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Intracellular Cl Regulation and Synaptic Inhibition in Vertebrate and Invertebrate Neurons

  • Francisco J. Alvarez-Leefmans

Abstract

Cl movements across plasma membrane channels and carriers play a central role in a number of mechanisms essential for neuronal function and survival. These include regulation and maintenance of intracellular pH (Boron, 1983; Thomas, 1984; see Russell and Boron, this volume), regulation and maintenance of cell volume (Ballanyi and Grafe, 1988; see Chapter 2, this volume), and modulation of neuronal excitability through anion channels activated by inhibitory neurotransmitters (Alger, 1985; Barker, 1985; Roberts, 1986; Siggins-Gruol, 1986), intracellular Ca2+ (see Mayer et al.,this volume), or transmembrane voltage (see Chesnoy-Marchais, this volume). Furthermore, Cl has recently been shown to exert modulatory effects on G proteins (Deterre et al., 1983; Higashijima et al., 1987). The latter are known to be an essential part of the intracellular messenger machinery coupling receptor binding of neurotransmitters (or hormones) to their specific cell responses. All the above considerations make evident the importance of understanding the mechanisms by which Cl is regulated and maintained in nerve cells. Given the wide spectrum of the subjects involved, the present account will be confined to considering Cl regulation in relation to inhibitory neurotransmitter actions.

Keywords

Presynaptic Inhibition Dorsal Root Ganglion Cell Synaptic Inhibition Squid Giant Axon Primary Afferent Depolarization 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Aickin, C. C., Deisz, R. A., and Lux, H. D., 1982, Ammonium action on postsynaptic inhibition in crayfish neurones: Implications for the mechanism of chloride extrusion, J. Physiol. (London) 329:319–339.Google Scholar
  2. Aickin, C. C., Deisz, R. A., and Lux, H. D., 1984, Mechanisms of chloride transport in crayfish stretch receptor neurones and guinea pig vas deferens: Implications for inhibition mediated by GABA, Neurosci. Lett. 97: 239–244.CrossRefGoogle Scholar
  3. Akaike, N., Hattori, K., Inomata, N., and Oomura, Y., 1985, y-Aminobutyric-acid-and pentobarbitonegated chloride currents in internally perfused frog sensory neurones, J. Physiol. (London) 360: 367–386.Google Scholar
  4. Alger, B. E., 1985, GABA and glycine: Postsynaptic actions, in: Neurotransmitter Actions in the Vertebrate Nervous System ( M. A. Rogawski and J. L. Barker, eds.), pp. 33–69, Plenum Press, New York.CrossRefGoogle Scholar
  5. Alger, B. E., and Nicoll, R. A., 1982, Pharmacological evidence for two kinds of GABA receptor on rat hippocampal pyramidal cells studied in vitro, J. Physiol. (London) 328: 125–141.Google Scholar
  6. Alger, B. E., and Nicoll, R. A., 1983, Ammonia does not selectively block IPSPs in rat hippocampal pyramidal cells, J. Neurophysiol. 49: 1381–1391.PubMedGoogle Scholar
  7. Allakhverdov, B. L., Burovina, I. V., Chmykhova, N. M., and Shapovalov, A. I., 1980, Electron probe x-ray microanalysis of intracellular sodium, potassium and chlorine contents in amphibian motoneurones, Neuroscience 5: 2023–2031.PubMedCrossRefGoogle Scholar
  8. Allen, G. I., Eccles, J., Nicoll, R. A., Oshima, T., and Rubia, F. J., 1977, The ionic mechanisms concerned in generating the IPSPs of hippocampal pyramidal cells, Proc. R. Soc. London Ser. B 198: 363–384.CrossRefGoogle Scholar
  9. Altamirano, A. A., and Russell, J. M., 1987, Coupled Na/K/Cl efflux. “Reverse” unidirectional fluxes in squid giant axons, J. Gen. Physiol. 89: 669–686.PubMedCrossRefGoogle Scholar
  10. Altamirano, A. A., Breitwieser, G. E., and Russell, J. M., 1989, Na+,K+,Cl- coupled transport in squid axon, Acta Physiol. Scand. 136 (Suppl. 582): 16.Google Scholar
  11. Alvarez-Leefmans, F. J., and Noguerdn, I., 1989, Intracellular chloride homeostasis in vertebrate nerve cells, Acta Physiol. Scand. 136(Suppl. 582):17.Google Scholar
  12. Alvarez-Leefmans, F. J., Gamino, S. M., and Giraldez, F., 1986, Direct demonstration that chloride ions are not passively distributed across the membrane of dorsal root ganglion cells of the frog: Preliminary studies on the nature of the chloride pump, Biophys. J. 49: 413a.Google Scholar
  13. Alvarez-Leefmans, F. J., Giraldez, F., and Gamino, S. M., 1987, Intracellular chloride regulation in vertebrate sensory neurones, Neuroscience 22 (Suppl.): 5200.Google Scholar
  14. Alvarez-Leefmans, F. J., Gamino, S. M., Giraldez, F., and Nogueron, I., 1988, Intracellular chloride regulation in amphibian dorsal root ganglion neurones studied with ion-selective microelectrodes, J. Physiol. (London) 406: 225–246.Google Scholar
  15. Andersen, P., Dingledine, R., Gjerstad, L., Langmoen, 1. A., and Laursen, A., 1980, Two different responses of hippocampal pyramidal cells to application of gamma-amino butyric acid, J. Physiol. (London) 305: 279–296.Google Scholar
  16. Ascher, P., Kunze, D., and Neild, T. O., 1976, Chloride distribution in Aplysia neurons, J. Physiol. (London) 256: 441–464.Google Scholar
  17. Ballanyi, K., and Grafe, P., 1985, An intracellular analysis of y-aminobutyric-acid-associated ion movements in rat sympathetic neurons, J. Physiol. (London) 365: 41–58.Google Scholar
  18. Ballanyi, K., and Grafe, P., 1988, Cell volume regulation in the nervous system, Renal Physiol. Biochem. 3–5: 142–157.Google Scholar
  19. Ballanyi, K., Grafe, P., Reddy, M. M., and Ten Bruggencate, G., 1984, Different types of potassium transport linked to carbachol and y-aminobutyric acid actions in rat sympathetic neurons, Neuroscience 12: 917–927.PubMedCrossRefGoogle Scholar
  20. Barker, J. L., 1985, GABA and glycine: Ion channel mechanisms, in: Neurotransmitter Actions in the Vertebrate Nervous System ( M. A. Rogawski and J. L. Barker, eds.), pp. 71–100, Plenum Press, New York.CrossRefGoogle Scholar
  21. Barker, J. L., and Nicoll, R. A., 1972, Gamma-aminobutyric acid. Role in primary afferent depolarization, Science 176: 1043–1045.PubMedCrossRefGoogle Scholar
  22. Barker, J. L., and Nicoll, R. A. 1973, The pharmacology and ionic dependency of amino acid responses in the frog spinal cord, J. Physiol. (London) 228: 259–277.Google Scholar
  23. Barker, J. L., and Ransom, B. R., 1978, Amino acid pharmacology of mammalian central neurones grown in tissue culture, J. Physiol. (London) 280: 331–354.Google Scholar
  24. Barker, J. L., Nicoll, R. A., and Padjen, A., 1975, Studies on convulsants in the isolated frog spinal cord. I. Antagonism of amino acid responses, J. Physiol. (London) 245: 521–536.Google Scholar
  25. Ben-Art, Y., Krnjevié, K., and Reinhardt, W., 1979, Hippocampal seizures and failure of inhibition, Can. J. Physiol. Pharmacol. 57: I462–1466.Google Scholar
  26. Benninger, C., Kadis, J., and Prince, D. A., 1980, Extracellular calcium and potassium change; in hippocampal slices, Brain Res. 187: 165–182.PubMedCrossRefGoogle Scholar
  27. Boistel, J., and Fatt, P., 1958, Membrane permeability change during inhibitory transmitter action in crustacean muscle, J. Physiol. (London) 144: 176–191.Google Scholar
  28. Bolz, J., and Gilbert, C. D., 1986, Generation of end-inhibition in the visual cortex via interlaminar connections, Nature 320: 362–364.PubMedCrossRefGoogle Scholar
  29. Bormann, J., Hamill, O. P., and Sakmann, B., 1987, Mechanism of anion permeation through channels gated by glycine and -y-aminobutyric acid in mouse cultured spinal neurones, J. Physiol. (London) 385: 243–286.Google Scholar
  30. Boron, W. F., 1983, Transport of H+ and of ionic weak acids and bases, J. Membr. Biol. 72: 1–16.PubMedCrossRefGoogle Scholar
  31. Boron, W. F., 1985, Intracellular pH-regulating mechanism of the squid axon, J. Gen. Phy.siol. 85: 325–345.Google Scholar
  32. Boron, W. F., and De Weer, P., 1976, Intracellular pH transients in squid giant axons caused by CO2, NH3 and metabolic inhibitors, J. Gen. Physiol. 67: 91–112.PubMedCrossRefGoogle Scholar
  33. Boron, W. F., and Russell, J. M., 1983, Stoichiometry and ion dependencies of the intracellular-pHregulating mechanism in squid giant axons, J. Gen. Physiol. 81: 373–399.PubMedCrossRefGoogle Scholar
  34. Boron, W. F., Russell, J. M., Brodwick, M. S., Keifer, D. W., and Roos, A., 1978, Influence of cyclic AMP on intracellular pH regulation and chloride fluxes in barnacle muscle fibers, Nature 276: 511–513.PubMedCrossRefGoogle Scholar
  35. Bowery, N. G., Hill, D. R., Hudson, A. L., Price, G. W., Turnbull, M. J., and Wilkin, G. P., 1984, Heterogeneity of mammalian GABA receptors, in: Actions and Interactions of GABA and Benzodiazepines ( N. G. Bowery, ed.), pp. 81–108, Raven Press, New York.Google Scholar
  36. Brazy, P., and Gunn, R. B., 1976, Furosemide inhibition of CI transport in human red blood cells, J. Gen. Physiol. 68: 583–599.PubMedCrossRefGoogle Scholar
  37. Brown, A. M., and Kunze, D. L., 1974, Ionic activities in identifiable Aplysia neurons, in: Ion-Selective Microelectrodes ( H. J. Berman and N. C. Hebert, eds.), pp. 57–73, Plenum Press, New York.CrossRefGoogle Scholar
  38. Brown, A. M., Walker, J. L., and Sutton, R. B., 1970, Increased chloride conductance as the proximate cause of hydrogen ion concentration effects in Aplysia neurons, J. Gen. Physiol. 56: 559–582.PubMedCrossRefGoogle Scholar
  39. Brown, H. M., Ottoson, D., and Rydquist, B., 1978, Crayfish stretch receptor: An investigation with voltage-clamp and ion-sensitive electrodes, J. Physiol. (London) 284: 155–180.Google Scholar
  40. Brown, T. H., Perkel, D. H., Norris, J. C., and Peacock, J. N., 1981, Electrotonic structure and specific membrane properties of mouse dorsal root ganglion neurons, J. Neurophysiol. 45: 1–15.PubMedGoogle Scholar
  41. Brugnara, C., Thuong, V. H., and Tosteson, D. C., 1989, Role of chloride in potassium transport through a K-Cl cotransport system in human red blood cells, Am. J. Physiol. 256: 994–1003.Google Scholar
  42. Bührle, C. P., and Sonnhof, U., 1983, Intracellular ion activities and equilibrium potentials in motoneurones and glia cells of the frog spinal cord, Pfluegers Arch. 396: 144–153.CrossRefGoogle Scholar
  43. Bührle, C. P., and Sonnhof, U., 1985, The ionic mechanism of postsynaptic inhibition in motoneurons of the frog spinal cord, Neuroscience 14: 581–592.PubMedCrossRefGoogle Scholar
  44. Burke, R. E., and Rudomin, P., 1977, Spinal neurons and synapses, in: Handbook of Physiology, Section 1, The Nervous System, Volume 1, Cellular Biology of Neurons, Part 2 ( E. R. Kandel, ed.), pp. 877–944, American Physiological Society, Bethesda.Google Scholar
  45. Cherksey, B. D., and Zeuthen, T., 1987, A membrane protein with a K+ and a Cl- channel, Act Physiol. Scand. 129: 137–138.Google Scholar
  46. Chester, M., 1986, Regulation of intracellular pH in reticulospinal neurones of the lamprey, Petromyzon marinus, J. Physiol. (London) 381: 241–261.Google Scholar
  47. Chesler, M., 1987, pH regulation in the vertebrate central nervous system: Microelectrode studies in the brain stem of the lamprey, Can. J. Physiol. Pharmacol. 65: 986–993.Google Scholar
  48. Chipperfield, A. R., 1986, The (Na+-K+ -Cl) cotransport system, Clin. Sci. 71: 465–467.PubMedGoogle Scholar
  49. Connors, B. W., Malenka, R. C., and Silva, L. R., 1988, Two inhibitory postsynaptic potentials and GABAA and GABAB receptor-mediated responses in neocortex of rat and cat, J. Physiol. (London) 406: 443–468.Google Scholar
  50. Constanti, A., and Nistri, A., 1976, A comparative study of the action of y-aminobutyric acid and piperazine on the lobster muscle fiber and the spinal cord, Br. J. Pharmacol. 57: 347–358.PubMedCrossRefGoogle Scholar
  51. Coombs, J. S., Eccles, J. C., and Fatt, P., 1955, The specific ionic conductances and the ionic movements across the motoneuronal membrane that produce the inhibitory postsynaptic potential, J. Physiol. (London) 130: 326–373.Google Scholar
  52. Corcia, A., and Armstrong, W. M., 1983, KCI cotransport: A mechanism for basolateral chloride exit in Necturus gallbladder, J. Membr. Biol. 76: 173–182.PubMedCrossRefGoogle Scholar
  53. Cornwall, M. C., Peterson, D. F., Kunze, D. L., Walker, J. L., and Brown, A. M., 1970, Intracellular potassium and chloride activities measured with liquid ion exchanger microelectrodes, Brain Res. 23: 433–436.PubMedCrossRefGoogle Scholar
  54. Curtis, D. R., Phillis, J. W., and Watkins, J. C., 1961, Actions of amino acids on the isolated hemisected spinal cord of the toad, Br. J. Pharmacol. Chemother. 16: 262–283.PubMedCrossRefGoogle Scholar
  55. Davidoff, R. A., and Hackman, J. C., 1984, Spinal inhibition, in: Handbook of the Spinal Cord, Volume 2, Anatomy and Physiology of the Spinal Cord, ( R. A. Davidoff, ed.), pp. 385–459, Dekker, New York.Google Scholar
  56. Davidoff, R. A., and Hackman, J. C., 1985, GABA: Presynaptic actions, in: Neurotransmitter Actions in the Vertebrate Nervous System ( M. A. Rogawski and J. L. Barker, eds.), pp. 3–32, Plenum Press, New York.CrossRefGoogle Scholar
  57. DeGroat, W. C., 1972, GABA-depolarization of a sensory ganglion: Antagonism by picrotoxin and bicuculline, Brain Res. 38: 429–439.CrossRefGoogle Scholar
  58. Deisz, R. A., and Lux, H. D., 1982, The role of intracellular chloride in hyperpolarizing postsynaptic inhibition of crayfish stretch receptor neurones, J. Physiol. (London) 326: 123–138.Google Scholar
  59. Desarmenien, M., Feltz, P., Occhipinti, G., Santangelo, F., and Schlichter, R., 1984, Coexistence of GABAA and GABA13 receptors on A and C primary afferents, Br. J. Pharmacol. 81: 327–333.PubMedCrossRefGoogle Scholar
  60. Deschenes, M., Feltz, P., and Lamour, Y., 1976, A model for an estimate in vivo of the ionic basis of presynaptic inhibition: An intracellular analysis of the GABA-induced depolarization in rat dorsal root ganglia, Brain Res. 118: 486–493.PubMedCrossRefGoogle Scholar
  61. Deterre, P., Gozlan, H., and Bockaert, J., 1983, GTP-dependent anion-sensitive adenylate cyclase in snail ganglia potentiation of neurotransmitter effects, J. Biol. Chem. 258: 1467–1473.PubMedGoogle Scholar
  62. Dingledine, R., and Langmoen, I. A., 1980, Conductance changes and inhibitory actions of hippocampal recurrent IPSPs, Brain Res. 185: 277–287.PubMedCrossRefGoogle Scholar
  63. Dykes, R. W., Landry, P., Metherate, R., and Hicks, T. P., 1984, Functional role of GABA in cat primary somatosensory cortex: Shaping receptive fields of cortical neurons, J. Neurophysiol. 52: 1066–1093.PubMedGoogle Scholar
  64. Eccles, J. C., 1957, The Physiology of Nerve Cells, Johns Hopkins Press, Baltimore.Google Scholar
  65. Eccles, J. C., 1964a, The Physiology of Synapses, Springer, Berlin.CrossRefGoogle Scholar
  66. Eccles, J. C., 1964b, Presynaptic inhibition in the spinal cord, Prog. Brain Res. 12: 65–89.CrossRefGoogle Scholar
  67. Eccles, J. C., 1969, The Inhibitory Pathways of the Central Nervous System, Thomas, Springfield, Ill.Google Scholar
  68. Eccles, J. C., Eccles, R. M., and Ito, M., 1964a, Effects of intracellular potassium and sodium injection on the inhibitory postsynaptic potential, Proc. R. Soc. London Ser. B 160: 181–196.CrossRefGoogle Scholar
  69. Eccles, J. C., Eccles, R. M., and Ito, M., 1964b, Effects produced on inhibitory postsynaptic potentials by the coupled injections of cations and anions into motoneurones, Proc. R. Soc. London Ser. B 160: 197–210.CrossRefGoogle Scholar
  70. Eccles, J., Nicoll, R. A., Oshima, T., and Rubia, F. J., 1977, The anionic permeability of the inhibitory postsynaptic membrane of hippocampal pyramidal cells, Proc. R. Soc. London Ser. B 198: 345–361.CrossRefGoogle Scholar
  71. Edwards, C., 1982, The selectivity of ion channels in nerve and muscles, Neuroscience 7: 1355–1366.CrossRefGoogle Scholar
  72. Ellory, J. C., and Stewart, G. W., 1982, The human erythrocyte Cl--dependent Na—K cotransport system as a possible model for studying the action of loop diuretics, Br. J. Pharmacol. 75: 183–188.PubMedCrossRefGoogle Scholar
  73. Ellory, J. C., Dunham, P. B., Logue, P. J., and Stewart, G. W., 1982, Anion-dependent cation transport in erythrocytes, Philos. Trans. R. Soc. London Ser. B 299: 483–495.CrossRefGoogle Scholar
  74. Fatt, P., 1974, Postsynaptic cell characteristics determining membrane potential changes, in: Lecture Notes in Biomathematics, Volume 4, Physics and Mathematics of the Nervous System ( M. Conrad, W. Göttinger, and M. Dal Cin, eds.), pp. 150–170, Springer-Verlag, Berlin.Google Scholar
  75. Feltz, P., and Rasminsky, M., 1974, A model for the mode of action of GABA on primary afferent terminals: Depolarizing effects of GABA applied iontophoretically to neurones of mammalian dorsal root ganglia, Neuropharmacology 13: 553–563.PubMedCrossRefGoogle Scholar
  76. Forsythe, I. D., and Redman, S. J., 1988, The dependence of motoneuron membrane potential on extra-cellular ion concentrations studied in isolated rat spinal cord, J. Physiol. (London) 404: 83–99.Google Scholar
  77. Frank, K., and Fuortes, M. G. F., 1957, Presynaptic and postsynaptic inhibition of monosynaptic reflexes, Fed. Proc. 16: 39–40.Google Scholar
  78. Gallagher, J. P., Higashi, H., and Nishi, S., 1978, Characterization and ionic basis of GABA-induced depolarizations recorded in vitro from cat primary afferent neurones, J. Physiol. (London) 275: 263282.Google Scholar
  79. Gallagher, J. P., Nakamura, J., and Shinnick-Gallagher, P., 1983, The effects of temperature, pH and CI—pump inhibitors on GABA responses recorded from cat dorsal root ganglia, Brain Res. 267: 249–259.PubMedCrossRefGoogle Scholar
  80. Galvan, M., Dörge, A., Beck, F., and Rick, R., 1984, Intracellular electrolyte concentrations in rat sympathetic neurones measured with an electron microprobe, Pfluegers Arch. 400: 274–279.CrossRefGoogle Scholar
  81. Garay, R. P., Nazaret, C., Hannaert, P. A., and Cragoe, E. J., 1988, Demonstration of a [K F,Cl-]cotransport system in human red cells by its sensitivity to [(dihydroindenyl)oxy]alkanoic acids: Regulation of cell swelling and distinction from the bumetanide-sensitive [Na+,K+,C1-]-cotransport system, Mol. Pharmacol. 33: 696–701.PubMedGoogle Scholar
  82. Gardner, D. R., and Moreton, R. B., 1985, Intracellular chloride in molluscan neurons, Comp. Biochem. Physiol. 80A: 461–467.CrossRefGoogle Scholar
  83. Geck, P., and Heinz, E., 1986, The Na-K-2C1 cotransport system, J. Membr. Biol. 91: 97–105.PubMedCrossRefGoogle Scholar
  84. Gerencser, G. A., and Lee, S. H., 1983, Cl- -stimulated adenosine triphosphatase: Existence, location and function, J. Exp. Biol. 106: 143–161.PubMedGoogle Scholar
  85. Gold, M. R., and Martin, A. R., 1982, Intracellular CL accumulation reduces CL conductance in inhibitory synaptic channels, Nature 299: 828–830.PubMedCrossRefGoogle Scholar
  86. Goldman, D. E., 1943, Potential, impedance and rectification in membranes, J. Gen. Physiol. 27: 37–60.PubMedCrossRefGoogle Scholar
  87. Gunn, R. B., 1985, Bumetanide inhibition of anion exchange in human red blood cells, Biophys. J. 47: 326a.Google Scholar
  88. Haas, M., 1989, Properties and diversity of (Na-K-Cl) cotransporters, Annu. Rev. Physiol. 51: 443–457.PubMedCrossRefGoogle Scholar
  89. Harris, G. L., and Betz, W. J., 1987, Evidence for active chloride accumulation in normal and dencrvated rat lumbrical muscle, J. Gen. Physiol. 90: 127–144.PubMedCrossRefGoogle Scholar
  90. Hattori, K., Akaike, N., Oomura, Y., and Kuraoka, S., 1984, Internal perfusion studies demonstrating GABA-induced chloride responses in frog primary afferent neurons, Am. J. Physiol. 246: C259 - C265.PubMedGoogle Scholar
  91. Heinemann, V., and Lux, H. D., 1977, Ceiling of stimulus induced rises in extracellular potassium con-centration in the cerebral cortex of the cat, Brain Res. 120: 231–249.PubMedCrossRefGoogle Scholar
  92. Higashijima, T., Ferguson, K. M., and Sternweis, P. C., 1987, Regulation of hormone-sensitive GTPdependent regulatory proteins by chloride, J. Biol. Chem. 262: 3597–3602.PubMedGoogle Scholar
  93. Hille, B., 1975, Ionic selectivity of Na and K channels of nerve membranes, in: Membranes: A Series of Advances, Volume 3 ( G. Eisenman, ed.), pp. 255–323, Dekker, New York.Google Scholar
  94. Hino, N., 1979, Action of ammonium ions on the resting membrane of crayfish stretch receptor neuron, Jpn. J. Physiol. 29: 99–102.PubMedCrossRefGoogle Scholar
  95. Hodgkin, A. L., and Katz, B., 1949, The effect of sodium ions on the electrical activity of the giant axon of the squid, J. Physiol. (London) 108: 37–77.Google Scholar
  96. Hoffman, E. K., and Simonsen, L. O., 1989, Membrane mechanisms in volume and pH regulation in vertebrate cells, Physiol. Rev. 69: 315–382.Google Scholar
  97. Huguenard, J. R., and Alger, B. E., 1986, Whole cell voltage-clamp study of the fading of GABA-activated currents in acutely dissociated hippocampal neurons, J. Neurophysiol. 56: 1–18.PubMedGoogle Scholar
  98. Iles, J. F., and Jack, J. J. B., 1980, Ammonia: Assessment of its action on postsynaptic inhibition as a cause of convulsions, Brain 103: 555–578.PubMedCrossRefGoogle Scholar
  99. Ito, M., 1957, The electrical activity of spinal ganglion cells investigated with intracellular microelectrodes, Jpn. J. Physiol. 7: 297–323.PubMedCrossRefGoogle Scholar
  100. Iversen, L. L., 1975, Uptake processes for biogenic amines, in: Handbook of Psychopharmacology, Volume 3 ( L. L. Iversen, ed.), pp. 381–442, Plenum Press, New York.Google Scholar
  101. Jahnsen, H., and Llinds, R., 1984, Ionic basis for the electroresponsiveness and oscillatory properties of guinea-pig thalamic neurons in vitro, J. Physiol. (London) 349: 227–247.Google Scholar
  102. Janigro, D., and Schwartzkroin, P. A., 1988, Effects of GABA on CA3 pyramidal cell dendrites in rabbit hippocampal slices, Brain Res. 453: 265–274.PubMedCrossRefGoogle Scholar
  103. Kaila, K., Pasternack, M., Saarikoski, J., and Voipio, J., 1989, Influence of GABA-gated bicarbonate conductance on membrane potential, current and intracellular chloride in crayfish muscle fibres, J. Physiol. (London) 416:161–181.Google Scholar
  104. Kaneda, M., Wakamori, M., and Akaike, N., 1989, GABA-induced chloride current in rat isolated Purkinje cells, Am. J. Physiol. 256: C1153 - C1159.PubMedGoogle Scholar
  105. Kanner, B. I., and Schuldiner, S., 1987, Mechanism of transport and storage of neurotransmitters, CRC Crit. Rev. Biochem. 22: 1–38.PubMedCrossRefGoogle Scholar
  106. Kelly, J. S., Kmjevié, K., Morris, M. E., and Yim, G. K. W., 1969, Anionic permeability of cortical neurons, Exp. Brain Res. 7: 11–31.PubMedCrossRefGoogle Scholar
  107. Kerkut, G. A., and Meech, R. W., 1966a, The internal chloride concentration of H and D cells in the snail brain, Comp. Biochem. Physiol. 19: 819–832.CrossRefGoogle Scholar
  108. Kerkut, G. A., and Meech, R. W., 19666, Microelectrode determination of the intracellular chloride concentration in nerve cells, Life Sci. 5: 453–456.Google Scholar
  109. Keynan, S., and Kanner, B. I., 1988, y-Aminobutyric acid transport in reconstituted preparations from rat brain: Coupled sodium and chloride fluxes, Biochemistry 27: 12–17.Google Scholar
  110. Keynes, R. D., 1963, Chloride in the squid giant axon, J. Physiol. (London) 169: 690–705.Google Scholar
  111. Knepper, M. A., Packer, R., and Good, D. W., 1989, Ammonium transport in the kidney, Physiol. Rev. 69: 179–249.PubMedGoogle Scholar
  112. Korn, S. J., Giacchino, J. L., Chamberlin, N. L., and Dingledine, R., 1987, Epileptiform burst activity induced by potassium in the hippocampus and its regulation by GABA-mediated inhibition, J. Neurophysiol. 57: 325–340.PubMedGoogle Scholar
  113. Kostyuk, P. G., Veselovsky, N. S., Fedulova, S. A., and Tsyndrenko, A. Y., 1981, Ionic currents in the somatic membrane of rat dorsal root ganglion neurons. III. Potassium currents, Neuroscience 6: 2439–2444.PubMedCrossRefGoogle Scholar
  114. Kregenow, F. M., 1981, Osmoregulatory salt transporting mechanisms: Control of cell volume in anisosmotic media, Ann. Rev. Physiol. 43: 493–505.CrossRefGoogle Scholar
  115. Kmjevié, K., 1974, Chemical nature of synaptic transmission in vertebrates, Physiol. Rev. 54: 418–540.Google Scholar
  116. Kmjevié, K., 1981, Transmitters in motor systems, in: Handbook of Physiology, Section 2, The Nervous System, Volume II, Motor Control ( V. B. Brooks, ed.), pp. 107–154, American Physiological Society, Baltimore.Google Scholar
  117. Kmjevié, K., 1983, GABA-mediated inhibitory mechanisms in relation to epileptic discharges, in: Basic Mechanisms of Neuronal Hyperexcitability ( H. Jasper and N. van Gelder, eds.), pp. 249–280, Liss, New York.Google Scholar
  118. Kmjevié, K., 1984, Neurotransmitters in cerebral cortex: A general account, in: Cerebral Cortex, Volume 2, Functional Properties of Cortical Cells ( E. G. Jones and A. Peters, eds.), pp. 39–61, Plenum Press, New York.Google Scholar
  119. Kudo, Y., Abe, N., Goto, S., and Fukuda, H., 1975, The chloride-dependent depression by GABA in the frog spinal cord, Eur. J. Pharmacol. 32: 251–259.PubMedCrossRefGoogle Scholar
  120. Kunze, D. L., and Brown, A. M., 1971, Internal potassium and chloride activities and the effects of acetylcholine on identifiable Aplysia neurons, Nature (London) 229: 229–231.Google Scholar
  121. Landry, D. W., Reitman, M., Cragoe, E. J., and Al-Awqati, Q., 1987, Epithelial chloride channel, J. Gen. Physiol. 90: 779–798.PubMedCrossRefGoogle Scholar
  122. Latorre, R., and Miller, C., 1983, Conduction and selectivity in potassium channels, J. Membr. Biol. 71: 11–30.PubMedCrossRefGoogle Scholar
  123. Lauf, P. K., 1988, K: Cl cotransport: Emerging Molecular aspects of a ouabain-resistant, volume-responsive transport system in red blood cells, Renal Physiol. Biochem. 3–5: 248–259.Google Scholar
  124. Lauf, P. K., McManus, T. J., Haas, M., Forbush, B., Duhm, J., Flatman, P. W., Saier, M. H., and Russell, J. M., 1987, Physiology and biophysics of chloride and cation cotransport across cell membranes, Fed. Proc. 46: 2377–2394.Google Scholar
  125. Levy, R. A., 1977, The role of GABA in primary afferent depolarization, Prog. Neurobiol. (Oxford) 9: 211–267.CrossRefGoogle Scholar
  126. Lewis, D. V., and Schuette, W. H., 1975, NADH fluorescence and (K+), changes during hippocampal electrical stimulation, J. Neurophysiol. 38: 405–417.PubMedGoogle Scholar
  127. Llinâs, R., 1988, The intrinsic electrophysiological properties of mammalian neurons: Insights into central nervous function, Science 242: 1654–1664.PubMedCrossRefGoogle Scholar
  128. Llinâs, R., and Baker, R., 1972, A chloride-dependent inhibitory postsynaptic potential in cat trochlear motoneurons, J. Neurophysiol. 35: 484–492.PubMedGoogle Scholar
  129. Llinâs, R., Baker, R., and Precht, W., 1974, Blockage of inhibition by ammonium acetate action on chloride pump in cat trochlear motoneurons, J. Neurophysiol. 37: 522–532.PubMedGoogle Scholar
  130. Lopez, R., and Alvarez-Leefmans, F. J., 1984, Electrotonic structure and specific membrane properties of frog dorsal root ganglion neurons maintained in vitro, Soc. Neurosci. Abstr. 10 (1): 429.Google Scholar
  131. Lux, H. D., 1971, Ammonium and chloride extrusion: Hyperpolarizing synaptic inhibition in spinal motoneurons, Science 173: 555–557.PubMedCrossRefGoogle Scholar
  132. Lux, H. D., Loracher, C., and Neher, E., 1970, The action of ammonium on postsynaptic inhibition of cat spinal motoneurons, xp. Brain Res. 11: 431–447.Google Scholar
  133. Lytle, C., and McManus, T. J., 1987, Effect of loop diuretics and stilbene derivatives on swellin-induced KCI cotransport, J. Gen. Physiol. 90: 28a.Google Scholar
  134. McCarren, M., and Alger, B. E., 1985, Use-dependent depression of IPSPs in rat hippocampal pyramidal cells in vitro, J. Neurophysiol. 53: 557–571.PubMedGoogle Scholar
  135. Mayer, M. L., and Westbrook, G. L., 1983, A voltage-clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurons, J. Physiol. (London) 340; 19–45.Google Scholar
  136. Meyer, H., and Lux, H. D., 1974, Action of ammonium on a chloride pump, Pfluegers Arch. 350: 185 - I95.CrossRefGoogle Scholar
  137. Misgeld, U., Deisz, R. A., Dodt, H. V., and Lux, H. D., 1986, The role of chloride transport in postsynaptic inhibition of hippocampal neurons, Science 232: 1413–1415.PubMedCrossRefGoogle Scholar
  138. Moody, W. J., 1981, The ionic mechanisms of intracellular pH regulation in crayfish neurons, J. Physiol. (London) 316: 293–308.Google Scholar
  139. Moreton, R. B., and Gardner, D. R., 1981, Increased intracellular chloride activity produced by the molluscicide, N-(triphenylmethyl)morpholine (Freston), in Lymnaea stagnalis neurons, Pestle. Biochem. Physiol. 15: 1–9.Google Scholar
  140. Moser, H., 1985, Intracellular pH regulation in the sensory neuron of the stretch receptor of the crayfish (Astacus fluviatilis), J. Physiol. (London) 362: 23–38.Google Scholar
  141. Moser, H., 1987, Electrophysiological evidence for ammonium as a substitute for potassium in activating the sodium pump in a crayfish sensory neuron, Can. J. Physiol. Pharmacol. 65: 141–145.PubMedCrossRefGoogle Scholar
  142. Müller, W., Misgeld, U., and Lux, H. D., 1989, y-Aminobutyric acid-induced ion movements in the guinea pig hippocampal slice, Brain Res. 484: 184–191.Google Scholar
  143. Nakai, K., Sasaki, K., Matsumoto, M., and Takashima, K., 1988, Effects of furosemide on the resting membrane potentials and the transmitter-induced responses of the Aplysia ganglion cells, Tohoku J. Exp. Med. 156: 79–90.PubMedCrossRefGoogle Scholar
  144. Neild, T. O., and Thomas, R. C., 1974, Intracellular chloride activity and the effects of acetylcholine in snail neurones, J. Physiol. (London) 242: 453–470.Google Scholar
  145. Nelson, M. T., and Blaustein, M. P., 1982, GABA efflux from synaptosomes: Effects of membrane potential, and extemal GABA and cations, J. Membr. Biol. 69: 213–223.PubMedCrossRefGoogle Scholar
  146. Newberry, N. R., and Nicoll, R. A., 1985, Comparison of the action of baclofen with y-aminobutyric acid on rat hippocampal pyramidal cells in vitro, J. Physiol. (London) 360: 161–185.Google Scholar
  147. Nicoll, R. A., 1978, The blockade of GABA mediated responses in the frog spinal cord by ammonium ions and furosemide, J. Physiol. (London) 283: 121–132.Google Scholar
  148. Nicoll, R. A., 1988, The coupling of neurotransmitter receptors to ion channels in the brain, Science 241: 545–551.PubMedCrossRefGoogle Scholar
  149. Nicoll, R. A., and Alger, B. E., 1979, Presynaptic inhibition: Transmitter and ionic mechanisms, Int. Rev. Neurobiol. 21: 217–258.PubMedCrossRefGoogle Scholar
  150. Nishi, S., Minota, S., and Karczmar, A. G., 1974, Primary afferent neurones: The ionic mechanism of GABA-mediated depolarization, Neuropharmacology 13: 215–219.PubMedCrossRefGoogle Scholar
  151. Nistri, A., 1983, Spinal cord pharmacology of GABA and chemically related amino acids, in: Handbook of the Spinal Cord, Volume 1, Spinal Cord Pharmacology ( R. A. Davidoff, ed.), pp. 45–104, Dekker, New York.Google Scholar
  152. O’Grady, S. M., Palfrey, H. C., and Field, M., 1987, Characteristics and functions of Na-K-Cl cotransport in epithelial tissues, Am. J. Physiol. 253: 177–192.Google Scholar
  153. Olsen, R. W., and Leeb-Lundberg, F., 1981, Convulsant and anticonvulsant drug binding sites related toGoogle Scholar
  154. GABA-regulated chloride ion channels, in: GABA and Benzodiazepine Receptors (E. Costa, G. DiChiara, and G. L. Gessa, eds.), pp. 93–103, Raven Press, New York.Google Scholar
  155. Olsen, R. W., and Venter, J. C., 1986, Benzodiazepine/GABA Receptors and Chloride Channels: Structural and Functional Properties, Liss, New York.Google Scholar
  156. Otsuka, M., and Konishi, S., 1976, GABA in the spinal cord, in: GABA in Nervous System Function ( E. Roberts, T. N. Chase, and D. B. Tower, eds.), pp. 197–202, Raven Press, New York.Google Scholar
  157. Padjen, A., Nicoll, R., and Barker, J. L., 1973, Synaptic potentials in the isolated frog spinal cord studied using sucrose gap, J. Gen. Physiol. 61: 270–271.Google Scholar
  158. Peterson, R. P., and Pepe, I. A., 1961, The fine structure of inhibitory synapses in the crayfish, J. Biophys. Biochem. Cytol. 11: 159–169.CrossRefGoogle Scholar
  159. Raabe, W., and Gumnit, R. J., 1975, Disinhibition in cat motor cortex by ammonia, J. Neurophysiol. 38: 347–355.PubMedGoogle Scholar
  160. Radian, R., and Kanner, B. I., 1983, Stoichiometry of sodium-and chloride-coupled -y-aminobutyric acid transport by synaptic plasma membrane vesicles isolated from rat brain, Biochemistry 22: 1236–1241.PubMedCrossRefGoogle Scholar
  161. Radian, R., and Kanner, B. 1., 1985, Reconstitution and purification of the sodium and chloride-coupled y-aminobutyric acid transporter from rat brain, J. Biol. Chem. 260: 11859–11865.PubMedGoogle Scholar
  162. Radian, R., Bendahan, A., and Kanner, B. I., 1986, Purification and identification of the functional sodium-and chloride-coupled y-aminobutyric acid transport glycoprotein from rat brain, J. Biol. Chem. 261: 15437–15441.PubMedGoogle Scholar
  163. Reuss, L., 1983, Basolateral KCI cotransport in a NaCI-absorbing epithelium, Nature 305: 723–726.PubMedCrossRefGoogle Scholar
  164. Reuss, L., 1988, Cell volume regulation in nonrenal epithelia, Renal Physiol. Biochem. 3–5: 187–201.Google Scholar
  165. Reuss, L., 1989, Ion transport across gallbladder epithelium, Physiol. Rev. 69: 503–545.PubMedGoogle Scholar
  166. Roberts, E., 1986, GABA: The road to neurotransmitter status, in: Benzodiazepine/GABA Receptors and Google Scholar
  167. Chloride Channels: Structural and Functional Properties,pp. 1–39, Liss, New York.Google Scholar
  168. Roos, A., and Boron, W. F., 1981, Intracellular pH, Physiol. Rev. 61: 296–434.PubMedGoogle Scholar
  169. Rudy, B., 1988, Diversity and ubiquity of K channels, Neuroscience 25: 729–749.PubMedCrossRefGoogle Scholar
  170. Russell, J. M., 1976, ATP-dependent chloride influx into squid giant axon, J. Membr. Biol. 28: 335–350.PubMedCrossRefGoogle Scholar
  171. Russell, J. M., 1978, Effects of ammonium and bicarbonate-CO2 on intracellular chloride levels in Aplysia neurons, Biophys. J. 22: 131–137.PubMedCrossRefGoogle Scholar
  172. Russell, J. M., 1979, Chloride and sodium influx: A coupled uptake mechanism in the squid giant axon, J. Gen. Physiol. 73: 801–818.PubMedCrossRefGoogle Scholar
  173. Russell, J. M., 1980, Anion transport mechanisms in neurons, Ann. N.Y. Acad. Sci. 341: 510–523.PubMedCrossRefGoogle Scholar
  174. Russell, J. M., 1983, Cation-coupled chloride influx in squid axon: Role of potassium and stoichiometry of the transport process, J. Gen. Physiol. 81: 909–925.PubMedCrossRefGoogle Scholar
  175. Russell, J. M., 1984, Chloride in the squid giant axon, Curr. Top. Membr. Transp. 22: 177–193.CrossRefGoogle Scholar
  176. Russell, J. M., and Boron, W. F., 1982, Intracellular pH regulation in squid giant axons, in: Intracellular pH: Its Measurement, Regulation and Utilization in Cellular Functions, pp. 221–237, Liss, New York.Google Scholar
  177. Russell, J. M., and Brown, A. M., 1972, Active transport of chloride by the giant neuron of the Aplysia abdominal ganglion, J. Gen. Physiol. 60: 499–518.PubMedCrossRefGoogle Scholar
  178. Schlue, W.-R., and Deitmer, J. W., 1988, Ionic mechanisms of intracellular pH regulation in the nervous system, Ciba Found. Symp. 139: 49–69.Google Scholar
  179. Schlue, W.-R., and Thomas, R. C., 1985, A dual mechanism for intracellular pH regulation by leech neurons, J. Physiol. (London) 364: 327–338.Google Scholar
  180. Schmidt, R. F., 1963, Pharmacological studies on the primary afferent depolarization of the toad spinal cord, Pfluegers Arch. 277: 325–346.CrossRefGoogle Scholar
  181. Schwartzkroin, P. A., and Wheal, H. V., 1984, Electrophysiology of Epilepsy, Academic Press, New York.Google Scholar
  182. Serve, G., Endres, W., and Grafe, P., 1988, Continuous electrophysiological measurements of changes in cell volume of motoneurons in the isolated frog spinal cord, Pfluegers Arch. 411: 410–415.CrossRefGoogle Scholar
  183. Siggins, G. R., and Gruol, D. L., 1986, Mechanisms of transmitter action in the vertebrate central nervous system, in: Handbook of Physiology, Section I, The Nervous System, Volume 14, ( T. E. Bloom, ed.), pp. 1–114, American Physiological Society, Bethesda.Google Scholar
  184. Sillito, A. M., 1984, Functional considerations of the operation of GABAergic inhibitory processes in the visual cortex, in: Cerebral Cortex, Volume 2, Functional Properties of Cortical Cells ( E. G. Jones and A. Peters, eds.), pp. 91–117, Plenum Press, New York.Google Scholar
  185. Simmonds, M. A., 1984, Physiological and pharmacological characterization of the actions of GABA, in: Actions and Interactions of GABA and Benzodiazepines ( N. G. Bowery, ed.), pp. 27–40, Raven Press, New York.Google Scholar
  186. Somjen, G. G., 1979, Extracellular potassium in the mammalian central nervous system, Annu. Rev. Physiol. 41: 159–177.PubMedCrossRefGoogle Scholar
  187. Stein, W. D., 1986, Transport and Diffusion across Cell Membranes, Academic Press, New York. Steriade, M., and Llinâs, R., 1988, The functional states of the thalamus and the associated neuronal interplay, Physiol. Rev. 68: 649–736.Google Scholar
  188. Tanaka, C., and Taniyama, K., 1986, GABA transport in peripheral tissues: Uptake and efflux, in: GABAergic Mechanisms in the Mammalian Periphery ( S. L. Erdö and N. G. Bowery, eds.), pp. 57–72, Raven Press, New York.Google Scholar
  189. Thomas, R. C., 1976, The effect of carbon dioxide on the intracellular pH and buffering power of snail neurones, J. Physiol. (London) 255: 715–735.Google Scholar
  190. Thomas, R. C., 1977, The role of bicarbonate, chloride and sodium ions in the regulation of intracellular pH in snail neurones, J. Physiol. (London) 273; 317–338.Google Scholar
  191. Thomas, R. C., 1984, Experimental displacement of intracellular pH and the mechanism of its subsequent recovery, J. Physiol. (London) 354: 3P - 22 P.Google Scholar
  192. Thomas, R. C., and Cohen, C. J., 1981, A liquid ion-exchanger alternative to KCI for filling intracellular reference microelectrodes, Pfluegers Arch. 390: 96–98.CrossRefGoogle Scholar
  193. Thompson, S. M., and Gähwiler, B. H., I989a, Activity-dependent disinhibition. 1. Repetitive stimulation reduces IPSP driving force and conductance in the hippocampus in vitro, J. Neurophysiol. 61: 501–511.Google Scholar
  194. Thompson, S. M., and Gähwiler, B. H., 19896, Activity-dependent disinhibition. 11. Effects of extracellular potassium, furosemide, and membrane potential on Eel— in hippocampal CA3 neurons, J. Neurophysiol. 61: 512–523.Google Scholar
  195. Thompson, S. M., Deisz, R. A., and Prince, D. A., 1988a, Outward chloride/cation cotraisport in mammalian cortical neurons, Neurosci. Leu. 89: 49–54.CrossRefGoogle Scholar
  196. Thompson, S. M., Deisz, R. A., and Prince, D. A., 1988b, Relative contributions of passive equilibrium and active transport to the distribution of chloride in mammalian cortical neurons, J. Neurophysiol. 60: 105–124.PubMedGoogle Scholar
  197. Traub, R. D., Miles, R., and Wong, R. K. S., 1989, Model of the origin of rhythmic population os:illations in the hippocampal slice, Science 243: 1319–1325.PubMedCrossRefGoogle Scholar
  198. Vaughan-Jones, R. D., 1988, Regulation of intracellular p1-I in cardiac muscle, Ciba Found. Symp. 139: 2346.Google Scholar
  199. Verkman, A. S., Sellers, M. C., Chao, A. C., Leung, T.. and Ketcham, R., 1989, Synthesis and characterization of improved chloride sensitive fluorescent indicators for biological applications, Anal. Biochem. 178: 355–361.PubMedCrossRefGoogle Scholar
  200. Vitoux, D., Oliviero, O., Garay, R. P., Cragoe, E. J., Galacteros, F., and Benzard, Y., 1989, Inhibition of K ± efflux and dehydration of sickle cells by [(dihydroindenyl)oxy]alkanoic acid: An inhibitor of the K+,Cl- cotransport system, Proc. Natl. Acad. Sci. USA 86: 4273–4276.PubMedCrossRefGoogle Scholar
  201. Widdicombe, J. H., Nathanson, I. T., and Highland, E., 1983, Effects of loop diuretics on ion transport by dog tracheal epithelium, Am. J. Physiol. 245: C388 - C396.PubMedGoogle Scholar
  202. Wojtowicz, J. M., and Nicoll, R. A., 1982, Selective action of piretamide on primary afferent GABA responses in the frog spinal cord, Brain Res. 236: 173–181.PubMedCrossRefGoogle Scholar
  203. Wong, R. K. S., and Watkins, D. J., 1982, Cellular factors influencing GABA response in hippocampal pyramidal cells, J. Neurophysiol. 48: 938–951.PubMedGoogle Scholar
  204. Yudilevich, D. L., and Boyd, C. A. R., 1987, Amino Acid Transport in Animal Cells, Physiological Society Study Guides, No. 2, Manchester University Press, Great Britain.Google Scholar
  205. Zelikovic, I., Stejskal-Lorenz, E., Lohstroh, P., Budreau, A., and Chesney, R. W., 1989, Anion dependence of taurine transport by rat renal brush border membrane vesicles, Am. J. Physiol. 256: 646–655.Google Scholar

Copyright information

© Springer Science+Business Media New York 1990

Authors and Affiliations

  • Francisco J. Alvarez-Leefmans
    • 1
    • 2
  1. 1.Departamento de Farmacología y ToxicologíaCentro de Investigacíon y de Estudios Avanzados del I. P. N.Mexico D. F.Mexico D. F.
  2. 2.Departamento de NeurobiologíaInstituto Mexicano de PsiquiatríaMexico D. F.Mexico

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