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Electric Coupling in Epileptogenesis

  • Chapter
Gap Junctions in the Nervous System

Part of the book series: Neuroscience Intelligence Unit ((NIU.LANDES))

Abstract

One of the hallmarks of epileptiform activity is neural synchrony. There are several putative mechanisms for creating neural synchrony in a neural network including the chemical synaptic actions of decreased inhibition or increased excitation, extracellular ionic and volume shifts, and changes in electric coupling. Electric coupling includes ephaptic electrical field effects and direct interneuronal electrotonic (cable-like) coupling via gap junctions. Electric field coupling is governed by cell morphology, propagation velocity of depolarization waves, the rate of change to the transmembrane voltage, and extracellular resistivity. Such an effect can be approximately represented as a capacitative pathway via the extracellular fields. Gap junctional coupling can be represented by low resistive pathways through the adjacent connexins. ExceHeinnemann llent reviews of electrical interactions between neurons have been published.1–3

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References

  1. Bennett MVL. Electrical transmission: a functional analysis and comparison to chemical transmission. In: Kandel ER, ed. Handbook of Physiology, Section 1: The Nervous System, Vol. 1, Cellular Biology of Neurons, Part 1. Bethesda, Maryland: American Physiology Society, 1977: 357–412.

    Google Scholar 

  2. Korn H, Faber DS. Elictrical interactions between vertebrate neurons:field effects and electrotonic coupling. In: Schmitt FO, Worden FG, eds. The Neurosciences: Fourth Study Program. Cambridge: MIT Press, 1979: 333–358.

    Google Scholar 

  3. Dudek FE, Snow RW, Taylor CP. Role of electrical interactions in synchronization of epileptiform bursts. In: Delgado-Escueta AV, Ward AA Jr, Woodbury DM, Porter RJ, eds. Advances in Neurology, Vol 44. New York: Raven Press, 1986: 593–617.

    Google Scholar 

  4. Jansen BH. “Is it?” and “so what”-a critical view of EEG chaos. In: Duke DW, Pritchard WS, eds. Measuring Chaos in the Human Brain. Singapore, New Jersey, London, Hong Kong: World Scientific, 1991: 83–96.

    Google Scholar 

  5. Babloyantz A, Destexhe A. Low dimensional chaos in an instance of epilepsy. Proc Natl Acad Sci USA 1986; 83: 3513–3517.

    Article  PubMed  CAS  Google Scholar 

  6. Bardakjian BL, El-Sharkawy TY, Diamant NE. Interaction of coupled nonlinear oscillators having different intrinsic resting levels. J Theor Biol 1984; 106: 9–23.

    Article  PubMed  CAS  Google Scholar 

  7. Bortoff A. Propagation of electrical activity in gastrointestinal smooth muscle: the case for propagation by local circuit current flow. J Gastrointest Motil 1991; 3: 57–63.

    Google Scholar 

  8. Sperelakis N. Electrical field model: an alternative mechanism for cell-to-cell propagation in cardiac muscle and smooth muscle. J Gastrointest Motil 1991; 3: 76–84.

    Google Scholar 

  9. Eccles JC. The Physiology of Synapses. New York: Springer-Verlag, 1964: 1–316.

    Book  Google Scholar 

  10. Loewi O. Problems connected with the principle of humoral transmission of nervous impulses. Proc Roy Soc B 1933; 118: 299–316.

    Article  Google Scholar 

  11. Gutnick MJ, Prince DA. Dye coupling and possible electrotonic coupling in the guinea pig neocortical slice. Science 1981; 211: 67–70.

    Article  PubMed  CAS  Google Scholar 

  12. MacVicar BA, Dudek FD. Electrotonic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science 1981; 213: 782–785.

    Article  PubMed  CAS  Google Scholar 

  13. MacVicar BA, Dudek FD. Electrotonic coupling between granule cells of rat dentate gyrus: physiological and anatomical evidence. J Neurophysiol 1982; 47: 579–592.

    PubMed  CAS  Google Scholar 

  14. Knowles WD, Funch PG, Schwartzkroin PA. Electrotonic and dye coupling in hippocampal CA1 pyramidal cells in vitro. Neuroscience 1982; 7: 1713–1722.

    Article  PubMed  CAS  Google Scholar 

  15. Spencer WA, Kandel ER. Electrophysiology of hippocampal neurons. IV. Fast prepotentials. J Neurophysiology 1961; 24: 272–285.

    Google Scholar 

  16. Turner RW, Meyers DER, Barker JL. Fast pre-potential generation in rat hippocampal CA1 neurons. Neuroscience 1993; 53: 949–959.

    Article  PubMed  CAS  Google Scholar 

  17. Andrew RD, Taylor CP, Snow RW et al. Coupling in rat hippocampal slices: dye transfer between CA1 pyramidal cells. Brain Res. 1982; 8: 211–222.

    CAS  Google Scholar 

  18. Katsumaru H, Kosaka T, Heizmann C et al. Gap junctions on GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus (CA1 region). Exp Brain Res 1988; 7: 363–370.

    Google Scholar 

  19. Kosaka T, Neuronal gap junctions in the polymorph layer of the rat dentate gyrus. Brain Res 1984; 47–351.

    Google Scholar 

  20. Michelson HB, Wong RKS. Synchronization of inhibitory neurones in the guinea-pig hippocampus in vitro. J Physiol 1994; 4 (77): 35–45.

    Google Scholar 

  21. Shapovalov AI. Interneuronal synapses with electrical, dual and chemical mode of transmission in vertebrates. Neuroscience 1980; 5: 1113–1124.

    Article  PubMed  CAS  Google Scholar 

  22. Nagy JL, Yamamoto T, Sawchuk MA. et al. Quantitative immunohistochemical and biochemical correlates of connexin43 localization in rat brain. Glia 1992; 51–9.

    Google Scholar 

  23. Murphy TH, Blatter LA, Wier WG et al. Rapid communication between neurons and astrocytes in primary cortical cultures. J Neurosci 1993; 13 (6): 2672–2679.

    PubMed  CAS  Google Scholar 

  24. Charles AC. Glia-neuron intercellular calcium signaling. Dev Neurosci 1994; 16: 196–206.

    Article  PubMed  CAS  Google Scholar 

  25. Naus CCG, Bechberger JF, Paul DL. Gap junction gene expression in human seizure disorder. Exp Neurol 1994; 111: 198–203.

    Article  Google Scholar 

  26. Dermietzel R, Spray DC. Gap junctions in the brain: where, what type, how many and why? Trends Neurosci 1993; 16: 186–192.

    Article  PubMed  CAS  Google Scholar 

  27. Kepler TB, Marder E, Abbott LF. The effect of electrical coupling on the frequency of model neuronal oscillators. Science 1990; 248: 83–85.

    Article  PubMed  CAS  Google Scholar 

  28. Rayport SG, Kandel ER. Epileptogenic agents enhance transmission at an identified weak electrical synapse in aplysia. Science 1981; 213: 462–464.

    Article  PubMed  CAS  Google Scholar 

  29. Baimbridge KG, McLennan PMJ, Church J. Bursting response to currents-evoked depolarization in rat CA1 pyramidal neurons is correlated with lucifer yellow dye coupling but not with the presence of calbindin-D25k. Synapse 1994; 7: 269–277.

    Article  Google Scholar 

  30. Bardakjian BL, Diamant NE. A mapped clock oscillator model for transmembrane electrical rhythmic activity in excitable cells. J Theor Biol 1994; 166: 225–235.

    Article  PubMed  CAS  Google Scholar 

  31. Perez-Velazquez JL, Valiante TA, Carlen PL. Modulation of gap junctional mechanisms during calcium-free induced field burst activity: a possible role of electrotonic coupling in epileptogenesis. J Neuroscience 1994; 14: 4308–4317.

    CAS  Google Scholar 

  32. Taylor CP, Dudek FE. Synchronous neural afterdischarges in rat hippocampal slices without active chemical synapses. Science 1982; 218: 810–812.

    Article  PubMed  CAS  Google Scholar 

  33. Traub RD, Wong RKS. Synaptic mechanisms underlying interictal spike initiation in a hippocampal network. Neurology 1983; 33: 257–266.

    Article  PubMed  CAS  Google Scholar 

  34. Traub RD, Dudek FE, Taylor CP et al. Simulation of hippocampal afterdischarges synchronized by electrical interactions. Neuroscience 1985; 14: 1033–1038.

    Article  PubMed  CAS  Google Scholar 

  35. Traub RD, Dudek FE, Snow RW et al. Computer simulations indicate that electrical field effects contribute to the shape of the epileptiform field potential. Neuroscience 1985; 15: 947–958.

    Article  PubMed  CAS  Google Scholar 

  36. Bardakjian BL, Vigmond EJ. Effects of the propagation velocity of a surface depolarization wave on the extracellular potential of an excitable cell. IEEE Trans Biomed Eng 1994; 41: 432–439.

    Article  PubMed  CAS  Google Scholar 

  37. Dudek FE, Obenaus A, Tasker JG. Osmolality-induced changes in extracellular volume alter epileptiform bursts independent of chemical synapses in the rat: importance of nonsynaptic mechanisms in hippocampal epileptogenesis. Neuroscience 1990; 120: 267–270.

    CAS  Google Scholar 

  38. Andrew RD. Seizure and acute osmotic change: clinical and neurophysiological aspects. J Neurol 1991; 101: 7–18.

    CAS  Google Scholar 

  39. Roper SN, Obenaus A, Dudek FE. Osmolality and nonsynaptic epileptiform bursts in rat CA1 and dentate gyrus. Ann Neurol 1992; 31: 81–85.

    Article  PubMed  CAS  Google Scholar 

  40. Traynelis SF, Dingledine R. Role of extra-cellular space in hyperosmotic suppression of potassium-induced electrographic seizures. J Neurophysiol 1989; 61: 927–938.

    PubMed  CAS  Google Scholar 

  41. Deschenes M, Paradis M, Roy JP et al. Electrophysiology of neurons of lateral thalamic nuclei in cat: resting properties and burst discharges. J Neurophysiol 1984; 51 (6): 1196–1218.

    PubMed  CAS  Google Scholar 

  42. Soltesz I, Bourassa J, Deschenes M. The behaviour of mossy cells of the rat dentate gyrus during theta oscillations in vivo. Neurosci 1993; 57 (3): 555–564.

    Article  CAS  Google Scholar 

  43. MacVicar BA, Tse FW. Local neuronal circuitry underlying cholinergicrhythmical slow activity in CA3 area of rat hippocampal slices. J Physiol (Lond) 1989; 417: 197–212.

    CAS  Google Scholar 

  44. Klink R, Alonso A. Ionic mechanisms for the subthreshold oscillation and differential electroresponsiveness of medial entorhinal cortex layer II neurons. J Neurophysiol 1193; 70: 144–157.

    Google Scholar 

  45. Leung LS, Yim CY. Rhythmic delta-frequency activities in the nucleus accumbens of anesthetized and freely moving rats. Can J Physiol Pharmacol 1993; 71 (5–6): 311–320.

    Article  PubMed  CAS  Google Scholar 

  46. Kayyali H, Durand D. Effects of applied current on epileptiform bursts in vitro. Exp Neurol 1991; 113: 249–254.

    Article  PubMed  CAS  Google Scholar 

  47. Nagakawa M, Durand D. Suppression of spontaneous epileptiform activity with applied currents. Brain Res 1991; 567: 241–247.

    Article  Google Scholar 

  48. Durand D. Electrical stimulation can inhibit sybchronized neuronal activity. Brain Res 1986; 382: 139–144.

    Article  PubMed  CAS  Google Scholar 

  49. Rao G, Barnes CA, McNaughton BL. Occlusion of hippocampal electrical junctions by intracellular calcium injection. Brain Res 1987; 418 (1–2): 267–270.

    Article  Google Scholar 

  50. Miyachi E, KatoC, Nakaki I. Arachidonic acid blocks gap junctions between retinal horizontal cells. Neuro Report 1994; 5 (4): 485–488.

    CAS  Google Scholar 

  51. Bastide B, Herve JC, Deleze J. The uncoupling effect of diacylglycerol and gap junctional communication of mammalian heart cells is independent of protein Kinase C Exp Cell Res 1994; 214: 519–527.

    CAS  Google Scholar 

  52. Lampe, P.D. (1994). Analyzing phorbol ester effects on gap junctional communica-tion: A dramatic inhibition assembly. J Cell Biol 127(6),part 2: 1895–1905.

    Article  Google Scholar 

  53. Spray DC, Harris AL, Bennett MVL. Gap junctional conductance is a simple and sensitive function of intracellular pH. Science 1981; 211: 712–715.

    Article  PubMed  CAS  Google Scholar 

  54. Suppes T, Kriegstein AR, Prince DA. The influence of dopamine on epileptiform burst activity in hippocampal pyramidal neurons. Brain Res 1985; 326: 273–280.

    Article  PubMed  CAS  Google Scholar 

  55. ODonnell P, Grace AA. Dopaminergic modulation of dye coupling between neurons in the core and shell regions of the nucleus accumbens. J Neurosci 1993; 13: 3456–3471.

    CAS  Google Scholar 

  56. McMahon DG. Modulation of electrical synaptic transmission in zebrafish retinal horizontal cells. J Neurosci 1994; 14 (3): 1722–1734.

    PubMed  CAS  Google Scholar 

  57. Lasater EM. Retinal horizontal cell gap junctional conductance is modulated by dopamine through a cAMP-dependent protein kinase. Proc Natl Acad Sci 1987; 84: 7319–7323.

    Article  PubMed  CAS  Google Scholar 

  58. Herreras O, Largo C, Ibarz JM, Somjen GG et al. Role of neuronal synchronizing mechanisms in the propagation of spreading depression in the in vivo hippocampus. J Neurosci 1994; 14 (11): 7087–7098.

    PubMed  CAS  Google Scholar 

  59. Valiante TA, Perez Velazquez JL, Jahromi SS et al. Coupling potentials in CA1 neurons during calcium-free induced field burst activity. J Neurosci 1995; (in press).

    Google Scholar 

  60. Sperelakis N, Mann JE Jr. Evaluation of electrical field changes in the cleft between excitable cells. J Theor Biol 1977; 64: 71–96.

    Article  PubMed  CAS  Google Scholar 

  61. Mann JE Jr, Sperelakis N. Further development of a model for electrical transmission between myocardial cells not connected by low-resistance pathways. J Electrocardiol 1979; 12: 23–33.

    Article  PubMed  Google Scholar 

  62. Hogues H, Leon JL, Roberge FA. A model study of electric field interactions between cardiac myocytes. IEEE Trans Biomed Eng 1992; 39: 1232–1242.

    Article  PubMed  CAS  Google Scholar 

  63. Sperelakis N, Rubio R. Ultrastructural changes produced by hypertonicity in cat cardiac muscle. J Molec Cell Cardiol 1971; 3: 139–156.

    Article  CAS  Google Scholar 

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Authors
  1. Peter L. Carlen
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  2. Jose L. Perez-Velazquez
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  3. Taufik A. Valiante
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  4. Shokrollah S. Jahromi
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  5. Berj L. Bardakjian
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© 1996 Springer-Verlag Berlin Heidelberg

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Carlen, P.L., Perez-Velazquez, J.L., Valiante, T.A., Jahromi, S.S., Bardakjian, B.L. (1996). Electric Coupling in Epileptogenesis. In: Gap Junctions in the Nervous System. Neuroscience Intelligence Unit. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-21935-5_18

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  • DOI: https://doi.org/10.1007/978-3-662-21935-5_18

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-662-21937-9

  • Online ISBN: 978-3-662-21935-5

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