Electrotonic Coupling in the Nervous System

  • Stewart W. Jaslove
  • Peter R. Brink
Chapter

Abstract

The topic of cell-to-cell communication in the nervous system primarily concerns the electrotonic synapse. This is a low-resistance intercellular pathway that permits the direct flow of electrical current between coupled cells, thus obviating the need for a neurochemically mediated step. The first description of a definitive electrotonic synapse, the crayfish motor giant synapse, appeared in 1957 (Furshpan and Potter, 1957) and numerous other examples from nervous systems of many phyla have since been demonstrated. By definitive we mean a specific synaptic structure mediating neurotransmission, as opposed to a fusion or close apposition of neighboring cells. Several lines of anatomical and pharmacological evidence have shown that this structure is the gap junction intercellular channel (see Section 4).

Keywords

Ventral Nerve Cord Motor Axon Lucifer Yellow Giant Axon Chemical Synapse 
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References

  1. Alger, B. E., McCarren, M., and Fisher, R. S., 1983, On the possibility of simultaneously recording from two cells with a single microelectrode in the hippocampal slice, Brain Res. 270:137–141.PubMedGoogle Scholar
  2. Alkon, D. L., and Grossman, L., 1978, Evidence for nonsynaptic neuronal interaction, J. Neu- rophysiol. 41:640–653.Google Scholar
  3. Anderson, T. E., and Bittner, G. D., 1980, Long term alteration of electrotonic synapses, Brain Res. 184:13–36.Google Scholar
  4. Andrew, R. D., MacVicar, B. A., Dudek, F. E., and Hatton, G. I., 1981, Dye transfer through gap junctions between neuroendocrine cells of rat hypothalamus, Science 211:1187–1189.PubMedGoogle Scholar
  5. Arvanitaki, A., and Chalazonitis, N., 1959, Interactions electriques entre le soma geant A et les somata immediatement contigus, Bull. Inst. Oceanogr. Monaco No. 1143, pp. 1–30.Google Scholar
  6. Asada, Y., and Bennett, M. V. L., 1971, Experimental alteration of coupling resistance at an electrotonic synapse. J. Cell Biol. 49:159–172.PubMedGoogle Scholar
  7. Audesirk, G., Audesirk, T., and Bowsher, P., 1982, Variability and frequent failure of Lucifer Yellow to pass between two electrically coupled neurons in Lymnaea stagnalis, J. Neurobiol. 13:369–375.PubMedGoogle Scholar
  8. Auerbach, A. A., and Bennett, M. V. L., 1969, A rectifying electrotonic synapse in the central nervous system of a vertebrate, J. Gen. Physiol. 53:211–237.PubMedGoogle Scholar
  9. Baker, R., and Llinas, L., 1971, Electrotonic coupling between neurones in the rat mesencephalic nucleus, J. Physiol. (London) 212:45–63.Google Scholar
  10. Barr, L., Dewey, M. M., and Berger, W., 1965, Propagation of action potentials and the structure of the nexus in cardiac muscle, J. Gen. Physiol. 48:797–823.PubMedGoogle Scholar
  11. Barr, L., Berger, W., and Dewey, M. M., 1968, Electrical transmission at the nexus between smooth muscle cells, J. Gen. Physiol. 51:347–368.PubMedGoogle Scholar
  12. Baux, G., Simonneau, M., Tauc, L., and Segundo, J. P., 1978, Uncoupling of electrotonic synapses by calcium, Proc. Natl. Acad. Sci. USA 75:4577–4581.PubMedGoogle Scholar
  13. Baylor, D. A., and Nicholls, J. G., 1969, Chemical and electrical synaptic connexions between cutaneous mechanoreceptor neurones in the central nervous system of the leech, J. Physiol. (London) 203:591–609.Google Scholar
  14. Baylor, D. A., Fuortes, M. G. F., and O’Bryan, P. M., 1971, Receptive fields of cones in the retina of the turtle, J. Physiol. (London) 214:265–294.Google Scholar
  15. Bennett, M. V. L., 1966, Physiology of electrotonic junctions, Ann. N.Y. Acad. Sci. 137(Art. 2):509–539.PubMedGoogle Scholar
  16. Bennett, M. V. L., 1968, Similarities between chemically and electrically mediated transmission, in: Physiological and Biochemical Aspects of Nervous Integration (F. D. Carlson, ed.), pp. 73– 128, Prentice-Hall, Englewood Cliffs, N.J.Google Scholar
  17. Bennett, M. V. L., 1972, A comparison of electrically and chemically mediated transmission, in: Structure and Function of Synapses (G. D. Pappas and D. P. Purpura, eds.), pp. 221–256, Raven Press, New York.Google Scholar
  18. Bennett, M. V. L., 1973, Permeability and structure of electrotonic junctions and intercellular movements of tracers, in: Intracellular Staining in Neurobiology (S. B. Kater and C. Nicholson, eds.), pp. 115–134, Springer-Verlag, Berlin.Google Scholar
  19. Bennett, M. V. L., 1977, Electrical transmission: A functional analysis and comparison to chemical transmission, in: Handbook of Physiology-The Nervous System I (E. R. Kandel, ed.), pp. 357– 416, Williams & Wilkins, Baltimore.Google Scholar
  20. Bennett, M. V. L., and Pappas, G. D., 1983, The electromotor system of the stargazer: A model for integrative actions at electrotonic synapses, J. Neurosci. 3:748–761.PubMedGoogle Scholar
  21. Bennett, M. V. L., Aljure, E., Nakajima, Y., and Pappas, G. D., 1963, Electrotonic junctions between teleost spinal neurons: Electrophysiology and ultrastructure, Science 141:262–264. Bennett, M. V. L., Nakajima, Y., and Pappas, G. D., 1967a, Physiology and ultrastructure of electrotonic junctions. I. Supramedullary neurons, J. Neurophysiol. 30:161-179.PubMedGoogle Scholar
  22. Bennett, M. V. L., Aljure, E., Nakajima, Y., and Pappas, G. D., 1963, Electrotonic junctions between teleost spinal neurons: Electrophysiology and ultrastructure, Science 141:262-264. Bennett, M. V. L., Nakajima, Y., and Pappas, G. D., 1967a, Physiology and ultrastructure of electrotonic junctions. I. Supramedullary neurons, J. Neurophysiol. 30:161–179.PubMedGoogle Scholar
  23. Bennett, M. V. L., Pappas, G. D., Aljure, E., and Nakajima, Y., 1967b, Physiology and ultrastructure of electrotonic junctions. II. Spinal and medullary electromotor nuclei in mormyrid fish, J. Neurophysiol. 30:180–208.PubMedGoogle Scholar
  24. Bennett, M. V. L., Nakajima, Y., and Pappas, G. D., 1967c., Physiology and ultrastructure of electrotonic junctions, III. Giant electromotor neurons of Malapterurus electricus, J. Neurophysiol. 30:209–235.PubMedGoogle Scholar
  25. Bennett, M. V. L., Pappas, G. D., Gimenez, M., and Nakajima, Y., 1967d, Physiology and ultrastructure of electrotonic junctions. IV. Medullary electromotor nuclei in gymnotid fish, J. Neurophysiol. 30:236–300.PubMedGoogle Scholar
  26. Bennett, M. V. L., Spira, M. E., and Pappas, G. D., 1972, Properties of electrotonic junctions between embryonic cells of Fundulus, Dev. Biol. 29:419–435.PubMedGoogle Scholar
  27. Bennett, M. V. L., Feder, N., Reese, T. S., and Stewart, W., 1973, Movement during fixation of peroxidases injected into the crayfish septate axon, J. Gen. Physiol. 61:254–255.Google Scholar
  28. Bennett, M. V. L., Spira, M. E., and Spray, D. C., 1978, Permeability of gap junctions between embryonic cells of Fundulus A reevaluation, Dev. Biol. 65:114–125.PubMedGoogle Scholar
  29. Bennett, M. V. L., Spray, D. C., and Harris, A. L., 1981, Electrical coupling in development, Am. Zool. 21:413–427.Google Scholar
  30. Bennett, M. V. L., Zimering, M. B., Spira, M. E., and Spray, D. C., 1985, Interaction of electrical and chemical synapses, in: Gap Junctions (M. V. L. Bennett and D. C. Spray, eds.), pp. 355– 366, Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.Google Scholar
  31. Berry, M. S., 1972, Electrotonic coupling between identified large cells in the buccal ganglia of Planorbis corneus, J. Exp. Biol. 57:173–185.Google Scholar
  32. Bittner, G. D., 1981, Trophic interactions of CNS giant axons in crayfish, Comp. Biochem. Physiol. 68A:299–306.Google Scholar
  33. Bittner, G. D., and Ballinger, M. L., 1980, Ultrastructural changes at gap junctions between lesioned crayfish axons, Cell Tissue Res. 207:143–153.PubMedGoogle Scholar
  34. Brenowitz, G. L., Collins, W. F., III, and Erulkar, S. D., 1983, Dye and electrical coupling between frog motoneurons, Brain Res. 274:371–375.PubMedGoogle Scholar
  35. Brightman, M. W., and Reese, T. S., 1969, Junctions between intimately apposed cell membranes in the vertebrate brain, J. Cell Biol. 40:648–677.PubMedGoogle Scholar
  36. Brink, P. R., 1983, Effect of deuterium oxide on junctional membrane channel permeability, J. Membr. Biol. 71:79–87.PubMedGoogle Scholar
  37. Brink, P. R., and Barr, L., 1977, The resistance of the septum of the median giant axon of the earthworm, J. Gen. Physiol. 69:517–536.PubMedGoogle Scholar
  38. Brink, P. R., and Dewey, M. M., 1980, Evidence for fixed charge in the nexus, Nature 285:101– 102.PubMedGoogle Scholar
  39. Brink, P. R., and Ramanan, S. V., 1985, A model for the diffusion of fluorescent probes in the septate giant axon of earthworm: Axoplasmic diffusion and junctional membrane permeability, Biophys. J. 48:299–309.PubMedGoogle Scholar
  40. Brink, P. R., Dewey, M. M., Colflesh, D. E., and Kensler, R. W., 1981, Polymorphic nexuses in the earthworm Lumbricus terrestris, J. Ultrastruct. Res. 77:233–240.PubMedGoogle Scholar
  41. Bulloch, A. G. M., and Kater, S. B., 1982, Neurite outgrowth and selection of new electrical connections by adult Helisoma neurons, J. Neurophysiol. 48:569–583.PubMedGoogle Scholar
  42. Carbonetto, S., and Muller, K. J., 1977, A regenerating neurone in the leech can form an electrical synapse on its severed axon segment, Nature 267:450–452.PubMedGoogle Scholar
  43. Carew, T. J., and Kandel, E. R., 1976, Two functional effects of decreased conductance EPSPs: Synaptic augmentation and increased electrotonic coupling, Science 192:150–153.PubMedGoogle Scholar
  44. Cobbett, P., and Hatton, G. I., 1984, Dye coupling in hypothalamic slices: Dependence on in vitro hydration state and osmolality of incubation medium, J. Neurosci. 4:3034–3038. Cohan, C. S., Hadley, R. D., and Kater, S. B., 1983, “Zap axotomy”: Localized fluorescent excitation of single dye-filled neurons induces growth by selective axotomy, Brain Res. 270: 93-101.PubMedGoogle Scholar
  45. Cobbett, P., and Hatton, G. I., 1984, Dye coupling in hypothalamic slices: Dependence on in vitro hydration state and osmolality of incubation medium, J. Neurosci. 4:3034-3038. Cohan, C. S., Hadley, R. D., and Kater, S. B., 1983, “Zap axotomy”: Localized fluorescent excitation of single dye-filled neurons induces growth by selective axotomy, Brain Res. 270: 93–101.PubMedGoogle Scholar
  46. Connors, B. W., Bernardo, L. S., and Prince, D. A., 1983, Coupling between neurons of the developing rat neocortex, J. Neurosci. 3:773–782.PubMedGoogle Scholar
  47. Coombs, J. S., Eccles, J. C., and Fatt, P., 1955, Excitatory synaptic action in motoneurones, J. Physiol. (London) 130:374–395.Google Scholar
  48. Daniel, E. E., Daniel, V. P., Duchon, G., Garfield, R. E., Nichols, M., Malhotra, S. K., and Oki, M., 1976, Is the nexus necessary for cell-to-cell coupling of smooth muscle? J. Membr. Biol. 28:207–239.PubMedGoogle Scholar
  49. Decker, R. S., and Friend, D. S., 1974, Assembly of gap junctions during amphibian neurulation, J. Cell Biol. 62:32–47.PubMedGoogle Scholar
  50. De Mello, W. C., 1982, Changes in cell-to-cell coupling during the cardiac cycle, Physiologist 25:197.Google Scholar
  51. De Mello, W. C., 1984, Modulation of junctional permeability, Fed. Proc. 43:2692–2696.PubMedGoogle Scholar
  52. Detwiler, P. B., and Hodgkin, A. L., 1979, Electrical coupling between cones in turtle retina, J. Physiol. (London) 291:75–100.Google Scholar
  53. Dixon, J. S., and Cronly-Dillon, J. R., 1972, The fine structure of the developing retina in Xenopus laevis, J. Embryol. Exp. Morphol. 28:659–666.PubMedGoogle Scholar
  54. Dowling, J. E., 1968, Synaptic organization of the frog retina: An electron microscopic analysis comparing the retinas of frogs and primates, Proc. R. Soc. London Ser. B 170:205–228.Google Scholar
  55. Edwards, F. R., Redman, S. J., and Walmsley, B., 1976, The effect of polarizing currents on unitary Ia excitatory post-synaptic potentials evoked in spinal motoneurons, J. Physiol. (London) 259:705–723.Google Scholar
  56. Engberg, I., and Marshall, K. C., 1979, Reversal potential for Ia excitatory post synaptic potentials in spinal motoneurons of cats, Neuroscience 4:1583–1591.PubMedGoogle Scholar
  57. Fawcett, D. W., 1961, Intercellular bridges, Exp. Cell Res. Suppl. 8:174–187.Google Scholar
  58. Findlay, I., and Petersen, O. H., 1982, Acetylcholine-evoked uncoupling restricts the passage of Lucifer Yellow between pancreatic acinar cells, Cell Tissue Res. 225:633–638.PubMedGoogle Scholar
  59. Finkel, A. S., and Gage, P. W., 1985, Conventional voltage clamping with two intracellular microelectrodes, in: Voltage and Patch Clamping with Microelectrodes (T. G. Smith, H. Lecar, S. J. Redman, and P. W. Gage, eds.), pp. 47–94, American Physiological Society, Bethesda.Google Scholar
  60. Fulton, B. P., Miledi, R., and Takahashi, T., 1980, Electrical synapses between motoneurons in the spinal cord of the newborn rat, Proc. R. Soc. London Ser. B 208:115–120.Google Scholar
  61. Furshpan, E. J., 1964, “Electrical transmission” at an excitatory synapse in a vertebrate brain, Science 144:878–880.PubMedGoogle Scholar
  62. Furshpan, E. J., and Potter, D. D., 1957, Mechanism of nerve-impulse transmission at a crayfish synapse, Nature 180:342–343.PubMedGoogle Scholar
  63. Furshpan, E. J., and Potter, D. D., 1959, Transmission at the giant motor synapses of the crayfish, J. Physiol. (London) 145:289–325.Google Scholar
  64. Furshpan, E. J., and Potter, D. D., 1968, Low-resistance junctions between cells in embryos and tissue culture, Curr. Top. Dev. Biol. 3:95–127.PubMedGoogle Scholar
  65. Furukawa, T., and Furshpan, E. J., 1963, Two inhibitory mechanisms in the Mauthner neurons of goldfish, J. Neurophysiol. 26:140–176.PubMedGoogle Scholar
  66. Garfield, R. E., Sims, S. M., Kannan, M. S., and Daniel, E. E., 1978, Possible role of gap junctions in activation of myometrium during parturition, Am. J. Physiol. 235:C168–C179.PubMedGoogle Scholar
  67. Getting, P. A., 1974, Modification of neuron properties by electrotonic synapses. I. Input resistance, time constant, and integration, J. Neurophysiol. 37:846–857.PubMedGoogle Scholar
  68. Getting, P. A., and Willows, A. O. D., 1974, Modification of neuron properties by electrotonic synapses. II. Burst formation by electrotonic synapses, J. Neurophysiol. 37:858–868.PubMedGoogle Scholar
  69. Giaume, C., and Kom, H., 1982, Ammonium sulfate induced uncouplings of crayfish septate axons with and without increased junctional resistance, Neuroscience 7:1723–1730.PubMedGoogle Scholar
  70. Giaume, C., and Korn, H., 1983, Biomechanical transmission at the rectifying electrotonic synapse: A voltage-dependent process, Science 220:84–87.PubMedGoogle Scholar
  71. Giaume, C., and Korn, H., 1984, Voltage-dependent dye coupling at a rectifying electrotonic synapse of the crayfish, J. Physiol. (London) 356:151–167.Google Scholar
  72. Giaume, C., Spira, M. E., and Korn, H., 1980, Uncoupling of invertebrate electrotonic synapses by carbon dioxide, Neurosci. Lett. 17:197–202.PubMedGoogle Scholar
  73. Gilula, N. B., 1974, Junctions between cells, in: Cell Communication (R. P. Cox, ed.), pp. 1–29, Wiley, New York.Google Scholar
  74. Gogan, P., Gueritaud, J. P., Horcholle-Bossavit, G., and Tyc-Dumont, S., 1974, Electrotonic coupling between motoneurones in the abducens nucleus of the cat, Exp. Brain Res. 21:139– 154.PubMedGoogle Scholar
  75. Gomez-Ramos, P., and Rodriguez-Echandia, E. L., 1981, Retrograde axonal transport and trans- neuronal transference of horseradish peroxidase in the rat ciliary ganglion, Experientia 37:1337–1339.PubMedGoogle Scholar
  76. Goodenough, O. A., and Gilula, N. B., 1974, The splitting of hepatocyte gap junctions and zonulae occludentes with hypertonic disaccharides, J. Cell Biol. 61:575–590.PubMedGoogle Scholar
  77. Goodman, C. S., and Spitzer, N. C., 1979, Embryonic development of identified neurones: Differentiation from neuroblast to neurone, Nature 280:208–214.PubMedGoogle Scholar
  78. Grace, A. A., and Llinas, R., 1985, Morphological artifacts induced in intracellularly stained neurons by dehydration: Circumvention using rapid dimethyl sulfoxide clearing, Neurosciences 16:461–475.Google Scholar
  79. Gregory, W. A., Hall, D. H., and Bennett, M. V. L., 1984, Ultrastructural studies of membrane specializations in the goldfish preoptic area, Soc. Neurosci. Abstr. 10:1178.Google Scholar
  80. Grinnell, A. D., 1966, A study of the interaction between motoneurons in the frog spinal cord, J. Physiol. (London) 182:612–648.Google Scholar
  81. Gutnick, M. J., and Lobel-Yaakov, R., 1983, Carbon dioxide uncouples dye-coupled neuronal aggregates in neocortical slices, Neurosci. Lett. 42:197–200.PubMedGoogle Scholar
  82. Gutnick, M. J., and Prince, D. A., 1981, Dye coupling and possible electrotonic coupling in the guinea pig neocortical slice, Science 211:67–70.PubMedGoogle Scholar
  83. Gutnick, M. J., Connors, B. W., and Ransom, B. R., 1981, Dye-coupling between glial cells in the guinea pig neocortical slice, Brain Res. 213:486–492.PubMedGoogle Scholar
  84. Gutnick, M. J., Lobel-Yaakov, R., and Rimon, G., 1985, Incidence of neuronal dye-coupling in neocortical slices depends on the plane of section, Neuroscience 15:659–666.PubMedGoogle Scholar
  85. Hadley, R. D., and Kater, S. B., 1983, Competence to form electrical connections is restricted to growing neuntes in the snail, Helisoma, J. Neurosci. 3:924–932.Google Scholar
  86. Hadley, R. D., Bodnar, D. A., and Kater, S. B., 1985, Formation of electrical synapses between isolated, cultured Helisoma neurons requires mutual neurite elongation, J. Neurosci. 5:3145– 3153.PubMedGoogle Scholar
  87. Hanna, R. B., Pappas, G. D., and Bennett, M. V. L., 1984, The fine structure of identified electrotonic synapses following increased coupling resistance, Cell Tissue Res. 235:243– 249.PubMedGoogle Scholar
  88. Harris, A. L., Spray, D. C., and Bennett, M. V. L., 1983, Control of intercellular communication by voltage dependence of gap junctional conductance, J. Neurosci. 3:79–100.PubMedGoogle Scholar
  89. Hertzberg, E. L., Spray, D. C., and Bennett, M. V. L., 1985, Reduction of gap junctional conductance by microinjection of antibodies against the 27-kDa liver gap junction polypeptide, Proc. Natl. Acad. Sci. USA 82:2412–2416.PubMedGoogle Scholar
  90. Hopfield, J. J., and Tank, D. W., 1986, Computing with neural circuits: A model, Science 233:625– 633.PubMedGoogle Scholar
  91. Jaslove, S. W., and Brink, P. R., 1986, The mechanism of rectification at the electrotonic motor giant synapse of the crayfish, Nature 323:63–65.PubMedGoogle Scholar
  92. Johnston, M. F., and Ramon, F., 1981, Electrotonic coupling in internally perfused crayfish segmented axons, J. Physiol. (London) 317:509–518.Google Scholar
  93. Johnston, M. F., and Ramon, F., 1982, Voltage independence of an electrotonic synapse, Biophys. J. 39:115–117.PubMedGoogle Scholar
  94. Kaczmarek, L. K., Finbow, M., Revel, J.-P., and Strumwasser, F., 1979, The morphology and coupling of Aplysia bag cells within the abdominal ganglion and in cell culture, J. Neurobiol. 1:535–550.Google Scholar
  95. Kaneko, A., Nishimura, Y., Tauchi, M., and Shimai, K., 1981, Morphological observation of retinal cells presumably made syncytial by an electrode penetration, J. Neurosci. Methods 4:299–303.PubMedGoogle Scholar
  96. Kanno, Y., and Loewenstein, W. R., 1966, Cell-to-cell passage of large molecules, Nature 212:629–630.PubMedGoogle Scholar
  97. Kater, S. B., 1974, Feeding in Helisoma trivolvis The morphological and physiological bases of a fixed action pattern, Am. Zool. 14:1017–1036.Google Scholar
  98. Kensler, R. W., 1978, An untrastructural study of the nexuses in frog heart, earthworm lateral axon, and Mytilus ABRM, Doctoral dissertation, State University of New York, Stony Brook.Google Scholar
  99. Knowles, W. D., Funch, P. G., and Schwartzkroin, P. A., 1982, Electrotonic and dye coupling in hippocampal CA1 pyramidal cells in vitro, Neuroscience 7:1713–1722.PubMedGoogle Scholar
  100. Korn, H., and Bennett, M. V. L., 1975, Vestibular nystagmus and teleost oculomotor neurons- Functions of electrotonic coupling and dendritic impulse initiation, J. Neurophysiol. 38:430– 451.PubMedGoogle Scholar
  101. Korn, H., and Faber, D. S., 1975, An electrically mediated inhibition in goldfish medulla, J. Neurophysiol. 38:452–471.PubMedGoogle Scholar
  102. Korn, H., Sotelo, C., and Crepel, F., 1973, Electrotonic coupling between neurons in the rat lateral vestibular nucleus, Exp. Brain Res. 16:255–275.PubMedGoogle Scholar
  103. Korn, H., Sotelo, C., and Bennett, M. V. L., 1977, The lateral vestibular nucleus of the toadfish Opanus tau Ultrastructural and electrophysiological observations with special reference to electrotonic transmission, Neuroscience 2:851–884.Google Scholar
  104. Kriebel, M. E., Bennett, M. V. L., Waxman, S. G., and Pappas, G. D., 1969, Oculomotor neurons in fish: Electrotonic coupling with multiple sites of impulse initiation, Science 166:520–524.PubMedGoogle Scholar
  105. Kuhnt, U., Kelly, M. J., and Schaumberg, R., 1979, Transsynaptic transport of Procion Yellow in the central nervous system, Exp. Brain Res. 35:371–385.PubMedGoogle Scholar
  106. Landmesser, L., and Pilar, G., 1970, Selective reinnervation of two cell populations in the adult pigeon ciliary ganglion, J. Physiol. (London) 211:203–216.Google Scholar
  107. Landmesser, L., and Pilar, G., 1972, The onset and development of transmission in the chick ciliary gangion, J. Physiol. (London) 222:691–713.Google Scholar
  108. Lane, J., and Swales, L. S., 1980, Dispersal of junctional particles, not internalization, during the in vivo disappearance of gap junctions, Cell 19:579–586.PubMedGoogle Scholar
  109. Larsen, W. J., Azarnia, R., and Loewenstein, W. R., 1977, Intercellular communication and tissue growth. IX. Junctional membrane structure of hybrids between communication-competent and communication-incompetent cells, J. Membr. Biol. 34:39–54.PubMedGoogle Scholar
  110. Levitan, H., Tauc, L., and Segundo, J. P., 1970, Electrical transmission among neurons in the buccal ganglion of a mollusc., Navanax inermis, J. Gen. Physiol. 55:484–496.Google Scholar
  111. Llinas, R. R., 1973, Discussion, in: Intracellular Staining in Neurobiology (S. B. Kater and C. Nicholson, eds.), pp. 134, 215, Springer-Verlag, Berlin.Google Scholar
  112. Llinas, R. R., 1985, Electrotonic transmission in the mammalian central nervous system, in: Gap Junctions (M. V. L. Bennett and D. C. Spray, eds.), pp. 337–353, Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.Google Scholar
  113. Llinas, R., and Yarom, Y., 1981, Electrophysiology of mammalian inferior olivary neurones in vitro Different types of voltage-dependent ionic conductances, J. Physiol. (London) 315:549– 567.Google Scholar
  114. Llinas, R., and Yarom, Y., 1986, Oscillatory properties of guinea-pig inferior olivary neurones and their pharmacological modulation: An in vitro study, J. Physiol. (London) 376:163–182.Google Scholar
  115. Llinas, R., Baker, R., and Sotelo, C., 1974, Electrotonic coupling between neurons in cat inferior olive, J. Neurophysiol. 37:560–571.PubMedGoogle Scholar
  116. Lo, C. W., and Gilula, N. B., 1979, Gap junctional communication in the post-implantation mouse embryo, Cell 18:411–422.PubMedGoogle Scholar
  117. Loewenstein, W. R., 1979, Junctional intercellular communication and the control of growth, Biochim. Biophys. Acta 560:1–65.PubMedGoogle Scholar
  118. LoPresti, V., Macagno, E. R., and Levinthal, C., 1974, Structure and development of neuronal connections in isogenic organisms: Transient gap junctions between growing optic axons and lamina neuroblasts, Proc. Natl. Acad. Sci. USA 71:1098–1102.PubMedGoogle Scholar
  119. McCarrager, G., and Chase, R., 1985, Quantification of ultrastructural symmetry at molluscan chemical synapses, J. Neurobiol. 16:69–74.PubMedGoogle Scholar
  120. MacVicar, B. A., and Dudek, F. E., 1980, Dye-coupling between CA3 pyramidal cells of the rat hippocampus, Brain Res. 196:494–499.PubMedGoogle Scholar
  121. MacVicar, B. A., and Dudek, F. E., 1981, Electrotonic coupling between pyramidal cells: A direct demonstration in rat hippocampal slices, Science 213:782–785.PubMedGoogle Scholar
  122. Margiotta, J. F., and Walcott, B., 1983, Conductance and dye permeability of a rectifying electrical synapse, Nature 305: 52–55.PubMedGoogle Scholar
  123. Martin, A. R., and Pilar, G., 1963, Dual mode of synaptic transmission in the avian ciliary ganglion, J. Physiol. (London) 168:443–463.Google Scholar
  124. Martin, A. R., and Pilar, G., 1964, An analysis of electrical coupling at synapses in the avian ciliary ganglion, J. Physiol. (London) 171:454–475.Google Scholar
  125. Meszler, R. M., Pappas, G. D., and Bennett, M. V. L., 1972, Morphological demonstration of electrotonic coupling of neurons by way of presynaptic fibers, Brain Res. 37:412–415.Google Scholar
  126. Meyer, D. J., Yancey, S. B., and Revel, J.-P., 1981, Intercellular communication in normal and regenerating rat liver: A quantitative analysis, J. Cell Biol.91:505–523.PubMedGoogle Scholar
  127. Miller, J. P., and Selverston, A. J., 1979, Rapid killing of single neurons by irradiation of intra- cellularly injected dye, Science 206:702–704.PubMedGoogle Scholar
  128. Muller, K. J., and Scott, S. A., 1981, Transmission at a “direct” electrical connexion mediated by an interneurone in the leech, J. Physiol. (London) 311:565–583.Google Scholar
  129. Mulloney, B., 1970, Structure of the giant fibers of earthworms, Science 168:994–996.PubMedGoogle Scholar
  130. Mulloney, B., and Selverston, A., 1972, Antidromic action potentials fail to demonstrate known interactions between neurons, Science 177:69–72.PubMedGoogle Scholar
  131. Murphy, A. D., Hadley, R. D., and Kater, S. B., 1983, Axotomy-induced parallel increases in electrical and dye coupling between identified neurons of Helisoma, J. Neurosci. 3:1422–1429.PubMedGoogle Scholar
  132. Nassel, D. R., 1982, Transneuronal uptake of horseradish peroxidase in the central nervous system of dipterous insects, Cell Tissue Res. 225:639–662.PubMedGoogle Scholar
  133. Neyton, J., and Trautmann, A., 1985, Single-channel currents of an intercellular junction, Nature 317:331–335.PubMedGoogle Scholar
  134. Nicholls, J. G., and Purves, D., 1970, Monosynaptic chemical and electrical connexions between sensory and motor cells in the central nervous system of the leech, J. Physiol. (London) 209:647–667.Google Scholar
  135. Obara, S., 1974, Receptor cell activity at “rest” with respect to the tonic operation of a specialized lateralis receptor, Proc. J. Acad. 50:386–391.Google Scholar
  136. Obara, S., and Oomura, Y., 1973, Disfacilitation as the basis for the sensory suppression in a specialized lateralist receptor of the marine catfish, Proc. J. Acad. 49:213–217.Google Scholar
  137. Pappas, G. D., Asada, Y., and Bennett, M. V. L., 1971, Morphological correlates of increased coupling resistance at an electrotonic synapse, J. Cell Biol. 49:173–188.PubMedGoogle Scholar
  138. Pappas, G. D., Waxman, S. G., and Bennett, M. V. L., 1975, Morphology of spinal electromotor neurons and presynaptic coupling pathways in the gymnotid Sternarchus albifrons, J. Neu- rocytol. 4:469–478.Google Scholar
  139. Payton, B. W., Bennett, M. V. L., and Pappas, G. D., 1969, Permeability and structure of junctional membranes at an electrotonic synapse, Science 166:1641–1643.PubMedGoogle Scholar
  140. Peracchia, C., 1981, Direct communication between axons and sheath glial cells in crayfish, Nature 290:597–598.PubMedGoogle Scholar
  141. Peracchia, C., and Bernardini, G., 1984, Gap junction structure and cell-to-cell coupling regulation: Is there a calmodulin involvement? Fed. Proc. 43:2681–2691.PubMedGoogle Scholar
  142. Peracchia, C., and Dulhunty, A. F., 1976, Low resistance junctions in crayfish, J. Cell Biol. 70:419–439.PubMedGoogle Scholar
  143. Piccolino, M., Neyton, J., Witkovsky, P. and Gerschenfeld, H. M., 1982, γ-Aminobutyric acid antagonists decrease junctional communication between L-horizontal cells of the retina, Proc. Natl. Acad. Sci. USA 79:3671–3675.PubMedGoogle Scholar
  144. Piccolino, M., Neyton, J., and Gerschenfeld, H. M., 1984, Decrease of gap junction permeability induced by dopamine and cyclic adenosine 3’:5’-monophosphate in horizontal cells of turtle retina, J. Neurosci. 4:2477–2488.PubMedGoogle Scholar
  145. Politoff, A. L., 1977, Protein semiconduction: An alternative explanation of electrical coupling, in: Intercellular Communication (W. C. De Mello, ed.), pp. 127–143, Plenum Press, New York.Google Scholar
  146. Politoff, A., Pappas, G. D., and Bennett, M. V. L., 1974, Cobalt ions cross an electrotonic synapse if cytoplasmic concentration is low, Brain Res. 76:343–346.PubMedGoogle Scholar
  147. Powell, S. L., and Westerfield, M., 1984, The absence of specific dye-coupling among frog spinal neurons, Brain Res. 294:9–14.PubMedGoogle Scholar
  148. Rall, W. G., Shepherd, G. M., Reese, T. S., and Brightman, M. W., 1966, Dendrodendritic synaptic pathway for inhibition in the olfactory bulb, Exp. Neurol. 14:44–56.PubMedGoogle Scholar
  149. Raviola, E., and Gilula, N. B., 1973, Gap junctions between photoreceptor cells in the vertebrate retina, Proc. Natl. Acad. Sci. USA 70:1677–1681.PubMedGoogle Scholar
  150. Raviola, E., and Gilula, N. B., 1975, Intramembrane organization of specialized contacts in the outer plexiform layer of the retina: A freeze-fracture study in monkeys and rabbits, J. Cell Biol. 65:192–222.PubMedGoogle Scholar
  151. Rayport, S. G., and Kandel, E. R., 1980, Developmental modulation of an identified electrical synapse: Functional uncoupling, J. Neurophysiol 44:555–567.PubMedGoogle Scholar
  152. Rieske, E., Schubert, P., and Kreutzberg, G. W., 1975, Transfer of radioactive material between electrically coupled neurons of the leech central nervous system, Brain Res. 84:365–382.PubMedGoogle Scholar
  153. Ringham, G. L., 1975, Localization and electrical characteristics of a giant synapse in the spinal cord of the lamprey, J. Physiol. (London) 251:395–407.Google Scholar
  154. Rose, B., and Rick, R., 1978, Intracellular pH, intracellular free Ca, and junctional cell-cell coupling, J. Membr. Biol. 44:377–415.PubMedGoogle Scholar
  155. Rose, B., Simpson, I., and Loewenstein, W. R., 1977, Calcium ion produces graded changes in permeability of membrane channels in cell junctions, Nature 267:625–627.PubMedGoogle Scholar
  156. Schmalbruch, H., and Jahnsen, H., 1981, Gap junctions on CA3 pyramidal cells of guinea pig hippocampus shown by freeze-fracture, Brain Res. 217:175–178.PubMedGoogle Scholar
  157. Schwarzmann, G., Wiegandt, H., Rose, B., Zimmerman, A., Ben-Haim, D., and Loewenstein, W. R., 1981, Diameter of the cell-to-cell junctional membrane channels as probed with neutral molecules, Science 213:551–553.PubMedGoogle Scholar
  158. Shapovalov, A. I., 1980, Interneuronal synapses with electrical, dual and chemical mode of transmission in vertebrates, Neuroscience 5:1113–1124.Google Scholar
  159. Shapovalov, A. I., 1982, Evolution of the mechanisms of connection between neurons: Electrical, mixed and chemical synapses, Neurosci. Behav. Physiol. 12:169–176.PubMedGoogle Scholar
  160. Shapovalov, A. I., and Shiriaev, B. I., 1980, Dual mode of junctional transmission at synapses between single primary afferent fibres and motoneurones in the amphibian, J. Physiol. (London) 306:1–15.Google Scholar
  161. Sheridan, J. D., 1973, Functional evaluation of low resistance junctions: Influence of cell shape and size, Am. Zool. 13:1119–1128.Google Scholar
  162. Silinsky, E. M., 1985, The biophysical pharmacology of calcium-dependent acetylcholine secretion, Pharmocol. Rev. 37:81–132.Google Scholar
  163. Simpson, I., Rose, B., and Loewenstein, W. R., 1977, Size limit of molecules permeating the junctional membrane channels, Science 195:294–296.PubMedGoogle Scholar
  164. Smith, T. G., and Baumann, F., 1969, The functional organization within the ommatidium of the lateral eye of Limulus, Prog. Brain Res. 31:313–349.PubMedGoogle Scholar
  165. Smith, T. G., Baumann, F., and Fuortes, M. G. F., 1965, Electrical connections between visual cells in the ommatidium of Limulus, Science 147:1446–1447.PubMedGoogle Scholar
  166. Smith, T. G., Wuerker, R. B., and Frank, K., 1967, Membrane impedance changes during synaptic transmission in cat spinal motoneurons, J. Neurophysiol. 30:1072–1096.PubMedGoogle Scholar
  167. Socolar, S. J., 1977, The coupling coefficient as an index of junctional conductance, J. Membr. Biol. 34:29–37.PubMedGoogle Scholar
  168. Sotelo, C., and Korn, H., 1978, Morphological correlates of electrical and other interactions through low-resistance pathways between neurons of the vertebrate central nervous system, Int. Rev. Cytol. 55:67–107.PubMedGoogle Scholar
  169. Sotelo, C., and Taxi, J., 1970, Ultrastructural aspects of electrotonic junctions in the spinal cord of the frog, Brain Res. 17:137–141.PubMedGoogle Scholar
  170. Spencer, A. N., and Satterlie, R. A., 1980, Electrical and dye coupling in an identified group of neurons in a coelenterate, J. Neurobiol. 11:13–19.PubMedGoogle Scholar
  171. Spira, M. E., and Bennett, M. V. L., 1972, Synaptic control of electrotonic coupling between neurons, Brain Res. 37:294–300.PubMedGoogle Scholar
  172. Spira, M. E., Spray, D. C., and Bennett, M. V. L., 1976, Electrotonic coupling: Effective sign reversal by inhibitory neurons, Science 194:1065–1067.PubMedGoogle Scholar
  173. Spira, M. E., Spray, D. C., and Bennett, M. V. L., 1980, Synaptic organization of expansion motoneurons of Navanax inermis, Brain Res. 195:241–269.PubMedGoogle Scholar
  174. Spray, D. C., and Bennett, M. V. L., 1985, Physiology and pharmacology of gap junctions, Annu. Rev. Physiol. 47:281–303.PubMedGoogle Scholar
  175. Spray, D. C., Harris, A. L., and Bennett, M. V. L., 1979, Voltage dependence of junctional conductance in early amphibian embryos, Science 204:432–434.PubMedGoogle Scholar
  176. Spray, D. C., Stern, J. H., Harris, A. L., and Bennett, M. V. L., 1982, Gap junctional conductance: Comparison of sensitivities to H and Ca ions, Proc. Natl. Acad. Sci. USA 79:441–445.PubMedGoogle Scholar
  177. Stell, W. K., 1972, The morphological organization of the vertebrate retina, in: Handbook of Sensory Physiology ,Vol. VII/2 (M. G. F. Fuortes, ed.), pp. 111–213, Springer-Verlag, Berlin.Google Scholar
  178. Stewart, W. W., 1978, Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer, Cell 14:741–759.PubMedGoogle Scholar
  179. Stewart, W. W., 1981, Lucifer dyes-Highly fluorescent dyes for biological tracing, Nature 292:17–21.PubMedGoogle Scholar
  180. Strausfeld, N. J., and Obermayer, M., 1976, Resolution of intraneuronal and transynaptic migration of cobalt in the insect visual and central nervous systems, J. Comp. Physiol. 110:1–12.Google Scholar
  181. Taghert, P. H., Bastiani, M. J., Ho, R. K., and Goodman, C. S., 1982, Guidance of pioneer growth cones: Filopodial contacts and coupling revealed with an antibody to Lucifer Yellow, Dev. Biol. 94:391–399.PubMedGoogle Scholar
  182. Tauc, L., 1959, Interaction non synaptique entre deux neurones adjacents du ganglion abdominal de l’aplysie, C.R. Acad. Sci. 248:1857–1859.Google Scholar
  183. Tauc, L., 1969, Polyphasic synaptic activity, Prog. Brain Res. 31:247–257.PubMedGoogle Scholar
  184. Taylor, C. P., and Dudek, F. E., 1982a, A physiological test for electrotonic coupling between CA1 pyramidal cells in rat hippocampal slices, Brain Res. 235:351–357.PubMedGoogle Scholar
  185. Taylor, C. P., and Dudek, F. E., 1982a, A physiological test for electrotonic coupling between CA1 pyramidal cells in rat hippocampal slices, Brain Res. 235:351-357. Taylor, C. P., and Dudek, F. E., 1982b, Synchronous neural afterdischarges in rat hippocampal slices without active chemical synapses, Science 218:810–812.PubMedGoogle Scholar
  186. Taylor, C. P., and Dudek, F. E., 1984, Excitation of hippocampal pyramidal cells by an electrical field effect, J. Neurophysiol. 52:126–142.PubMedGoogle Scholar
  187. Teranishi, T., Negishi, K., and Kato, S., 1983, Dopamine modulates s-potential amplitude and dye-coupling between external horizontal cells in carp retina, Nature 301:243–246.PubMedGoogle Scholar
  188. Traub, R. D., and Pedley, T. A., 1981, Virus-induced electrotonic coupling: Hypothesis on the mechanism of periodic EEG discharges in Creutzfeldt-Jakob disease, Ann. Neurol. 10:405– 410.PubMedGoogle Scholar
  189. Traub, R. D., Dudek, F. E., Taylor, C. P., and Knowles, W. D., 1985, Simulation of hippocampal after discharges synchronized by electrical interactions, Neuroscience 14:1033–1038.PubMedGoogle Scholar
  190. Triller, A., and Korn, H., 1981, Interneuronal transfer of horseradish peroxidase associated with exo/endocytotic activity in adjacent membranes, Exp. Brain Res. 43:233–236.PubMedGoogle Scholar
  191. van Venrooij, G. E. P. M., Hax, W. M. A., Schouten, V. J. A., Denier van der Gon, J. J., and van der Vorst, H. A., 1975, Absence of cell communication for fluorescein and dansylated amino acids in an electrotonic coupled cell system, Biochim. Biophys. Acta 394:620–632.PubMedGoogle Scholar
  192. Verselis, V., and Brink, P. R., 1984, Voltage clamp of the earthworm septum, Biophys. J. 45:147– 150.PubMedGoogle Scholar
  193. Viancour, T. A., Bittner, G. D., and Ballinger, M. L., 1981, Selective transfer of Lucifer Yellow CH from axoplasm to adaxonal glia, Nature 293:65–66.PubMedGoogle Scholar
  194. Warner, A. E., 1973, The electrical properties of the ectoderm in the amphibian embryo during induction and early development of the nervous system, J. Physiol. (London) 235:267– 286.Google Scholar
  195. Warner, A. E., Guthrie, S. C., and Gilula, N. B., 1984, Antibodies to gap-junctional protein selectively disrupt junctional communication in the early amphibian embryo, Nature 311:127– 131.PubMedGoogle Scholar
  196. Watanabe, A., and Bullock, T. H., 1960, Modulation of activity of one neuron by subthreshold slow potentials in another in lobster cardiac ganglion, J. Gen. Physiol. 43:1031–1045.PubMedGoogle Scholar
  197. Watanabe, A., and Grundfest, H., 1961, Impulse propagation at the septal and commissural junctions of crayfish lateral giant axons, J. Gen. Physiol. 45:267–308.PubMedGoogle Scholar
  198. Waxman, S. G., Waxman, M., and Pappas, G. D., 1980, Coordinated micropinocytotic activity of adjacent neuronal membranes in mammalian central nervous system, Neurosci. Lett. 20:141– 146.PubMedGoogle Scholar
  199. Weinstein, J. N., Yoshikami, S., Henkart, P., Blumenthal, R., and Hagins, W. A., 1977, Liposome-cell interactions: Transfer and intracellular release of a trapped fluorescent marker, Science 195:489–491.PubMedGoogle Scholar
  200. Werman, R., and Carlen, P. L., 1976, Unusual behavior of the Ia EPSP in cat spinal motoneurons, Brain Res. 112:395–401.PubMedGoogle Scholar
  201. Westerfield, M., and Frank, E., 1982, Specificity of electrical coupling among neurons innervating forelimb muscles of the adult bullfrog, J. Neurophysiol. 48:904–913.PubMedGoogle Scholar
  202. Williams, E. H., and DeHaan, R. L., 1981, Electrical coupling among heart cells in the absence of ultrastructurally defined gap junctions, J. Membr. Biol. 60:237–248.PubMedGoogle Scholar
  203. Wong, R. K. S., Prince, D. A., and Basbaum, A. I., 1979, Intradendritic recordings from hippocampal neurons, Proc. Natl. Acad. Sci. USA 76:986–990.PubMedGoogle Scholar
  204. Wylie, R. M., 1973, Evidence of electrotonic transmission in the vestibular nuclei of the rat, Brain Res. 50:179–183.PubMedGoogle Scholar
  205. Yarom, Y., and Spira, M. E., 1982, Extracellular potassium ions mediate specific neuronal interaction, Science 216:80–82.PubMedGoogle Scholar
  206. Zampighi, G., Ramon, F., and Duran, W., 1978, Fine structure of the electrotonic synapse of the lateral giant axons in a crayfish (Procambarus clarkii), Tissue Cell 10:413–426.PubMedGoogle Scholar
  207. Zieglgansberger, W., and Reiter, C., 1974, Interneuronal movement of Procion Yellow in cat spinal neurones, Exp. Brain Res. 20:527–530.PubMedGoogle Scholar
  208. Zimmerman A. L., and Rose, B., 1985, Permeability properties of cell-to-cell channels: Kinetics of fluorescent tracer diffusion through a cell junction, J. Membr. Biol. 84:269–283.PubMedGoogle Scholar
  209. Zipser, B., 1979, Voltage-modulated membrane resistance in coupled leech neurons, J. Neu- rophysiol. 42:465–475.Google Scholar

Copyright information

© Plenum Press, New York 1987

Authors and Affiliations

  • Stewart W. Jaslove
    • 1
  • Peter R. Brink
    • 1
  1. 1.Department of Anatomical Sciences, Health Sciences CenterState University of New YorkStony BrookUSA

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