Abstract
Current and voltage-clamp techniques were used to study the effects of kainic (KA) and quisqualic (quis) acids on the slow synaptic inhibition evoked by mossy fibre stimulation in CA3 hippocampal pyramidal neurones in vitro. The K+ conductance underlying the slow synaptic inhibition is coupled to a gamma-aminobutyric acid b (GABAb) receptor by a guanosine-triphosphate (GTP)-binding protein. Both KA and quis reduce (after 7–10 min) the slow inhibitory post-synaptic current (IPSC) without changing the reversal potential. They also reduce the cellular response to exogenously applied (±)baclofen and 5-hydroxytryptamine, which are known to activate a similar K+ conductance. We conclude that KA and quis block the post-synaptic K+ conductance underlying the slow IPSC.
Similar content being viewed by others
References
Alger BE (1984) Characteristics of a slow hyperpolarizing synaptic potential in rat hippocampal pyramidal cells in vitro. J Neurophysiol 52:892–910
Alger BE, Nicoll RA (1982) Feed-forward dendritic inhibition in rat hippocampal pyramidal cells studied in vitro. J Physiol (Lond) 328:105–123
Andersen P, Eccles JC, Løyning Y (1964) Pathway of postsynaptic inhibition in the hippocampus. J Neurophysiol 27:608–619
Andrade R, Malenka RC, Nicoll RA (1986) A G protein couples serotonin and GABAB receptors to the same channels in hippocampus. Science 234:1261–1265
Ascher P, Nowak L (1988) Quisqualate- and kainate-activated channels in mouse central neurones in culture. J Physiol (Lond) 399:227–245
Ben-Ari Y, Gho M (1988) Long-lasting induction of an evoked network burst in rat hippocampal CA3 neurones in vitro. J Physiol (Lond) 404:365–384
Ben-Ari Y, Gho M, Rovira C (1988) Kainic acid reduces both the baclofen induced outward current and the late inhibitory postsynaptic current in rat hippocampal CA3 neurones in vitro. J Physiol (Lond) 398:20P
Blaxter TJ, Carlen PL (1985) Pre- and postsynaptic effects of baclofen in the rat hippocampal slice. Brain Res 341:195–199
Brown TH, Johnston D (1983) Voltage-clamp analysis of mossy fiber synaptic input to hippocampal neurons. J Neurophysiol 50:487–507
Brown TH, Fricke RA, Perkel DH (1981) Passive electrical contacts in three classes of hippocampal neurons. J Neurophysiol 46:812–827
Buzsàki G (1984) Feed-forward inhibition in the hippocampal formation. Prog Neurobiol 22:131–153
Carnevale NT, Johnston D (1982) Electrophysiological characterization of remote chemical synapses. J Neurophysiol 47:606–621
Cherubini E, Rovira C, Ben-Ari Y, Nistri A (1989) Effects of kainate on the excitability of rat hippocampal neurones. Epilepsy Res (in press)
Cull-Candy SG, Howe JR, Ogden DC (1988) Noise and single channels activated by excitatory amino acids in rat cerebellar granule neurones. J Physiol (Lond) 400:189–222
Dumuis A, Sebben M, Haynes L, Pin J-P, Bockaert J (1988) NMDA receptor activate the arachidonic cascade system in striatal neurons. Nature 336:68–70
Dutar P, Nicoll RA (1988) A physiological role for GABAb receptors in the central nervous system. Nature 332:156–158
Fisher RS, Alger BE (1984) Electrophysiological mechanisms of kainic acid-induced epileptiform activity in the rat hippocampal slice. J Neurosci 4:1312–1323
Gähwiler BH, Brown DA (1985) GABAb-receptor-activated K+ current in voltage-clamped CA3 pyramidal cells in hippocampal cultures. Proc Natl Acad Sci USA 82:1558–1562
Gho M, King A, Ben-Ari Y, Cherubini E (1986) Kainate reduces two voltage-dependent potassium conductances in rat hippocampal neurons in vitro. Brain Res 385:411–414
Ginsborg BL (1973) Electrical changes in the membrane in junctional transmission. Biochim Biophys Acta 300:289–317
Hablitz JJ, Thalmann RH (1987) Conductance changes underlying a late synaptic hyperpolarization in hippocampal CA3 neurons. J Neurophysiol 58:160–179
Johnston D (1981) Passive cable properties of hippocampal CA3 pyramidal neurons. Cell Mol Neurobiol 1:41–55
Johnston D, Brown TH (1983) Interpretation of voltage-clamp measurements in hippocampal neurons. J Neurophysiol 50:464–486
Kandel ER, Spencer WA, Brinley FJ (1961) Electrophysiology of hippocampal neurons. I. Sequential invasion and synaptic organization. J Neurophysiol 24:225–242
Kehl SJ, McLennan H (1983) Evidence for a bicuculline insensitive long lasting inhibition in the CA3 region of the hippocampal slice. Brain Res 279:278–281
Kehl SJ, McLennan H (1985a) An electrophysiological characterization of inhibitions and postsynaptic potentials in rat hippocampal CA3 neurones in vitro. Exp Brain Res 60:299–308
Kehl SJ, McLennan H (1985b) A pharmacological characterization of chloride- and potassium-dependant inhibitions in the CA3 region of the rat hippocampus in vitro. Exp Brain Res 60:309–317
Kehoe J (1985) Synaptic block of a calcium-activated potassium conductance in aplysia neurones. J Physiol (Lond) 369:439–474
Knowles WD, Schneiderman JH, Wheal HV, Straftrom CE, Schartzkroin PA (1984) Hyperpolarizing potentials in guinea pig hippocampal CA3 neurons. Cell Mol Neurobiol 4:207–230
Mayer ML, Westbrook GL (1984) Mixed-agonist action of excitatory amino acids on mouse spinal cord neurones under voltage clamp. J Physiol (Lond) 354:29–53
Miles R, Wong RKS (1987) Inhibitory control of local excitatory circuits in the guinea pig hippocampus. J Physiol (Lond) 388:611–629
Newberry NR, Nicoll RA (1985b) A bicuculline-resistant inhibitory post-synaptic potential in rat hippocampal pyramidal cells in vitro. J Physiol (Lond) 348:239–254
Newberry NR, Nicoll RA (1985b) Comparison of the action of baclofen with γ-aminobutyric acid on rat hippocampal pyramidal cells in vitro. J Physiol (Lond) 360:161–185
Nicoll RA (1988) The coupling of neurotransmitter receptors to ion channels in the brain. Science 241:545–551
Nicoll RA, Kauer JA, Malenka RC (1988) The current excitement in long-term potentiation. Neuron 1:97–103
Nistri A, Constanti A (1979) Pharmacological characterization of different types of GABA and glutamate receptors in vertebrates and invertebrates. Prog Neurobiol 13:117–235
Repressa A, Tremblay E, Ben-Ari Y (1987) Kainate binding sites in the hippocampal mossy fibers: location and plasticity. Neuro-science 20:739–748
Reynolds JN, Baskys A, Carlen PL (1988) The effects of serotonin on N-methyl-Rosad-asparate and synaptically evoked depolarization in rat neocortical neurons. Brain Res 456:286–292
Robinson JH, Deadwyler SA (1981) Kainic acid produces depolarization of CA3 pyramidal cells in the in vitro hippocampal slice. Brain Res 221:117–127
Sladeczek F, Recasens M, Bockaert J (1988) A new mechanism for glutamate receptor action: phosphoinositide hydrolysis. Trends Neurosci 11:545–549
Soltesz Y, Haby M, Leresche N, Crunelli V (1988) GABAb antagonist inhibits the late potassium dependant IPSP in cat and rat thalamic and hippocampal neurons. Brain Res 448:351–354
Stelzer A, Wong RKS (1989) GABAA responses in hippocampal neurons are potentiated by glutamate. Nature 337:170–173
Stelzer A, Slater NT, Bruggencate G (1987) Activation of NMDA receptors blocks GABAergic inhibition in an in vitro model of epilepsy. Nature 326:698–701
Thalmann RH (1987) Pertussis toxin blocks a late inhibitory postsynaptic potential in hippocampal CA3 neurons. Neurosci Lett 82:41–46
Thalmann RH, Ayala GF (1982) A late increase in potassium conductance follows synaptic stimulation of granule neurons of the dentate gyrus. Neurosci Lett 9:243–248
Trussell LO, Jackson MB (1987) Dependence of an adenosine-activated potassium current on a GTP-binding protein in mammalian central neurons. J Neurosci 7:3306–3316
Watkins JC, Olverman HJ (1987) Agonists and antagonists for excitatory amino acid receptors. Trends Neurosci 10:265–272
Westbrook GL, Lothman EW (1983) Cellular and synaptic basis of kainic acid-induced hippocampal epileptiform activity. Brain Res 273:97–109
Wong RKS, Traub RD (1983) Synchronized bursts discharge in disinhibited hippocampal slice I Initiation in the CA2–CA3 region. J Neurophysiol 49:442–458
Wong RKS, Prince CA, Basbaum AI (1979) Intradendritic recordings from hippocampal neurons. Proc Natl Acad Sci USA 76:986–990
Worley PF, Baraban JM, McCarren M, Snyder SH, Alger BE (1987) Cholinergic phosphatidylinositol modulation of inhibitory, G protein-linked, neurotransmitter actions: electrophysiological studies in rat hippocampus. Proc Natl Acad Sci USA 84:3467–3471
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Rovira, C., Gho, M. & Ben-Ari, Y. Block of GABAb-activated K+ conductance by kainate and quisqualate in rat CA3 hippocampal pyramidal neurones. Pflügers Arch 415, 471–478 (1990). https://doi.org/10.1007/BF00373625
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00373625