Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1987 May;386:91–112. doi: 10.1113/jphysiol.1987.sp016524

Voltage-clamp analysis of a crayfish rectifying synapse.

C Giaume 1, R T Kado 1, H Korn 1
PMCID: PMC1192452  PMID: 2824761

Abstract

1. The rectifying crayfish giant motor synapse has been studied in the second abdominal ganglion, using the double-voltage-clamp technique which allowed direct measurements of junctional current at various fixed transjunctional potentials. 2. The transjunctional potential (Vj), defined as the difference between the voltages recorded in the lateral giant axon and the giant motor fibre, was varied from -70 to +50 mV, the minimum and maximum junctional chord conductances (gmin and gmax, respectively) were found to be 1.2 +/- 1.3 microS (n = 10) and 22.9 +/- 6.3 microS (n = 10), respectively. 3. For a given Vj, changes in the lateral giant axon or giant motor fibre membrane potential over a range of +/- 30 mV around their resting levels did not influence the junctional permeability (gj), indicating that the inside-outside potential of the junctional channel does not control gj. 4. Therefore, the steady-state junctional chord conductances were dependent only upon Vj. 5. The voltage dependence of the chord conductance was well fitted by a modified Boltzmann relation given by the equation (Formula: see text) with the constants: A = 0.15 +/- 0.03 mV-1 (n = 10) and V0 = 28 +/- 4 mV (n = 10); the latter two parameters were also found to be independent of both transmembrane potentials. 6. The junctional currents were already constant 1 ms after step changes in the junctional voltage; this was three orders of magnitude faster than the other known examples of voltage-controlled gap junctions between embryonic cells. 7. Our results may be interpreted by a highly voltage-dependent probability of opening of the junctional channels. They also suggest that the gap-junction channels forming the giant motor synapse respond very rapidly to potential and that the hemi-channels which constitute them may not be symmetric.

Full text

PDF
91

Selected References

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

  1. Asada Y., Bennett M. V. Experimental alteration of coupling resistance at an electrotonic synapse. J Cell Biol. 1971 Apr;49(1):159–172. doi: 10.1083/jcb.49.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Auerbach A. A., Bennett M. V. A rectifying electrotonic synapse in the central nervous system of a vertebrate. J Gen Physiol. 1969 Feb;53(2):211–237. doi: 10.1085/jgp.53.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bennett M. V. Physiology of electrotonic junctions. Ann N Y Acad Sci. 1966 Jul 14;137(2):509–539. doi: 10.1111/j.1749-6632.1966.tb50178.x. [DOI] [PubMed] [Google Scholar]
  4. FURSHPAN E. J., POTTER D. D. Transmission at the giant motor synapses of the crayfish. J Physiol. 1959 Mar 3;145(2):289–325. doi: 10.1113/jphysiol.1959.sp006143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Giaume C., Korn H. Ammonium sulfate induced uncouplings of crayfish septate axons with and without increased junctional resistance. Neuroscience. 1982 Jul;7(7):1723–1730. doi: 10.1016/0306-4522(82)90030-6. [DOI] [PubMed] [Google Scholar]
  6. Giaume C., Korn H. Bidirectional transmission at the rectifying electrotonic synapse: a voltage-dependent process. Science. 1983 Apr 1;220(4592):84–87. doi: 10.1126/science.6298940. [DOI] [PubMed] [Google Scholar]
  7. Giaume C., Korn H. Voltage-dependent dye coupling at a rectifying electrotonic synapse of the crayfish. J Physiol. 1984 Nov;356:151–167. doi: 10.1113/jphysiol.1984.sp015458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. HODGKIN A. L., HUXLEY A. F., KATZ B. Measurement of current-voltage relations in the membrane of the giant axon of Loligo. J Physiol. 1952 Apr;116(4):424–448. doi: 10.1113/jphysiol.1952.sp004716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hanna R. B., Keeter J. S., Pappas G. D. The fine structure of a rectifying electrotonic synapse. J Cell Biol. 1978 Dec;79(3):764–773. doi: 10.1083/jcb.79.3.764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Harris A. L., Spray D. C., Bennett M. V. Kinetic properties of a voltage-dependent junctional conductance. J Gen Physiol. 1981 Jan;77(1):95–117. doi: 10.1085/jgp.77.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Johnston M. F., Ramón F. Voltage independence of an electrotonic synapse. Biophys J. 1982 Jul;39(1):115–117. doi: 10.1016/S0006-3495(82)84497-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kramer A. P., Krasne F. B., Wine J. J. Interneurons between giant axons and motoneurons in crayfish escape circuitry. J Neurophysiol. 1981 Mar;45(3):550–573. doi: 10.1152/jn.1981.45.3.550. [DOI] [PubMed] [Google Scholar]
  13. Loewenstein W. R. Junctional intercellular communication: the cell-to-cell membrane channel. Physiol Rev. 1981 Oct;61(4):829–913. doi: 10.1152/physrev.1981.61.4.829. [DOI] [PubMed] [Google Scholar]
  14. Margiotta J. F., Walcott B. Conductance and dye permeability of a rectifying electrical synapse. Nature. 1983 Sep 1;305(5929):52–55. doi: 10.1038/305052a0. [DOI] [PubMed] [Google Scholar]
  15. Mittenthal J. E., Wine J. J. Connectivity patterns of crayfish giant interneurons: visualization of synaptic regions with cobalt dye. Science. 1973 Jan 12;179(4069):182–184. doi: 10.1126/science.179.4069.182. [DOI] [PubMed] [Google Scholar]
  16. Neyton J., Trautmann A. Single-channel currents of an intercellular junction. 1985 Sep 26-Oct 2Nature. 317(6035):331–335. doi: 10.1038/317331a0. [DOI] [PubMed] [Google Scholar]
  17. Nicholls J. G., Purves D. Monosynaptic chemical and electrical connexions between sensory and motor cells in the central nervous system of the leech. J Physiol. 1970 Aug;209(3):647–667. doi: 10.1113/jphysiol.1970.sp009184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Obaid A. L., Socolar S. J., Rose B. Cell-to-cell channels with two independently regulated gates in series: analysis of junctional conductance modulation by membrane potential, calcium, and pH. J Membr Biol. 1983;73(1):69–89. doi: 10.1007/BF01870342. [DOI] [PubMed] [Google Scholar]
  19. Patlak J., Horn R. Effect of N-bromoacetamide on single sodium channel currents in excised membrane patches. J Gen Physiol. 1982 Mar;79(3):333–351. doi: 10.1085/jgp.79.3.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ringham G. L. Localization and electrical characteristics of a giant synapse in the spinal cord of the lamprey. J Physiol. 1975 Oct;251(2):395–407. doi: 10.1113/jphysiol.1975.sp011100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Smith T. G., Baumann F. The functional organization within the ommatidium of the lateral eye of limulus. Prog Brain Res. 1969;31:313–349. doi: 10.1016/S0079-6123(08)63248-3. [DOI] [PubMed] [Google Scholar]
  22. Spira M. E., Bennett M. V. Synaptic control of electrotonic coupling between neurons. Brain Res. 1972 Feb 25;37(2):294–300. doi: 10.1016/0006-8993(72)90674-9. [DOI] [PubMed] [Google Scholar]
  23. Spitzer N. C. Voltage- and stage-dependent uncoupling of Rohon-Beard neurones during embryonic development of Xenopus tadpoles. J Physiol. 1982 Sep;330:145–162. doi: 10.1113/jphysiol.1982.sp014334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Spray D. C., White R. L., de Carvalho A. C., Harris A. L., Bennett M. V. Gating of gap junction channels. Biophys J. 1984 Jan;45(1):219–230. doi: 10.1016/S0006-3495(84)84150-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Verselis V., Brink P. R. Voltage clamp of the earthworm septum. Biophys J. 1984 Jan;45(1):147–150. doi: 10.1016/S0006-3495(84)84143-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. WATANABE A., GRUNDFEST H. Impulse propagation at the septal and commissural junctions of crayfish lateral giant axons. J Gen Physiol. 1961 Nov;45:267–308. doi: 10.1085/jgp.45.2.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Weingart R. Electrical properties of the nexal membrane studied in rat ventricular cell pairs. J Physiol. 1986 Jan;370:267–284. doi: 10.1113/jphysiol.1986.sp015934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Zimmerman A. L., Rose B. Permeability properties of cell-to-cell channels: kinetics of fluorescent tracer diffusion through a cell junction. J Membr Biol. 1985;84(3):269–283. doi: 10.1007/BF01871390. [DOI] [PubMed] [Google Scholar]

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

RESOURCES