Gap Junctions as Electrical Synapses

  • Michael V. L. Bennett
Part of the Neuroscience Intelligence Unit book series (NIU.LANDES)

Abstract

A synapse can be defined as a specialized site of functional interaction between neurons. By this definition gap junctions form one class of electrical synapse.1 There is another kind of electrical synapse that mediates short latency inhibition of the Mauthner cell of teleost fishes; this form of electrical transmission is not mediated by gap junctions, but involves a different kind of junctional specialization.2 In addition, there probably are electrical effects that occur between closely apposed cells without obvious gap junctions or specialization other than the absence of interposed glia.2,3 Whether these sites are to be considered synapses or incidental or accidental sites of interaction is a matter of opinion. I have no difficulty in using the term electrical synapse only for gap junctions between neurons and not for gap junctions between nonneuronal cells. Admittedly, this terminology leads to different names for gap junctions depending on where they are located, even when they are comprised of the same protein. However, I find less attractive the alternatives of calling the neuronal interactions mediated by gap junctions nonsynaptic or of using synapses to denote the junctions between such cells as hepatocytes. As will be seen below, transmission mediated at electrical synapses of the gap junction type can be very synaptic in its properties.

Keywords

Permeability Dopamine Recombination Propionate Adenosine 

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References

  1. 1.
    Bennett MVL. Electrical transmission: a functional analysis and comparison with chemical transmission. In: Kandel ER, ed. Cellular Biology of Neurons Vol. I, Sec. I, Handbook of Physiology. The Nervous System. Baltimore: Williams and Wilkins, 1977: 357–416.Google Scholar
  2. 2.
    Faber DS, Korn H. Electrical field effects: their relevance in central neural networks. Physiol Rev 1989; 69: 821–63.PubMedGoogle Scholar
  3. 3.
    Jefferys JG. Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol Rev 1995; 75: 689–723.PubMedGoogle Scholar
  4. 4.
    Bennett MVL, Barrio L, Bargiello TA, Spray DC et al. Gap junctions: new tools, new answers, new questions. Neuron 1991; 6: 305–320.PubMedCrossRefGoogle Scholar
  5. 5.
    White TW, Bruzzone R, Paul DL. The connexin family of intercellular channel forming proteins. Kidney Int 1995; 48: 1148–57.PubMedCrossRefGoogle Scholar
  6. 5A.
    Stauffer KA. The gap junction proteins beta 1-connexin (connexin32) and beta 2connexin (connexin26) can form heteromeric hemichannels. J Biol Chem 1995; 270: 6768–6772.PubMedCrossRefGoogle Scholar
  7. 6.
    Fatt P. Biophysics of junctional transmission. Physiol Rev 1954; 34: 674–710.PubMedGoogle Scholar
  8. 7.
    Furshpan EJ, Potter DD. Transmission at the giant motor synapses of the crayfish. J Physiol London 1959; 145: 289–325.PubMedGoogle Scholar
  9. 8.
    Watanabe A. The interaction of elecrical activity among neurons of lobster cardiac ganglion. Japan J Physiol 1958; 8: 305–318.CrossRefGoogle Scholar
  10. 9.
    Bennett MVL, Crain SM, Grundfest H. Electrophysiology of supramedullary neurons in Spheroides maculatus. III. Organization of the supramedullary neurons. J Gen Physiol 1959; 43: 221–250.PubMedCrossRefGoogle Scholar
  11. 10.
    Bennett MVL, Nakajima Y, Pappas GD. Physiology and ultrastructure of electrotonic junctions. I. Supramedullary neurons. J Neurophysiol 1967; 30: 161–179.PubMedGoogle Scholar
  12. 11.
    Barnes TM. OPUS: a growing family of gap junction proteins? Trends Genet 1994; 10: 303–5.PubMedCrossRefGoogle Scholar
  13. 12.
    Bennett MVL. Electric organs. In: Hoar WS, D.J. Randall DJ, eds. Fish Physiology, Vol. 5. New York: Academic Press, 1971: 347–491.Google Scholar
  14. 13.
    Bennett MVL. Neural control of electric organs. In: Ingle D, ed. The Central Nervous System and Fish Behavior. Chicago: Univ. of Chicago Press, 1968: 147–169.Google Scholar
  15. 14.
    Bennett MVL, Nakajima Y, Pappas GD. Physiology and ultrastructure of electrotonic junctions. III. Giant electromotor neurons of Malapterurus electricus. J Neurophysiol 1967; 30: 209–235.PubMedGoogle Scholar
  16. 15.
    Pappas GD, Bennett MVL. Specialized junctions in electrical transmission between neurons. Ann NY Acad Sci 1966; 37: 495–508.CrossRefGoogle Scholar
  17. 16.
    Korn H, Sotelo C, Crepel F. Electronic coupling between neurons in the rat lateral vestibular nucleus. Exp Brain Res 1973; 16: 255–75.PubMedCrossRefGoogle Scholar
  18. 17.
    Baker R, Llinas R. Electrotonic coupling between neurones in the rat mesencephalic nucleus. J Physiol London 1971; 212: 45–63.PubMedGoogle Scholar
  19. 18.
    Hinrichsen CFL, Larramendi LMH. Synapses and cluster formation of the mouse mesencephalic fifth nucleus. Brain Res 1968; 7: 296–299.PubMedCrossRefGoogle Scholar
  20. 19.
    Dani JW, Smith SJ. The triggering of astrocytic calcium waves by NMDA-induced neuronal activation. Ciba Found Symp 1995; 188:195–205; discussion 205–9.Google Scholar
  21. 20.
    Eccles JC. The Physiology of Synapses. Berlin: Springer Verlag, 1964.CrossRefGoogle Scholar
  22. 21.
    Tuttle R, Masuko S, Nakajima Y. Small vesicle bouton synapses on the distal half of the lateral dendrite of the goldfish Mauthner cell: freeze-fracture and thin section study. J Comp Neurol 1987; 265: 254–74.PubMedCrossRefGoogle Scholar
  23. 22.
    Sloper JJ. Gap junctions between dendrites in the primate neocortex. Brain Res 1972; 44: 641–646.PubMedCrossRefGoogle Scholar
  24. 23.
    Pinching AJ, Powell TPS. The neuropil of the glomeruli of the olfactory bulb. J Cell Sci 1971; 9: 347–377.PubMedGoogle Scholar
  25. 24.
    Sotelo C, Llinas R. Specialized membrane junctions between neurons in vertebrate cerebellar cortex. J Cell Biol 1972; 53: 271–289.PubMedCrossRefGoogle Scholar
  26. 25.
    Bennett MVL. Physiology of electrotonic junctions. Ann NY Acad Sci 1966; 37: 509–539.CrossRefGoogle Scholar
  27. 26.
    Bennett MVL, Pappas GD. The electromotor system of the stargazer: a model for integrative actions at electrotonic synapses. J Neurosci 1983; 3: 748–761.PubMedGoogle Scholar
  28. 27.
    Spira ME, Bennett MVL. Synaptic control of electrotonic coupling between neurons. Brain Res 1972; 37: 294–300.PubMedCrossRefGoogle Scholar
  29. 28.
    Llinas R, Baker R, Sotelo C. Electrotonic coupling between neurons in cat inferior olive. J Neurophysiol 1971; 37: 560–571.Google Scholar
  30. 29.
    Korn H, Bennett MVL. Vestibular nystagmus and teleost oculomotor neurons: functions of electrotonic coupling and dendritic impulse initiation. J Neurophysiol 1975; 38: 430–451.PubMedGoogle Scholar
  31. 30.
    Piccolino M, Neyton J, Gerschenfeld HM. Decrease of gap junction permeability induced by dopamine and cyclic adenosine 3’,5’-monophosphate in horizontal cells of turtle retina. J Neurosci 1984; 4: 2477–88.PubMedGoogle Scholar
  32. 31.
    Teranishi T, Negishi K, Kato S. Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature 1983; 301: 243–2466.PubMedCrossRefGoogle Scholar
  33. 32.
    Dowling JE. Retinal neuromodulation: the role of dopamine. Vis Neurosci 1991; 7: 87–97.PubMedCrossRefGoogle Scholar
  34. 33.
    Saez JC, Nairn AC, Czernik AJ et al. Phosphorylation of connexin32, the hepatocyte gap junction protein, by cAMP-dependent protein kinase, protein kinase C and Caz’/ calmodulin-dependent protein kinase II. Eur J Biochem 1990; 192: 263–273.PubMedCrossRefGoogle Scholar
  35. 34.
    Hampson EC, Weiler R, Vaney DI. pH-gated dopaminergic modulation of horizontal cell gap junctions in mammalian retina. Proc R Soc Lond B Biol Sci 1994; 255: 67–72.CrossRefGoogle Scholar
  36. 35.
    Vaney DI. Many diverse types of retinal neurons show tracer coupling when injected with biocytin or neurobiotin. Neurosci Lett 1991; 125: 187–90.PubMedCrossRefGoogle Scholar
  37. 36.
    Peinado A, Yuste R, Katz LC. Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron 1993; 10: 103–14.PubMedCrossRefGoogle Scholar
  38. 37.
    Roerig B, Klausa G, Sutor B. Dye coupling between pyramidal neurons in developing rat prefrontal and frontal cortex is reduced by protein kinase A activation and dopamine. J Neurosci 1995; 15: 7386–400.Google Scholar
  39. 38.
    Pereda AE, Faber DS. Activity-dependent short-term enhancement of intercellular coupling. J Neurosci 1996; 16: 983–92.PubMedGoogle Scholar
  40. 39.
    Hatton GI, Yang QZ. Incidence of neuronal coupling in supraoptic nuclei of virgin and lactating rats: estimation by neurobiotin and lucifer yellow. Brain Res 1994; 650: 63–9.PubMedCrossRefGoogle Scholar
  41. 40.
    Oliveira-Castro GM, Loewenstein WR. Junctional membrane permeability. Effects of divalent cations. J Membrane Biol 1971; 5: 51–77.CrossRefGoogle Scholar
  42. 41.
    Sanderson MJ. Intercellular calcium waves mediated by inositol trisphosphate. Ciba Found Symp 1995; 188:175–89, discussion 189–94.Google Scholar
  43. 42.
    Asada Y, Bennett MVL. Experimental alteration of coupling resistance at an electrotonic synapse. J Cell Biol 1971; 49: 159–172.PubMedCrossRefGoogle Scholar
  44. 43.
    Pappas GD, Asada Y, Bennett MVL. Morphological correlates of increased coupling resistance at an electrotonic synapse. J Cell Biol 1971; 49: 173–188.PubMedCrossRefGoogle Scholar
  45. 44.
    Turin L, Warner A. Carbon dioxide reversibly abolishes ionic communication between cells of early amphibian embryo. Nature 1977; 270: 56–7.PubMedCrossRefGoogle Scholar
  46. 45.
    Spray DC, Harris AL, Bennett MVL. Gap junctional conductance is a simple and sensitive function of intracellular pH. Science 1981; 211: 712–715.PubMedCrossRefGoogle Scholar
  47. 46.
    Blackshaw SE, Warner AE. Alterations in resting membrane properties during neural plate stages of development of the nervous system. J Physiol London 1976; 255: 231–47.PubMedGoogle Scholar
  48. 47.
    Ek JF, Delmar M, Perzova R et al. Role of histidine 95 on pH gating of the cardiac gap junction protein connexin43. Circ Res 1994; 74: 1058–64.PubMedCrossRefGoogle Scholar
  49. 48.
    Johnston MF, Simon SA, Ramon F. Interaction of anaesthetics with electrical synapses. Nature 1980; 286: 498–500.PubMedCrossRefGoogle Scholar
  50. 49.
    Burt JM, Spray DC. Volatile anesthetics block intercellular communication between neonatal rat myocardial cells. Circ Res 1989; 65: 829–37.PubMedCrossRefGoogle Scholar
  51. 50.
    Reaume AG, de Sousa PA, Kulkarni S et al. Cardiac malformation in neonatal mice lacking connexin43. Science 1995; 267: 1831–4.PubMedCrossRefGoogle Scholar
  52. 51.
    Moore LK, Burt JM. Selective block of gap junction channel expression with connexinspecific antisense oligodeoxynucleotides. Am J Physiol 1994; 267: C1371–80.PubMedGoogle Scholar
  53. 52.
    Meyer RA, Laird DW, Revel JP et al. Inhibition of gap junction and adherens junction assembly by connexin and A-CAM antibodies. J Cell Biol 1992; 119: 179–89.PubMedCrossRefGoogle Scholar
  54. 53.
    Spray DC, Harris AL, Bennett MVL. Voltage dependence of junctional conductance in early amphibian embryos. Science 1979; 204: 432–434.PubMedCrossRefGoogle Scholar
  55. 54.
    Auerbach AA, Bennett MVL. A rectifying synapse in the central nervous system of a vertebrate. J Gen Physiol 1969; 53: 211–237.PubMedCrossRefGoogle Scholar
  56. 55.
    Hall DH, Gilat E, Bennett MVL. Ultra-structure of the rectifying (electrical) synapses between giant fibers and pectoral fin adductor motoneurons in the hatchetfish. J Neurocytol 1985; 14: 825–834.PubMedCrossRefGoogle Scholar
  57. 56.
    Verselis VK, Bennett MVL, Bargiello TA. A voltage dependent gap junction in Drosophila ntelanogaster. Biophys J 1991; 59: 114–126.PubMedCrossRefGoogle Scholar
  58. 57.
    Verselis VK, Ginter CS, Bargiello TA. Opposite voltage gating polarities of two closely related connexins. Nature 1994; 368: 348–51.PubMedCrossRefGoogle Scholar
  59. 58.
    Bennett MVL, Verselis VK, White RL et al. Gap junctional conductance: gating. In: Hertzberg EL, Johnson R eds. Gap Junctions. New York: Alan Liss, Inc., 1988: 287–304.Google Scholar
  60. 59.
    Knier J, Verselis VK, Spray DC et al. Gap junctions between tunicate blastomeres: gating similarities and differences compared to amphibia. Biophys J 1986; 49: 203a.Google Scholar
  61. 60.
    Harris AL, Spray DC, Bennett MVL. Control of intercellular communication by voltage dependence of gap junctional conductance. J Neurosci 1983; 3: 79–100.PubMedGoogle Scholar
  62. 61.
    Chang M, Dahl C, Werner R. Is the role of connexin33 an inhibitory one? Biophys J 1994; 66: A20.Google Scholar
  63. 62.
    Reed KE, Westphale EM, Larson DM et al. Molecular cloning and functional expression of human connexin37, an endothelial cell gap junction protein. J Clin Invest 1993; 91: 997–1004.PubMedCrossRefGoogle Scholar
  64. 63.
    Gouger JA, Paul DL. Expression of gap junction proteins Cx26, Cx31.1, Cx37, and Cx43 in developing and mature rat epidermis. Dev Dyn 1994; 200: 1–13.CrossRefGoogle Scholar
  65. 64.
    Barrio LC, Suchyna T, Bargiello TA et al. Gap junctions formed by connexin26 and 32 alone and in combination are differently affected by applied voltage. Proc Natl Acad Sci USA 1991; 88: 8410–8414.PubMedCrossRefGoogle Scholar
  66. 65.
    Trexler EB, Bennett MVL, Bargiello TA et al. Voltage gating and permeation in a gap junction hemichannel. Proc Natl Acad Sci USA 1996; 93: in press.Google Scholar
  67. 66.
    Perez-Armendariz EM, Romano M, Luna J et al. Characterization of gap junctions between pairs of Leydig cells from mouse testis. Amer J Physiol 1994; 267: C570–0580.PubMedGoogle Scholar
  68. 67.
    Moreno AP, Rook MB, Fishman GI et al. Gap junction channels: distinct voltage-sensitive and -insensitive conductance states. Biophys J 1994; 67: 113–119.PubMedCrossRefGoogle Scholar
  69. 68.
    Bukauskas FF, Elfgang C, Willecke K et al. Heterotypic gap junction channels (connexi n26-connexin32) violate the paradigm of unitary conductance. Pflugers Arch 1995; 429: 870–2.PubMedCrossRefGoogle Scholar
  70. 69.
    Valiante TA, Perez Velazquez JL, Jahromi SS et al. Coupling potentials in CA1 neurons during calcium-free-induced field burst activity. J Neurosci 1995; 15: 6946–56.PubMedGoogle Scholar
  71. 70.
    Bennett MVL. Nicked by Occam’s razor: unitarianism in the investigation of synaptic transmission. Biol Bull 1985; 168 (Suppl.): 159–167.CrossRefGoogle Scholar
  72. 71.
    White TW, Paul DL, Goodenough DA et al. Functional analysis of selective interactions among rodent connexins. Mol Biol Cell 1995; 6: 459–70.PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 1996

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  • Michael V. L. Bennett

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