Abstract
γ-Aminobutyric acid (GABA) is a transmitter compound with a wide distribution and an exclusively inhibitory role in both vertebrate and invertebrate nervous systems (Gerschenfeld, 1973; Krnjević, 1974). Apart from its action on vertebrate GABAB-type receptors (see Dutar and Nicoll, 1988), the inhibitory effect of GABA is based on the opening of postsynaptic Cl − channels (Boistel and Fatt, 1958; Siggins and Gruol, 1986). An increase in postsynaptic Cl − conductance is also characteristic of glycine-mediated inhibition in vertebrates (Siggins and Gruol, 1986) and of acetylcholine-mediated inhibition in some invertebrate synapses (e.g., Kerkut and Thomas, 1964). The inhibitory effect of an increase in postsynaptic Cl − conductance is due to the fact that in most excitable cells, the equilibrium potential of chloride is at a level more negative than the threshold for action-potential generation.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Aickin, C. C., Deisz, R. A., and Lux, H. D., 1982, Ammonium action on post-synaptic inhibition in crayfish neurones: Implications for the mechanism of chloride extrusion, J. Physiol. (London) 329: 319–339.
Alger, E., and Nicoll, R. A., 1979, GABA-mediated biphasic inhibitory responses in hippocampus, Nature 281: 315–317.
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.
Ammann, D., 1986, lon-Selective Microelectrodes, Springer-Verlag, Berlin.
Araki, T., Ito, M., and Oscarsson, O., 1961, Anion permeability of the synaptic and non-synaptic motoneurone membrane, J. Physiol. (London) 159: 410–435.
Aronson, P. S., 1985, Kinetic properties of the plasma membrane Na +-H+ exchanger, Annu. Rev. Physiol. 47: 545–560.
Atwood, H. L., 1976, Organization and synaptic physiology of crustacean neuromuscular systems, Prog. Neurobiol. 7: 291–391.
Balestrino, M., and Somjen, G. G., 1988, Concentration of carbon dioxide, interstitial pH and synaptic transmission in hippocampal formation of the rat, J. Physiol. (London) 396: 247–266.
Ballanyi, K., and Grafe, P., 1985, An intracellular analysis of y-aminobutyric-acid associated ion movements in rat sympathetic neurones, J. Physiol. (London) 365: 41–58.
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.
Boistel, J., and Fatt, P., 1958, Membrane permeability change during inhibitory transmitter action in crustacean muscle, J. Physiol. (London) 144: 176–191.
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.
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.
Boron, W. F., Hogan, E., and Russell, J. M., 1988, pH-sensitive activation of the intracellular-pH regulation system in squid axons by ATP-y-S, Nature 332: 262–265.
Brodwick, M. S., and Eaton, D. C., 1978, Sodium channel inactivation in squid axon is removed by high internal pH or tyrosine-specific reagents, Science 200: 1494–1496.
Busa, W. B., 1986, Mechanisms and consequences of pH-mediated cell regulation, Annu. Rev. Physiol. 48: 389–402.
Byerly, L., Meech, R. W., and Moody, W. J., 1984, Rapidly activating hydrogen ion currents in perfused neurones of the snail Lymnaea stagnalis, J. Physiol. (London) 351: 199–216.
Carbone, E., Testa, P. L., and Wanke, E., 1981, Intracellular pH and ionic channels in the Loligo vulgaris giant axon, Biophys. J. 35: 393–413.
Chesler, M., and Chan, C. Y., 1988, Stimulus-induced extracellular pH transients in the in vitro turtle cerebellum, Neuroscience 37: 941–948.
Chesler, M., and Kraig, R. P., 1987, Intracellular pH of astrocytes increases rapidly with cortical stimulation, Am. J. Physiol. 253: R666 - R670.
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 post-synaptic potential, J. Physiol. (London) 130: 326–373.
Deisz, R. A., and Lux, H. D., 1982, The role of intracellular chloride in hyperpolarizing post-synaptic inhibition of crayfish stretch receptor neurones, J. Physiol. (London) 326: 123–138.
Dudel, J., 1977, Voltage dependence of amplitude and time course of inhibitory synaptic current in crayfish muscle, Pfluegers Arch. 371: 167–174.
Dudel, J., and Rüdel, R., 1969, Voltage controlled contractions and current voltage relations of crayfish muscle fibers in chloride-free solutions, Pfluegers Arch. 308: 291–314.
Dudel, J., Finger, W., and Stettmeier, H., 1980, Inhibitory synaptic channels activated by -y-aminobutyric acid (GABA) in crayfish muscle, Pfluegers Arch. 387: 143–151.
Dutar, P., and Nicoll, R. A., 1988, A physiological role for GABAB receptors in the central nervous system, Nature 332: 156–158.
Eccles, J. C., 1964, The Physiology of Synapses, Springer, Berlin.
Edwards, C., 1982, The selectivity of ion channels in nerve and muscle, Neuroscience 6: 1335–1366.
Endres, W., Grafe, P., Bostock, H., and ten Bruggencate, G., 1986, Changes in extracellular pH during electrical stimulation of isolated vagus nerve, Neurosci. Lett. 64: 201–205.
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.
Galler, S., and Moser, H., 1986, The ionic mechanism of intracellular pH regulation in crayfish muscle fibres, J. Physiol. (London) 374: 137–151.
Gerschenfeld, H. M., 1973, Chemical transmission in invertebrate central nervous systems and neuromuscular junctions, Physiol. Rev. 53: 1–119.
Goldman, D. E., 1943, Potential, impedance, and rectification in membranes, J. Gen. Physiol. 27: 37–60.
Gruol, D. L., Barker, J. L., Huang, L.-Y.M., MacDonald, J. F., and Smith, T. G., 1980, Hydrogen ions have multiple effects on the excitability of cultured mammalian neurons„ Brain Res. 183: 247–252.
Gutknecht, J., and Tosteson, D. C., 1973, Diffusion of weak acids across lipid bilayer membranes: Effects of chemical reactions in the unstirred layers, Science 182: 1258–1261.
Hansen, A. J., and Zeuthen, T., 1981, Extracellular ion concentrations during spreading depression and ischemia in the rat brain cortex, Acta Physiol. Scand. 113: 437–445.
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.
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.
Ito, M., Kostyuk, P. G., and Oshima, T., 1962, Further study on anion permeability of inhibitory post-synaptic membrane of cat motoneurones, J. Physiol. (London) 164: 150–156.
Iwasaki, S., and Florey, E., 1969, Inhibitory miniature potentials in the stretch receptor neurons of crayfish, J. Gen. Physiol. 53: 666–682.
Jack, J. J. B., Noble, D., and Tsien, R. W., 1975, Electric Current Flow in Excitable Cells, Oxford University Press ( Clarendon ), London.
Kaila, K., 1988, GABA-activated movements of formate and acetate: Influence on intracellular pH and surface pH in crayfish skeletal muscle fibres, Ciba Found. Symp. 139: 184–186.
Kaila, K., and Voipio, J., 1987, Postsynaptic fall in intracellular pH induced by GABA-activated bicarbonate conductance, Nature 330: 163–165.
Kaila, K., Mattsson, K., and Voipio, J., 1989a, Fall in intracellular pH and increase in resting tension induced by a mitochondrial uncoupling agent in crayfish muscle, J. Physiol. (London) 408: 271–293.
Kaila, K., Pasternack, M., Saarikoski, J., and Voipio, J., 1989b, Influence of GABA-gated bicarbonate conductance on potential, current and intracellular chloride in crayfish muscle fibers, J. Physiol. (London) 416: 161–181.
Kaila, K., Saarikoski, J., and Voipio, J., 1990, Mechanism of action of GABA on intracellular pH and on surface pH in crayfish muscle fibers, (submitted).
Katz, B., 1969, The Release of Neural Transmitter Substances, Liverpool University Press, Liverpool.
Kelly, J. S., Kmjevie, K., Morris, M. E., and Yim, G. K. W., 1969, Anionic permeability of cortical neurones, Exp. Brain Res. 7: 11–31.
Kerkut, G. A., and Thomas, R. C., 1964, The effect of anion injection and changes in the external potassium and chloride concentration on the reversal potentials of the IPSP and acetylcholine, Comp. Biochem. Physiol. 11: 199–213.
Konnerth, A., Lux, H. D., and Morad, M., 1987, Proton-induced transformation of calcium channel in chick dorsal root ganglion cells, J. Physiol. (London) 386: 603–633.
Kraig, R. P., Ferreira-Filho, C. S., and Nicholson, C., 1983, Alkaline and acid transients in cerebellar microenvironment, J. Neurophysiol. 49: 831–850.
Krishtal, O. A., and Pidoplichko, V. 1., 1980, A receptor for protons in the nerve cell membrane, Neuroscience 5: 2325–2327.
Krishtal, O. A., Osipchuk, Y. V., Shelest, T. N., and Smirnoff, S. V., 1987, Rapid extracellular pH transients related to synaptic transmission in rat hippocampal slices, Brain Res. 436: 352–356.
Kmjevie, K., 1974, Chemical nature of synaptic transmission in vertebrates, Physiol. Rev. 54: 418–540.
Kuffler, S. W., and Eyzaguirre, C., 1955, Synaptic inhibition in an isolated nerve cell, J. Gen. Physiol. 39: 155–184.
Llinas, 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.
Lux, H. D., 1971, Ammonium and chloride extrusion: Hyperpolarizing synaptic inhibition in spinal motoneurons, Science 173: 555–557.
Lux, H. D., Loracher, C., and Neher, E., 1970, The action of ammonium on postsynaptic inhibition of cat spinal motoneurons, Exp. Brain Res. 11: 431–447.
McLaughlin, S. G. A., and Dilger, J. P., 1980, Transport of protons across membranes by weak acids, Physiol. Rev. 60: 825–863.
Mahnensmith, R. L., and Aronson, P. S., 1985, The plasma membrane sodium—hydrogen exchanger and its role in physiological and pathophysiological processes, Circ. Res. 56: 773–788.
Mason, M. J., Mattsson, K., Pastemack, M., Voipio, J., and Kaila, K., 1990, Postsynaptic fall in intracellular pH and increase in surface pH caused by efflux of fornate and acetate through GABA-gated channels in crayfish muscle fibres, Neuroscience (in press).
Meech, R. W., 1979, Membrane potential oscillations in molluscan “burster” neurones, J. Exp. Biol. 81: 93–112.
Meech, R. W., and Thomas, R. C., 1987, Voltage-dependent intracellular pH in Helix aspersa neurones, J. Physiol. (London) 390: 433–452.
Meier, P. C., Ammann, D., Morf, W. E., and Simon, W., 1980, Liquid-membrane ion-sensitive electrodes and their biomedical applications, In: Medical and Biomedical Applications of Electrochemical Devices ( J. Koryta, ed.), Wiley, New York, pp. 13–91.
Melnik, V. I., Glebow, R. N., and Kryhanovski, G. N., 1985, ATP-dependent translocation of protons across the membrane of rat brain synaptic vesicles, Bull. Exp. Biol. Med. 99: 35–38.
Moody, W. J., 1980, Appearance of calcium action potentials in crayfish slow muscle fibres under conditions of low intracellular pH, J. Physiol. (London) 302: 335–346.
Moody, W. J., 1984, Effects of intracellular H+ on the electrical properties of excitable cells, Annu. Rev. Neurosci. 7: 257–278.
Motokizawa, F., Reuben, J. P., and Grundfest, H., 1969, Ionic permeability of the inhibitory postsynaptic membrane of lobster muscle fibers, J. Gen. Physiol. 54: 437–461.
Mutch, W. A. C., and Hansen, A. J., 1984, Extracellular pH changes during spreading depression and cerebral ischemia: Mechanisms of brain pH regulation, J. Cerebr. Blood Flow Metabol. 4: 17–27.
Phillips, J. M., and Nicholson, C., 1979, Anion permeability in spreading depression investigated with ion-sensitive microelectrodes, Brain Res. 173: 567–571.
Phillis, J. W., and Ochs, S., 1971, Excitation and depression of cortical neurones during spreading depression, Exp. Brain Res. 12: 132–149.
Pontén, U., and Siesjö, B. K., 1966, Gradients of CO2 tension in brain, Acta Physiol. Scand. 67: 129–140.
Raabe, W., and Gumnit, R. J., 1975, Disinhibition in cat motor cortex by ammonia, J. Neurophysiol. 38: 347–355.
Rice, M. E., and Nicholson, C., 1988, Behavior of extracellular K+ and pH in skate (Raja erinacea) cerebellum, Brain Res. 461: 328–334.
Robinson, R. A., and Stokes, R. H., 1959, Electrolyte Solutions, Butterworths, London. Roos, A., and Boron, W. F., 1981, Intracellular pH, Physiol. Rev. 61: 296–433.
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.
Sharp, A. P., and Thomas, R. C., 1981, The effects of chloride substitution on intracellular pH in crab muscle, J. Physiol. (London) 312: 71–80.
Siggaard-Andersen, O., 1974, The Acid-Base Status of the Blood, 4th ed., Munskgaard, Copenhagen.
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 IV ( F. E. Bloom, ed.), American Physiological Society, Bethesda, pp. 1–114.
Spuler, A., Endres, W., and Grafe, P., 1987, Metabolic origin of activity-related pH-changes in mammalian peripheral and central unmyelinated fibre tracts, Pfluegers Arch. 408: R69 (abstract).
Stadler, H., and Tsukita, S., 1984, Synaptic vesicles contain an ATP-dependent proton pump and show `knob-like’ protrusions on their surface, EMBO J. 3: 3333–3337.
Sykovà, E., 1988, Extracellular pH and stimulated neurons, Ciba Found. Symp. 139: 220–235.
Takeuchi, A., and Takeuchi, N., 1965, Localized action of gamma-amino butyric acid on the crayfish muscle, J. Physiol. (London) 177: 225–238.
Takeuchi, A., and Takeuchi, N., 1967, Anion permeability of the inhibitory post-synaptic membrane of the crayfish neuromuscular junction, J. Physiol. (London) 191: 575–590.
Takeuchi, A., and Takeuchi, N., 1969, A study of the action of picrotoxin on the inhibitory neuromuscular junction of the crayfish, J. Physiol. (London) 205: 377–391.
Thomas, R. C., 1976, The effect of carbon dioxide on the intracellular pH and buffering power of snail neurones, J. Physiol. 255: 715–735.
Thomas, R. C., 1984, Experimental displacement of intracellular pH and the mechanism of its subsequent recovery, J. Physiol. (London) 354: 3P - 22 P.
Thomas, R. C., 1988, Changes in the surface pH of voltage-clamped snail neurones apparently caused by H+ fluxes through a channel, J. Physiol. (London) 398: 313–327.
Thomas, R. C., and Meech, R. W., 1982, Hydrogen ion currents and intracellular pH in depolarized voltage-clamped snail neurones, Nature 299: 826–828.
Urbanics, R., Leniger-Follert, E., and Lubbers, D. W., 1978, Time course of changes of extracellular H+ and K+ activities during and after direct electrical stimulation of the brain cortex, Pfluegers Arch. 378: 47–53.
Vanheel, B., De Hemptinne, A., and Leusen, I., 1986, Influence of surface pH on intracellular pH regulation in cardiac and skeletal muscle, Am. J. Physiol. 250: C748 - C760.
Voipio, J., Rydqvist, B., and Kaila, K., 1988, The reversal potential of GABA-activated current (EGABA) may be sensitive to metabolic production of CO2/HCO3, Eur. J. Neurosci. ENA-Suppl. p. 61 (abstract).
Wanke, E., Carbone, E., and Testa, P. L., 1979, K+ conductance modified by a titratable group accessible to protons from the intracellular side of the squid axon membrane, Biophys. J. 26: 319–324.
Wanke, E., Carbone, E., and Testa, P. L., 1980, The sodium channel and intracellular H+ blockage in squid axons, Nature 287: 62–63.
Wichser, J., and Kazemi, H., 1975, CSF bicarbonate regulation in respiratory acidosis and alkalosis, J. Appl. Physiol. 38: 504–512.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1990 Springer Science+Business Media New York
About this chapter
Cite this chapter
Kaila, K., Voipio, J. (1990). GABA-Activated Bicarbonate Conductance. In: Alvarez-Leefmans, F.J., Russell, J.M. (eds) Chloride Channels and Carriers in Nerve, Muscle, and Glial Cells. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-9685-8_12
Download citation
DOI: https://doi.org/10.1007/978-1-4757-9685-8_12
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4757-9687-2
Online ISBN: 978-1-4757-9685-8
eBook Packages: Springer Book Archive