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. 1986 Jan;370:111–126. doi: 10.1113/jphysiol.1986.sp015925

The electrotonic location of low-resistance intercellular junctions between a pair of giant neurones in the snail Lymnaea.

P R Benjamin, J B Pilkington
PMCID: PMC1192671  PMID: 3958976

Abstract

The passive electrotonic properties of neurones VD1 and RPD2 in the brain of the snail Lymnaea can be represented by a soma-finite cable model with closed-circuit axon termination. There is a considerable individual variation in input resistance, membrane time constant, electrotonic length and axon-soma conductance ratio, but the average values for these parameters are similar in the two neurones. The cells are tightly coupled by an electrotonic synapse giving an average steady-state coupling coefficient of 0.68 and an average resistance measured between recording sites in the cell bodies of 20 M omega. Calculations using a model consisting of a symmetrical pair of cells with standard values for the electrotonic parameters show that in this system, for a soma-soma resistance of 20 M omega, the junction cannot be more than 0.16 length constants from the cell bodies. Reduction in coupling due to membrane current losses in such short proximal axon segments is insignificant. Intra-axonal recordings indicate that most of the coupling resistance is located at the junction between VD1 and RPD2, which must therefore be closer to the cell bodies than the limiting value of 0.16 length constants assuming an electrical equivalent model which includes the standard electrotonic parameters. If all the soma-soma resistance is located at the junction, then it could be physically a single array of gap-junction particles. Despite its low conductance (1/20 M omega = 50 nS) and possibly small physical dimensions, the electrotonic synapse is more than sufficient to ensure spike synchrony in the two cells.

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Selected References

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

  1. Audesirk G., Audesirk T., Bowsher P. Variability and frequent failure of lucifer yellow to pass between two electrically coupled neurons in Lymnaea stagnalis. J Neurobiol. 1982 Jul;13(4):369–375. doi: 10.1002/neu.480130407. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Boer H. H., Schot L. P., Roubos E. W., ter Maat A., Lodder J. C., Reichelt D., Swaab D. F. ACTH-like immunoreactivity in two electronically coupled giant neurons in the pond snail Lymnaea stagnalis. Cell Tissue Res. 1979 Nov;202(2):231–240. doi: 10.1007/BF00232237. [DOI] [PubMed] [Google Scholar]
  4. Egelhaaf M., Benjamin P. R. Coupled neuronal oscillators in the snail Lymnaea stagnalis: endogenous cellular properties and network interactions. J Exp Biol. 1983 Jan;102:93–114. doi: 10.1242/jeb.102.1.93. [DOI] [PubMed] [Google Scholar]
  5. Getting P. A. Modification of neuron properties by electrotonic synapses. I. Input resistance, time constant, and integration. J Neurophysiol. 1974 Sep;37(5):846–857. doi: 10.1152/jn.1974.37.5.846. [DOI] [PubMed] [Google Scholar]
  6. Getting P. A., Willows A. O. Modification of neuron properties by electrotonic synapses. II. Burst formation by electrotonic synapses. J Neurophysiol. 1974 Sep;37(5):858–868. doi: 10.1152/jn.1974.37.5.858. [DOI] [PubMed] [Google Scholar]
  7. Gorman A. L., Mirolli M. The passive electrical properties of the membrane of a molluscan neurone. J Physiol. 1972 Dec;227(1):35–49. doi: 10.1113/jphysiol.1972.sp010018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hall D. H., Spray D. C., Bennett M. V. Gap junctions and septate-like junctions between neurons of the opisthobranch mollusc Navanax inermis. J Neurocytol. 1983 Oct;12(5):831–846. doi: 10.1007/BF01258154. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Lux H. D., Pollen D. A. Electrical constants of neurons in the motor cortex of the cat. J Neurophysiol. 1966 Mar;29(2):207–220. doi: 10.1152/jn.1966.29.2.207. [DOI] [PubMed] [Google Scholar]
  11. Rall W. Time constants and electrotonic length of membrane cylinders and neurons. Biophys J. 1969 Dec;9(12):1483–1508. doi: 10.1016/S0006-3495(69)86467-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Rose B., Loewenstein W. R. Permeability of cell junction depends on local cytoplasmic calcium activity. Nature. 1975 Mar 20;254(5497):250–252. doi: 10.1038/254250a0. [DOI] [PubMed] [Google Scholar]
  13. Sheridan J. D., Hammer-Wilson M., Preus D., Johnson R. G. Quantitative analysis of low-resistance junctions between cultured cells and correlation with gap-junctional areas. J Cell Biol. 1978 Feb;76(2):532–544. doi: 10.1083/jcb.76.2.532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Spray D. C., Harris A. L., Bennett M. V. Gap junctional conductance is a simple and sensitive function of intracellular pH. Science. 1981 Feb 13;211(4483):712–715. doi: 10.1126/science.6779379. [DOI] [PubMed] [Google Scholar]
  15. Spray D. C., Harris A. L., Bennett M. V. Voltage dependence of junctional conductance in early amphibian embryos. Science. 1979 Apr 27;204(4391):432–434. doi: 10.1126/science.312530. [DOI] [PubMed] [Google Scholar]
  16. Stewart W. W. Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell. 1978 Jul;14(3):741–759. doi: 10.1016/0092-8674(78)90256-8. [DOI] [PubMed] [Google Scholar]

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