinea-pig. J Physiol. 1969 Jul;203(1):173–198. doi: 10.1113/jphysiol.1969.sp008858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Colquhoun D., Dreyer F., Sheridan R. E. The actions of tubocurarine at the frog neuromuscular junction. J Physiol. 1979 Aug;293:247–284. doi: 10.1113/jphysiol.1979.sp012888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Colquhoun D., Large W. A., Rang H. P. An analysis of the action of a false transmitter at the neuromuscular junction. J Physiol. 1977 Apr;266(2):361–395. doi: 10.1113/jphysiol.1977.sp011772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Crawford A. C., McBurney R. N. On the elementary conductance event produced by L-glutamate and quanta of the natural transmitter at the neuromuscular junctions of Maia squinado. J Physiol. 1976 Jun;258(1):205–225. doi: 10.1113/jphysiol.1976.sp011415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. DEL CASTILLO J., KATZ B. Interaction at end-plate receptors between different choline derivatives. Proc R Soc Lond B Biol Sci. 1957 May 7;146(924):369–381. doi: 10.1098/rspb.1957.0018. [DOI] [PubMed] [Google Scholar]
  13. Dennis M. J., Harris A. J., Kuffler S. W. Synaptic transmission and its duplication by focally applied acetylcholine in parasympathetic neurons in the heart of the frog. Proc R Soc Lond B Biol Sci. 1971 Apr 27;177(1049):509–539. doi: 10.1098/rspb.1971.0045. [DOI] [PubMed] [Google Scholar]
  14. Dionne V. E., Steinbach J. H., Stevens C. F. An analysis of the dose-response relationship at voltage-clamped frog neuromuscular junctions. J Physiol. 1978 Aug;281:421–444. doi: 10.1113/jphysiol.1978.sp012431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dionne V. E., Stevens C. F. Voltage dependence of agonist effectiveness at the frog neuromuscular junction: resolution of a paradox. J Physiol. 1975 Oct;251(2):245–270. doi: 10.1113/jphysiol.1975.sp011090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dreyer F., Peper K. Iontophoretic application of acetylcholine: advantages of high resistance micropipettes in connection with an electronic current pump. Pflugers Arch. 1974 Apr 22;348(3):263–272. doi: 10.1007/BF00587417. [DOI] [PubMed] [Google Scholar]
  17. Dreyer F., Peper K., Sterz R. Determination of dose-response curves by quantitative ionophoresis at the frog neuromuscular junction. J Physiol. 1978 Aug;281:395–419. doi: 10.1113/jphysiol.1978.sp012430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gage P. W. Generation of end-plate potentials. Physiol Rev. 1976 Jan;56(1):177–247. doi: 10.1152/physrev.1976.56.1.177. [DOI] [PubMed] [Google Scholar]
  19. Gage P. W., McBurney R. N. Effects of membrane potential, temperature and neostigmine on the conductance change caused by a quantum or acetylcholine at the toad neuromuscular junction. J Physiol. 1975 Jan;244(2):385–407. doi: 10.1113/jphysiol.1975.sp010805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Graubard K. Voltage attenuation within Aplysia neurons: the effect of branching pattern. Brain Res. 1975 May 2;88(2):325–332. doi: 10.1016/0006-8993(75)90394-7. [DOI] [PubMed] [Google Scholar]
  21. Hartzell H. C., Kuffler S. W., Stickgold R., Yoshikami D. Synaptic excitation and inhibition resulting from direct action of acetylcholine on two types of chemoreceptors on individual amphibian parasympathetic neurones. J Physiol. 1977 Oct;271(3):817–846. doi: 10.1113/jphysiol.1977.sp012027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hartzell H. C., Kuffler S. W., Yoshikami D. Post-synaptic potentiation: interaction between quanta of acetylcholine at the skeletal neuromuscular synapse. J Physiol. 1975 Oct;251(2):427–463. doi: 10.1113/jphysiol.1975.sp011102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Katz B., Miledi R. The binding of acetylcholine to receptors and its removal from the synaptic cleft. J Physiol. 1973 Jun;231(3):549–574. doi: 10.1113/jphysiol.1973.sp010248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Katz B., Miledi R. The statistical nature of the acetycholine potential and its molecular components. J Physiol. 1972 Aug;224(3):665–699. doi: 10.1113/jphysiol.1972.sp009918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kordas M. An attempt at an analysis of the factors determining the time course of the end-plate current. I. The effects of prostigmine and of the ratio of Mg 2+ to Ca 2+ . J Physiol. 1972 Jul;224(2):317–332. doi: 10.1113/jphysiol.1972.sp009897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kuba K., Koketsu K. Synaptic events in sympathetic ganglia. Prog Neurobiol. 1978;11(2):77–169. doi: 10.1016/0301-0082(78)90010-2. [DOI] [PubMed] [Google Scholar]
  27. Kuba K., Nishi S. Characteristics of fast excitatory postsynaptic current in bullfrog sympathetic ganglion cells. Effects of membrane potential, temperature and Ca ions. Pflugers Arch. 1979 Jan 31;378(3):205–212. doi: 10.1007/BF00592737. [DOI] [PubMed] [Google Scholar]
  28. Kuba K., Tomita T. Effect of prostigmine on the time course of the end-plate potential in the rat diaphragm. J Physiol. 1971 Mar;213(3):533–544. doi: 10.1113/jphysiol.1971.sp009398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Landau E. M. Function and structure of the ACh receptor at the muscle end-plate. Prog Neurobiol. 1978;10(4):253–288. doi: 10.1016/0301-0082(78)90005-9. [DOI] [PubMed] [Google Scholar]
  30. Large W. A., Rang H. P. Factors affecting the rate of incorporation of a false transmitter into mammalian motor nerve terminals. J Physiol. 1978 Dec;285:1–24. doi: 10.1113/jphysiol.1978.sp012553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lichtman J. W. The reorganization of synaptic connexions in the rat submandibular ganglion during post-natal development. J Physiol. 1977 Dec;273(1):155–177. doi: 10.1113/jphysiol.1977.sp012087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. MARTIN A. R., PILAR G. QUANTAL COMPONENTS OF THE SYNAPTIC POTENTIAL IN THE CILIARY GANGLION OF THE CHICK. J Physiol. 1964 Dec;175:1–16. doi: 10.1113/jphysiol.1964.sp007499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. MacDermott A. B., Connor E. A., Dionne V. E., Parsons R. L. Voltage clamp study of fast excitatory synaptic currents in bullfrog sympathetic ganglion cells. J Gen Physiol. 1980 Jan;75(1):39–60. doi: 10.1085/jgp.75.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Magleby K. L., Stevens C. F. The effect of voltage on the time course of end-plate currents. J Physiol. 1972 May;223(1):151–171. doi: 10.1113/jphysiol.1972.sp009839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Magleby K. L., Terrar D. A. Factors affecting the time course of decay of end-plate currents: a possible cooperative action of acetylcholine on receptors at the frog neuromuscular junction. J Physiol. 1975 Jan;244(2):467–495. doi: 10.1113/jphysiol.1975.sp010808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Marchais D., Marty A. Interaction of permeant ions with channels activated by acetylcholine in Aplysia neurones. J Physiol. 1979 Dec;297(0):9–45. doi: 10.1113/jphysiol.1979.sp013025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Meech R. W. The sensitivity of Helix aspersa neurones to injected calcium ions. J Physiol. 1974 Mar;237(2):259–277. doi: 10.1113/jphysiol.1974.sp010481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. NISHI S., KOKETSU K. Electrical properties and activities of single sympathetic neurons in frogs. J Cell Comp Physiol. 1960 Feb;55:15–30. doi: 10.1002/jcp.1030550104. [DOI] [PubMed] [Google Scholar]
  39. Neher E., Sakmann B. Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature. 1976 Apr 29;260(5554):799–802. doi: 10.1038/260799a0. [DOI] [PubMed] [Google Scholar]
  40. Neher E., Sakmann B. Voltage-dependence of drug-induced conductance in frog neuromuscular junction. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2140–2144. doi: 10.1073/pnas.72.6.2140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Rang H. P. Acetylcholine receptors. Q Rev Biophys. 1974 Jul;7(3):283–399. doi: 10.1017/s0033583500001463. [DOI] [PubMed] [Google Scholar]
  42. Rang H. P. Allosteric mechanisms at neuromuscular junctions. Neurosci Res Program Bull. 1973 Jun;11(3):220–224. [PubMed] [Google Scholar]
  43. Rang H. P. Synaptic currents of rat parasympathetic ganglion cells [proceedings]. J Physiol. 1979 Nov;296:74P–75P. [PubMed] [Google Scholar]
  44. Selyanko A. A., Derkach V. A., Skok V. I. Fast excitatory postsynaptic currents in voltage-clamped mammalian sympathetic ganglion neurones. J Auton Nerv Syst. 1979 Dec;1(2):127–137. doi: 10.1016/0165-1838(79)90011-0. [DOI] [PubMed] [Google Scholar]
  45. Selyanko A. A., Skok V. I. Activation of acetylcholine receptors in mammalian sympathetic ganglion neurones. Prog Brain Res. 1979;49:241–252. doi: 10.1016/S0079-6123(08)64637-3. [DOI] [PubMed] [Google Scholar]
  46. Sheridan R. E., Lester H. A. Rates and equilibria at the acetylcholine receptor of Electrophorus electroplaques: a study of neurally evoked postsynaptic currents and of voltage-jump relaxations. J Gen Physiol. 1977 Aug;70(2):187–219. [PMC free article] [PubMed] [Google Scholar]
  47. Suzuki T., Kusano K. Hyperpolarizing potentials induced by Ca-mediated K-conductance increase in hamster submandibular ganglion cells. J Neurobiol. 1978 Sep;9(5):367–392. doi: 10.1002/neu.480090504. [DOI] [PubMed] [Google Scholar]
  48. Suzuki T., Volle R. L. Nicotinic, muscarinic and adrenergic receptors in a parasympathetic ganglion. J Pharmacol Exp Ther. 1979 Oct;211(1):252–256. [PubMed] [Google Scholar]
  49. Wathey J. C., Nass M. M., Lester H. A. Numerical reconstruction of the quantal event at nicotinic synapses. Biophys J. 1979 Jul;27(1):145–164. doi: 10.1016/S0006-3495(79)85208-X. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES