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. 1971 Apr 1;49(1):173–188. doi: 10.1083/jcb.49.1.173

MORPHOLOGICAL CORRELATES OF INCREASED COUPLING RESISTANCE AT AN ELECTROTONIC SYNAPSE

George D Pappas 1, Y Asada 1, M V L Bennett 1
PMCID: PMC2108204  PMID: 4995387

Abstract

Close appositions between axonal membranes are present in the septum between adjacent axonal segments of the septate or lateral giant axons of the crayfish Procambarus. In sections the closely apposed membranes appear separated by a space or gap. The use of lanthanum indicates that there may be structures connecting the apposed membranes. The apparent gap is actually a network of channels continuous with the extracellular space. Adjacent axonal segments are electrotonically coupled at the septa. The coupling resistance is increased by mechanical injury of an axon, immersion in low Cl- solutions, and immersion in low Ca++ solutions, followed by a return to normal physiological solution. Septa at which coupling resistance had been measured were examined in the electron microscope. The induced increases in coupling resistance are associated with separation of the junctional membranes (with the exception of the moderate increases during immersion in low Ca++ solutions). Schwann cell processes are present between the separated axonal membranes. When nerve cords in low Cl- solutions are returned to normal physiological solution, coupling, i.e., electrotonic synapses. A model of an electrotonic synapse is proposed in which tween axonal membranes are again found. The association between the morphological and physiological findings provides further evidence that the junctions are the sites of electrotonic coupling, i.e., electrotonic, synapses. A model of an electrotonic synapse is proposed in which intercytoplasmic channels not open to the extracellular space are interlaced with a hexagonal network of extracellular channels between the apposed junctional membranes.

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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. BARR L., DEWEY M. M., BERGER W. PROPAGATION OF ACTION POTENTIALS AND THE STRUCTURE OF THE NEXUS IN CARDIAC MUSCLE. J Gen Physiol. 1965 May;48:797–823. doi: 10.1085/jgp.48.5.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barr L., Berger W., Dewey M. M. Electrical transmission at the nexus between smooth muscle cells. J Gen Physiol. 1968 Mar;51(3):347–368. doi: 10.1085/jgp.51.3.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bennett M. V. Electrical impedance of brain surfaces. Brain Res. 1969 Oct;15(2):584–590. doi: 10.1016/0006-8993(69)90191-7. [DOI] [PubMed] [Google Scholar]
  5. Bennett M. V., Nakajima Y., Pappas G. D. Physiology and ultrastructure of electrotonic junctions. 3. Giant electromotor neurons of Malapterurus electricus. J Neurophysiol. 1967 Mar;30(2):209–235. doi: 10.1152/jn.1967.30.2.209. [DOI] [PubMed] [Google Scholar]
  6. Bennett M. V., Pappas G. D., Aljure E., Nakajima Y. Physiology and ultrastructure of electrotonic junctions. II. Spinal and medullary electromotor nuclei in mormyrid fish. J Neurophysiol. 1967 Mar;30(2):180–208. doi: 10.1152/jn.1967.30.2.180. [DOI] [PubMed] [Google Scholar]
  7. Bennett M. V., Pappas G. D., Giménez M., Nakajima Y. Physiology and ultrastructure of electrotonic junctions. IV. Medullary electromotor nuclei in gymnotid fish. J Neurophysiol. 1967 Mar;30(2):236–300. doi: 10.1152/jn.1967.30.2.236. [DOI] [PubMed] [Google Scholar]
  8. Bennett M. V., Trinkaus J. P. Electrical coupling between embryonic cells by way of extracellular space and specialized junctions. J Cell Biol. 1970 Mar;44(3):592–610. doi: 10.1083/jcb.44.3.592. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brightman M. W., Reese T. S. Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol. 1969 Mar;40(3):648–677. doi: 10.1083/jcb.40.3.648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bullivant S., Loewenstein W. R. Structure of coupled and uncoupled cell junctions. J Cell Biol. 1968 Jun;37(3):621–632. doi: 10.1083/jcb.37.3.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chalcroft J. P., Bullivant S. An interpretation of liver cell membrane and junction structure based on observation of freeze-fracture replicas of both sides of the fracture. J Cell Biol. 1970 Oct;47(1):49–60. doi: 10.1083/jcb.47.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. FARQUHAR M. G., PALADE G. E. Junctional complexes in various epithelia. J Cell Biol. 1963 May;17:375–412. doi: 10.1083/jcb.17.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goodenough D. A., Revel J. P. A fine structural analysis of intercellular junctions in the mouse liver. J Cell Biol. 1970 May;45(2):272–290. doi: 10.1083/jcb.45.2.272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. HAMA K. Some observations on the fine structure of the giant fibers of the crayfishes (Cambarus virilus and Cambarus clarkii) with special reference to the submicroscopic organization of the synapses. Anat Rec. 1961 Dec;141:275–293. doi: 10.1002/ar.1091410403. [DOI] [PubMed] [Google Scholar]
  15. Holtzman E., Freeman A. R., Kashner L. A. A cytochemical and electron microscope study of channels in the Schwann cells surrounding lobster giant axons. J Cell Biol. 1970 Feb;44(2):438–445. doi: 10.1083/jcb.44.2.438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Loewenstein W. R. On the genesis of cellular communication. Dev Biol. 1967 Jun;15(6):503–520. doi: 10.1016/0012-1606(67)90050-4. [DOI] [PubMed] [Google Scholar]
  17. Pappas G. D., Bennett M. V. Specialized junctions involved in electrical transmission between neurons. Ann N Y Acad Sci. 1966 Jul 14;137(2):495–508. doi: 10.1111/j.1749-6632.1966.tb50177.x. [DOI] [PubMed] [Google Scholar]
  18. Pappas G. D. Some morphological considerations of the blood-brain barrier. J Neurol Sci. 1970 Mar;10(3):241–246. doi: 10.1016/0022-510x(70)90152-8. [DOI] [PubMed] [Google Scholar]
  19. Payton B. W., Bennett M. V., Pappas G. D. Permeability and structure of junctional membranes at an electrotonic synapse. Science. 1969 Dec 26;166(3913):1641–1643. doi: 10.1126/science.166.3913.1641. [DOI] [PubMed] [Google Scholar]
  20. Payton B. W., Bennett M. V., Pappas G. D. Temperature-dependence of resistance at an electrotonic synapse. Science. 1969 Aug 8;165(3893):594–597. doi: 10.1126/science.165.3893.594. [DOI] [PubMed] [Google Scholar]
  21. ROBERTSON J. D. THE OCCURRENCE OF A SUBUNIT PATTERN IN THE UNIT MEMBRANES OF CLUB ENDINGS IN MAUTHNER CELL SYNAPSES IN GOLDFISH BRAINS. J Cell Biol. 1963 Oct;19:201–221. doi: 10.1083/jcb.19.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Revel J. P., Karnovsky M. J. Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J Cell Biol. 1967 Jun;33(3):C7–C12. doi: 10.1083/jcb.33.3.c7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]

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