Abstract
A wide range of neurotransmitters, such as gamma-aminobutyric acid (GABA), serotonin (5-hydroxytryptamine, 5HT), acetylcholine, noradrenaline, dopamine, and adenosine, have been found to activate potassium channels in central neurons. It is possible that many of these transmitters activate the same potassium channels (Nicoll et al., 1990). An increase in potassium conductance would make cells less excitable and would clearly influence neuronal behavior. In this chapter, we will focus our attention on the characteristics of potassium channels activated and modulated by GABA in the mammalian hippocampus. Emphasis will be placed on “subconductance” states of these channels and their relationship to normal channel behavior. It may turn out that the other transmitters activate and modulate channels in a similar way.
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
Alger, B. E. 1984. Characteristics of a slow hyperpolarizing synaptic potential in rat hippocampal pyramidal cells in vitro. J. Neurophysiol., 52: 892–910.
Andrade, R., Malenka, R. C., and Nicoll, R. A. 1986. A G protein couples serotonin and GABAB receptors to the same channels in hippocampus. Science, 234: 1261–1265.
Atkins, P. T., Surmeier, D. J., and Kitai, S. T. 1990. Muscarinic modulation of a transient K+ conductance in rat neostriatal neurons. Nature, 344: 240–242.
Axelrod, J. A., Burch, R. M., and Jelsema, C. L. 1988. Receptor-mediated activation of phospholipase A2 via GTP-binding proteins: Arachidonic acid and its metabolites as second messengers. Trends Neurosci., 11: 117–123.
Baum, L. E. 1972. An inequality and associated maximization technique in statistical estimation for probabilistic functions of Markov process. Inequalities, 3: 1–8.
Baum, L. E., and Petrie, T. 1966. Statistical inference for probabilistic functions of finite state Markov chains. Ann. Math. Statist., 37: 1554–1563.
Baum, L. E., Petrie, T., Soules, G., and Weiss, N. 1970. A maximization technique occurring in the statistical probabilisticy analysis of robabilistic functions of Markov chains. Ann. Math. Statist. 41: 164–171.
Billingsley, P. 1961. Statistical Inference for Markov Processes. University of Chicago Press, Chicago. Bormann, J. 1988. Electrophysiology of GABAA and GABAB receptor subtypes. Trends Neurosci., 11: 11 2116.
Bowery, N. 1989. GABAB receptors and their significance in mammalian pharmacology. Trends Pharmacol. Sci., 10: 401–407.
Bowery, N. G., Hill, D. R., Hudson, A. L., Doble, A., Middlemiss, D. N., Shaw, J., and Turnbull, M. 1980. (-)Baclofen decreases neurotransmitter release in the mammalian CNS by an action at a novel GABA receptor. Nature, 283: 92–94.
Bowery, N. G., Doble, A., Hill, D. R., Hudson, A. L., Shaw, J. S., Turnbull, M. J., and Warrington, R. 1981. Bicuculline-insensitive GABA receptors on peripheral autonomic nerve terminals. Eur. J. Pharmacol., 71: 53–70.
Brown, A. M., and Birnbaumer, L. 1988. Direct G protein gating of ion channels. Am. J. Physiol., 23: H401 - H410.
Chung, S. H., and Kennedy, R. A. 1991. Forward-backward nonlinear filtering technique for extracting small biological signals from noise. J. Neurosci. Meth., 40: 71–86.
Chung, S.-H., Moore, J. B., Xia, L., Premkumar, L. S., and Gage, P. W. 1990. Characterization of single channel currents using digital signal processing techniques based on hidden Markov models. Phil. Trans. R. Soc. Lond. B, 329: 265–285.
Colmers, W. F., and Williams, J. T. 1988. Pertussis toxin treatment discriminates between pre-and postsynaptic actions of baclofen in rat dorsal raphe nucleus in vitro. Neurosci. Lett., 93: 300–306.
Colquhoun, D., and Hawkes, A. G. 1977. Relaxation and fluctuation of membrane currents that flow through drug-operated channels. Proc. R. Soc. B, Lond. B, 199: 231–262.
Colquhoun, D., and Hawkes, A. G. 1981. On the stochastic properties of single ion channels. Proc. R. Soc. Lond. B, 211: 205–235.
Colquhoun, D., and Hawkes, A. G. 1982. On the stochastic properties of bursts of single ion channel openings and of clusters of bursts. Phil. Trans. R. Soc. Lond. B, 300: 1–59.
Davies, C. H., Davies, S. N., and Collingridge, G. L. 1990. Paired-pulse depression of monosynaptic GABA- mediated inhibitory postsynaptic responses in rat hippocampus. J. Physiol. 424: 513–531.
Davies, C. H., Starkey, S. J., Pozza, M. F., and Collingridge, G. L. 1991. GABA autoreceptors regulate the induction of LTP. Nature, 349: 609–611.
Deisz, R. A., and Lux, H. D. 1985. r-Aminobutyric acid-induced depression of calcium currents of chick sensory neurons. Neurosci. Lett., 56: 205–210.
Dempster, A. P., Laird, N. M., and Rubin, D. B. 1977. Maximum likelihood estimation from incomplete data via the EM algorithm. J. R. Statist. Soc. B, 39: 1–38.
Dolphin, A. C. 1990. G protein modulation of calcium currents in neurons. Annu. Rev. Physiol., 52: 243255.
Dolphin, A. C., and Scott, R. H. 1987. Calcium channel currents and their inhibition by (-)-baclofen in rat sensory neurones: Modulation by guanine nucleotides. J. Physiol., 386: 1–17.
Dolphin, A. C., McGuirk, S. M., and Scott, R. H. 1989. An investigation into the mechanisms of inhibition of calcium channel currents in cultured sensory neurons of the rat by guanine nucleotide analogues and (-)-baclofen. Br. J. Pharmacol., 97: 263–273.
Dunlap, K., and Fischbach, G. D. 1981. Neurotransmitters decrease the calcium conductance activated by depolarization of embryonic sensory neurons. J. Physiol., 317: 519–535.
Dunlap, K., Holz, G. G., and Rane, S. G. 1987. G proteins as regulators of ion channel function. Trends Neurosci., 10: 241–244.
Dutar, P., and Nicoll, R. A. 1988a. Pre-and postsynaptic GABAB receptors in the hippocampus have different pharmacological properties. Neuron, 1: 585–591.
Dutar, P., and Nicoll, R. A. 1988b. A physiological role for GABAB receptors in the CNS. Nature, 332: 156158.
Enna, S. J., and Karbon, E. W. 1987. Receptor regulation: Evidence for a relationship between phospholipid metabolism and neurotransmitter receptor-mediated cAMP formation in brain. Trends Pharmacol. Sci., 8: 21–24.
Gahwiler, B. H., and Brown, D. A. 1985. GABAB-receptor-activated K+ current in voltage-clamped CA3 pyramidal cells in hippocampal cultures. Proc. Natl. Acad. Sci. USA, 82: 1558–1562.
Glossmann, H., and Striessnig, J. 1988. Structure and pharmacology of voltage-dependent calcium channels. ISI Atlas Sci.: Pharmacol., 2: 202–210.
Hablitz, J. J., and Thalmann, R. H. 1987. Conductance changes underlying a late synaptic hyperpolarization in hippocampal CA3 neurons. J. Neurophysiol, 58: 160–179.
Harrison, N. L. 1990. On the presynaptic action of baclofen at inhibitory synapses between cultured rat hippocampal neurones. J. Physiol., 422: 433–446.
Holz, G. G., Rane, S. G., and Dunlap, K. 1986. GTP-binding proteins mediate transmitter inhibition of voltage-dependent calcium channels. Nature, 319: 670–672.
Hunter, M., and Giebisch, G. 1987. Multi-barrelled K channels in renal tubules. Nature, 327: 522–524.
Huston, E., Scott, R. H., and Dolphin, A. C. 1990. A comparison of the effect of calcium channel ligands and GABAB agonists and antagonists on transmitter release and somatic calcium channel currents in cultured neurons. Neuroscience, 38: 721–729.
Hymel, L., Striessnig, J., Glossmann, H., and Schindler, H. 1988. Purified skeletal muscle 1,4-dihydropyridine receptor forms phosphorylation-dependent oligomeric calcium channels in planar bilayers. Proc. Natl. Acad. Sci. USA, 85: 4290–4294.
Innis, R. B., Nestler, E. J., and Aghajanian, G. K. 1988. Evidence for G-protein mediation of serotonin and GABAB induced hyperpolarization of dorsal root raphe neurons. Brain Res., 459: 27–36.
Inoue, M., Matsuo, T., and Ogata, N. 1985. Baclofen activates voltage-dependent and 4-aminopyridine sensitive K’ conductance in guinea-pig hippocampal pyramidal cells maintained in vitro. Br. J. Pharmacol., 84: 833–841.
Kerr, D. I. B., Ong, J., Prager, R. H., Gynther, B. D., and Curtis, D. R. 1987. Phaclofen; a peripheral and central baclofen antagonist. Brain Res., 405: 150–154.
Kerr, D. I. B., Ong, J., Johnston, G. A. R., Abbenante, J., and Prager, R. H. 1988. 2-Hydroxy-saclofen: An improved antagonist at central and peripheral GABAB receptors. Neurosci. Lett., 92: 92–96.
Krishnamurthy, V., Moore, J. B., and Chung, S. H. 1991. On hidden fractal model signal processing. Signal Processing, 24: 177–192.
Krouse, M. E., Schneider, G. T., and Gage, P. W. 1986. A large anion-selective channel has seven conductance levels. Nature, 319: 58–60.
Lambert, N. A., Harrison, N. L., Kerr, D. I. B., Ong, J., Prager, R. H., and Teyler, T. J. 1989. Blockade of the late IPSP in rat CAI hippocampal neurons by 2-hydroxy-saclofen. Neurosci. Lett., 107: 125–128.
Liebovitch, L. S., and Sullivan, J. M. 1987. Fractal analysis of a voltage-dependent potassium channel from cultured mouse hippocampal neurons. Biophys. J., 52: 979–988.
Liebovitch, L. S., Fischbarg, J., and Koniarek, J. P. 1987. Ion channel kinetics: A model based on fractal scaling rather than multistate Markov processes. Math. Biosci., 84: 37–68.
Login, I. S., Pancrazio, J. J., and Kim, Y. I. 1990. Dopamine enhances a voltage-dependent transient K` current in the MMQ cell, a clonal pituitary line expressing functional D2 dopamine receptors. Brain Res., 506: 331–334.
Miller, C. 1982. Open-state substructure of single chloride channels from Torpedo electroplax. Phil. Trans. R. Soc. Lond. B, 299: 401–411.
Newberry, N. R., and Nicoll, R. A. 1984. Direct hyperpolarizing action of baclofen on hippocampal pyramidal cells. Nature, 308: 450–452.
Newberry, N. R., and Nicoll, R. A. 1985. Comparison of the action of baclofen with T-aminobutyric acid on rat hippocampal pyramidal cells in vitro. J. Physiol., 360: 161–185.
Nicoll, R. A., Malenka, R. C., and Kauer, J. A. 1990. Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Physiol. Rev., 70: 513–551.
Olpe, H.-R., Karlsson, G., Pozza, M. F., Brugger, F., Steinmann, M., Van Reissan, H., Fagg, G., Hall, R. G., Froestl, W., and Bittiger, H. 1990. CGP 35348: A centrally active blocker of GABAB receptors. Eur. J. Pharmacol., 187: 27–38.
Padjen, A. L., and Mitsoglou, G. M. 1990. Some characteristics of baclofen-evoked responses of primary afferents in frog spinal cord. Brain Res., 516: 201–207.
Piomelli, D., and Greengard, P. 1990. Lipoxygenase metabolites of arachidonic acid in neuronal transmembrane signalling. Trends Pharmacol. Sci., 11: 367–373.
Premkumar, L. S., Chung, S.-H., and Gage, P. W. I990a. GABA-induced potassium channels in cultured neurons. Proc. R. Soc. Lond. Biol., 241: 153–158.
Premkumar, L. S., Gage, P. W., and Chung, S.-H. 1990b. Coupled potassium channels induced by arachidonic acid in cultured neurons. Proc. R. Soc. Lond. Biol., 242: 17–22.
Rabiner, L. R. 1989. A tutorial on hidden Markov models and selected applications in speech recognition. Proc. IEEE, 77: 257–285.
Rabiner, L. R., and Juang, B. H. 1986. An introduction to hidden Markov models. IEEE ASSP Mag., 3: 4–16.
Rudy, B. 1988. Diversity and ubiquity of K channels. Neuroscience, 25: 729–749.
Saint, D. A., Thomas, T., and Gage, P. W. 1990. GABAB agonists modulate a transient potassium current in cultured mammalian hippocampal neurons. Neurosci. Leu., 118: 9–13.
Seabrook, G. R., Howson, W., and Lacey, M. G. 1990. Electrophysiological characterization of potent agonists and antagonists at pre-and postsynaptic GABAB receptors on neurones in rat brain slices. Br. J. Pharmacol., 101: 949–957.
Sivilotti, L., and Nistri, A. 1990. GABA receptor mechanisms in the central nervous system. Prog. Neurobiol., 36: 35–92.
Stratton, K. R., Cole, A. J., Pritchett, J., Eccles, C. V., Worley, P. F., and Baraban, J. M. 1989. Intrahippocampal injection of pertussis toxin blocks adenosine suppression of synaptic responses. Brain Res., 494: 359–364.
Thalmann, R. H. 1987. Pertussis toxin blocks a late inhibitory postsynaptic potential in hippocampal CA3 neurons. Neurosci. Lett., 82: 41–46.
Thalmann, R. H. 1988. Evidence that guanosine triphosphate (GTP)-binding proteins control a synaptic response in brain: Effect of pertussis toxin and GTPTS on the late inhibitory postsynaptic potential of hippocampal CA3 neurons. J. Neurosci., 8: 4589–4602.
Titterington, D. M., Smith, A. F. M., and Makov, V. E. 1985. Statistical Analysis of Finite Mixture Distributions. Wiley, New York.
Wang, M. Y., and Dun, N. J. 1990. Phaclofen-insensitive presynaptic inhibitory action of (±)-baclofen in neonatal rat motorneurones in vitro. Br. J. Pharmacol., 99: 413–421.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1993 Springer Science+Business Media New York
About this chapter
Cite this chapter
Gage, P.W., Premkumar, L.S., Chung, Sh. (1993). Influence of GABA on Potassium Channels in Hippocampal Neurons. In: Glossmann, H., Striessnig, J. (eds) Methods in Pharmacology. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-2239-0_7
Download citation
DOI: https://doi.org/10.1007/978-1-4757-2239-0_7
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4419-3232-7
Online ISBN: 978-1-4757-2239-0
eBook Packages: Springer Book Archive