Chloride-cotransport blockade desynchronizes neuronal discharge in the 'epileptic' hippocampal slice

Journal of Neurophysiology

Volumn 83, Issue 1, 2000, Pages 406-417

  Hochman, Daryl W ^a   Schwartzkroin, Philip A ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; BRAIN SLICE; CHLORIDE TRANSPORT; CONTROLLED STUDY; EPILEPTIC DISCHARGE; HIPPOCAMPUS; NERVE CELL; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC TRANSMISSION;

EID: 0033981530     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.2000.83.1.406     Document Type: Article

References (58)

1. ABELES, M., PRUT, Y., BERGMAN, H., AND VAADIA, E. Synchronization in neuronal transmission and its importance for information processing. Prog. Brain Res. 102: 395-404, 1994.
2. ADELMAN, W. J. AND PALTI, Y. The influence of external potassium on the inactivation of sodium currents in the giant axon of the squid. Loligo pealei. J. Gen. Physiol. 53: 685-703, 1969.
3. ANDERSEN, P. Organization of hippocampal neurons and their interconnections. In: The Hippocampus, edited by R. H. Isaacson and K. H. Pribran. New York: Plenum, 1975, vol. 1, p. 155-174.
4. ANDREW, R. D. Seizure and acute osmotic change: clinical and neurophysiological aspects. J. Neural. Sci. 101: 7-18, 1991.
5. BLAND, B. H. AND COLOM, L. V. Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Prog. Neurobiol. 41: 157-208, 1993.
6. BLOCK, S. C. Introduction to Classical and Quantum Harmonic Oscillators. New York: John Wiley, 1997.
7. CHESLER, M. The regulation and modulation of pH in the nervous system. Prog. Neurobiol. 34: 401-427, 1990.
8. CHURCH, J. AND BAIMBRIDGE, K. G. Exposure to high-pH medium increases the incidence and extent of dye coupling between rat hippocampal CA1 neurons in vitro. J. Neurosci. 11: 3289-3295, 1991.
9. + conductance in hippocampus. Nature 389: 286-289, 1997.
10. DIAMOND, J. S. AND JAHR, C. E. Transporters buffer synaptically released glutamate on a submillisecond time scale. J. Neurosci. 17: 4627-4687, 1997.
11. DUDEK. F. E. AND TRAUB, R. D. Local synaptic and electrical interactions in hippocampus: experimental data and computer simulations. In: Neural Models of Plasticity, edited by J. H. Byrne and W. O. Berry. New York: Academic Press, 1989, p. 378-402.
12. FABER, D. S. AND KORN, H. Electrical field effects: their relevance in central neural networks. Physiol. Rev. 69: 821-863, 1989.
13. + modulation of NMDA receptor-mediated EPSCs revealed by carbonic anhydrase inhibition in rat hippocampus. J. Physiol. (Lond.) 478: 373-378, 1994.
14. GROSSMAN, Y., PARNAS, I., AND SPIRA, M. E. Ionic mechanisms involved in differential conduction of action potentials at high frequency in a branching axon. J. Physiol. (Lond.) 295: 307-322, 1979.
15. HOCHMAN, D. W., BARABAN, S. C., OWENS, J.W.M, AND SCHWARTZKROIN, P. A. Dissociation of syncrhonization and excitability in furosemide blockade of epileptiform activity in hippocampal slices. Science 270: 99-102, 1995.
16. HOCHMAN, D. W., D'AMBROSIO, R., JANIGRO, D., AND SCHWARTZKROIN, P. A. Extracellular chloride and the maintenance of spontaneous epileptiform activity in rat hippocampal slices. J. Neurophysiol. 81: 49-59, 1999.
17. HOLTHOFF, K. AND WITTE, O. W. Intrinsic optical signals in rat neocortical slices measured with near-infrared dark-field microscopy reveal changes in extracellular space. J. Neurosci. 16: 2740-2749, 1996.
18. HUERTA, P. T. AND LISMAN, J. E. Bi-directional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron 15: 1053-1063, 1995.
19. HUERTA, P. T. AND LISMAN, J. E. Low-frequency stimulation at the troughs of theta oscillations induces long-term depression of previously potentiated CA1 synapses. J. Neurophysiol. 75: 877-884, 1996.
20. JEFFERYS, J.G.R. Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol. Rev. 75: 689-723, 1995.
21. JEFFERYS, J.G.R. AND HAAS, H. L. Synchronized bursting of CA1 pyramidal cells in the absence of synaptic transmission. Nature 200: 448-450, 1982.
22. + channels and axonal geometry in the gating of action potential propagation along CA3 pyramidal cell axons: a simulation study. J. Neurosci. 18: 7436-7451, 1998.
23. LUSCHER, C., STREIT, J., LIPP, P., AND LUSCHER, H.-R. Action potential propagation through embryonic dorsal root ganglion cells in culture. II. Decrease of conduction reliability during repetitive stimulation. J. Neurophysiol. 72: 634-643, 1994a.
24. LUSCHER, C., STREIT, J., QUADRONI, R., AND LUSCHER, H.-R. Action potential propagation through embryonic dorsal root ganglion cells in culture. I. Influence of the cell morphology on propagation properties. J. Neurophysiol. 72: 622-633, 1994b.
25. MACVICAR, B. A. AND DUDEK, F. E. Electronic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science 213: 782-785, 1981.
26. MACVICAR, B. A. AND HOCHMAN, D. Imaging of synaptically evoked intrinsic optical signals in hippocampal slices. J. Neurosci. 11: 1458-1469, 1991.
27. MALENKA, R. C., KOCSIS, J. D., RANSOM, B. R., AND WAXMAN, S. G. Modulation of parallel fiber excitability by postsynaptically mediated changes in extracellular potassium. Science 214: 339-341, 1981.
28. MCBAIN, C. J., TRAYNELIS, S. F., AND DINGLEDINE, R. Regional variation of extracellular space in the hippocampus. Science 249: 674-677, 1990.
29. MCNAMARA, J. O. Cellular and molecular basis of epilepsy. J. Neurosci. 14: 3413-3425, 1994.
30. MISGELD, U., DIESZ, R. A., DODT, H. U, AND Lux, H. D. The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science 232: 1413-1415, 1986.
31. NEYTON, J. AND TRAUTMANN, A. Single-channel currents of an intercellular junction. Nature 317: 331-335, 1985.
32. NICOLL, R. A. AND ALGER, B. E. Presynaptic inhibition: transmitter and ionic mechanisms. Int. Rev. Neurobiol. 21: 217-258, 1979.
33. NICHOLLS, D. AND ATTWELL, D. The release and uptake of excitatory amino acids. Trends Pharmacol. Sci. 11: 462-468, 1990.
34. O'KEEFE, J. Hippocampus, theta, and spatial memory. Curr. Opin. Neurobiol. 3: 917-924, 1993.
35. OTMAKHOV, N., SHIRKE, A. M., AND MALINOW, R. Measuring the impact of probabilistic transmission on neuronal output. Neuron 10: 1101-1111, 1993.
36. PAPPAS, C. A. AND RANSOM, B. R. Depolarization-induced alkalinization (DIA) in rat hippocampal astrocytes. J. Neurophysiol. 72: 2816-2826, 1994.
37. PARNAS, I. Differential block at high frequency of branches of a single axon innervating two muscles. J. Neurophysiol. 35: 903-914, 1972.
38. PARNAS, I., HOCHSTEIN, S., AND PARNAS, H. Theoretical analysis of parameters leading to frequency modulation along an inhomogeneous axon. J. Neurophysiol. 39: 909-923, 1976.
39. RANSOM, B. R. Glial modulation of neural excitability mediated by extracellular pH: a hypothesis. Prog. Brain Res. 94: 37-46, 1992.
40. RANG, H. P. AND RITCHIE, J. M. On the electrogenic sodium pump in mammalian non-myelinated nerve fibres and its activation by various external cations. J. Physiol. (Lond.) 196: 183-221, 1968.
41. RUSAKOV, D. A. AND KULLMANN, D. M. Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor action. J. Neurosci. 18: 3158-3170, 1998.
42. SHEPHERD, G.M.G. AND HARRIS, K. M. Three-dimensional structure and composition of CA3-CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and campartmentalization. J. Neurosci. 18: 8300-8310, 1998.
43. SCHWARTZKROIN, P. A. Basic mechanisms of epileptogenesis. In: The Treatment of Epilepsy: Principles and Practices, edited by E. Wylie. Philadephia: Lea and Febiger, 1993, p. 83-98.
44. SCHWARTZKROIN, P. A., BARABAN, S. C, AND HOCHMAN, D. W. Osmolarity, ionic flux, and changes in brain excitabilility. Epilepsy Res. 32: 275-285, 1998.
45. SINGER, W. AND GRAY, C. M. Visual feature integration and the temporal correlation hypothesis. Anna. Rev. Neurosci. 18: 555-586, 1995.
46. SMITH, D. O. Mechanisms of action potential propagation failure at sites of axon branching in the crayfish. J. Physiol. (Lond.) 301: 243-259, 1980.
47. STANFORD, I. M., TRAUB, R. D., AND JEFFERYS, J.G.R. Limbic gamma rhythms. II. Synaptic and intrinsic mechanisms underlying spike doublets in oscillating subicular neurons. J. Neurophysiol. 80: 162-171, 1998.
48. TAYLOR, C. P. AND DUDEK, F. E. Synchronous neural afterdischarges in rat hippocampal slices without active chemical synapses. Science 218: 810-812, 1982.
49. THOMPSON, S. M., DEISZ, R. A., AND PRINCE, D. A. Relative contribution of passive equilibrium and active transport to the distribution of chloride in mammalian cortical neurons. J. Neurophysiol. 61: 512-523, 1989.
50. C1 in hippocampal CA3 neurons. J. Neurophysiol. 61: 512-523, 1989.
51. TONG, G. AND JAHR, C. E. Block of glutamate transporters potentiates postsynaptic excitation. Neuron 13: 1195-1203, 1994.
52. TRAUB, R. D. AND JEFFERYS, J.G.R. Are there unifying principles underlying the generation of epileptic afterdischarges in vitro? Prog. Brain Res. 102: 383-394, 1994.
53. TRAUB, R. D. AND MILES, R. Neuronal Networks of the Hippocampus. New York: Cambridge Univ. Press, 1991.
54. WESTRUM, L. E. AND BLACKSTAD T. W. An electron microscopic study of the stratum radiatum of the rat hippocampus (regio superior, CA1) with particular emphasis on synaptology. J. Comp. Neurol. 119: 281-309, 1962.
55. WILLIAMS, J. H. AND KAUER, J. A. Properties of carbachol-induced oscillatory activity in rat hippocampus. J. Neurophysiol. 78: 2631-2640, 1997.
56. WOLOSKER, H., DE SOUZA, D. O., AND DE MEIS, L. Regulation of glutamate transport into synaptic vesicles by chloride and proton gradient. J. Biol. Chem. 271: 11726-11731, 1996.
57. WONG, R. K. AND TRAUB, R. D. Synchronized burst discharge in disinhibited hippocampal slice. I. Initiation in CA2-CA3 region. J. Neurophysiol. 49: 442-458, 1983.
58. ZADOR, A. Impact of synaptic unreliability on the information transmitted by spiking neurons. J. Neurophysiol. 79: 1219-1229, 1998.