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Fast and Slow GABAergic Transmission in Hippocampal Circuits

  • Chapter
Hippocampal Microcircuits

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 5))

Abstract

Cortical neuronal networks consist of excitatory glutamatergic principal cells and a heterogeneous group of GABAergic inhibitory interneurons. Interneurons are embedded in feedforward and feedback microcircuits and control key aspects of cortical network function including the timing of the activation of principal cells and the generation of network oscillations (Freund and Buzsáki, 1996; McBain and Fisahn, 2001; Klausberger and Somogyi, 2008). Although interneurons comprise only 10% of the neuronal population, they are highly diverse and can be subdivided into several types on the basis of various criteria, such as intrinsic physiological properties, neurochemical marker content, morphological features, including the laminar distribution of the axon, and finally the postsynaptic target profile of their output (Freund and Buzsáki, 1996; Avoli et al., 2006). On the basis of synaptic targets, interneurons have been classified into two major groups, perisomatic- and dendrite-targeting cells.

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Further Reading

  • Alger BE, Nicoll RA (1979) GABA-mediated biphasic inhibitory responses in hippocampus. Nature 281:315–317.

    CAS  PubMed  Google Scholar 

  • Andersen P, Dingledine R, Gjerstad L, Langmoen IA, Laursen AM (1980) Two different responses of hippocampal pyramidal cells to application of gamma-amino butyric acid. J Physiol Lond 305:279–296.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Avoli M, Biagini G, de Curtis M (2006) Do interictal spikes sustain seizures and epileptogenesis? Epilepsy Curr 6:203–207.

    PubMed  Google Scholar 

  • Banke TG, McBain CJ (2006) GABAergic input onto CA3 hippocampal interneurons remains shunting throughout development. J Neurosci 26:11720–11725.

    CAS  PubMed  Google Scholar 

  • Banks MI, Li TB, Pearce RA (1998) The synaptic basis of GABAA, slow. J Neurosci 18:1305–1317.

    CAS  PubMed  Google Scholar 

  • Bartos M, Vida I, Frotscher M, Geiger JRP, Jonas P (2001) Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J Neurosci 21:2687–2698.

    CAS  PubMed  Google Scholar 

  • Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JRP, Jonas P (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in τ hippocampal interneuron networks. Proc Natl Acad Sci USA 99:13222–13227.

    CAS  PubMed  Google Scholar 

  • Bartos M, Vida I, Jonas P (2007) Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8:45–56.

    CAS  PubMed  Google Scholar 

  • Bettler B, Kaupmann K, Mosbacher J, Gassmann M (2004) Molecular structure and physiological functions of GABA(B) receptors. Physiol Rev 84:835–867.

    CAS  PubMed  Google Scholar 

  • Billinton A, Ige AO, Bolam JP, White JH, Marshall FH, Emson PC (2001) Advances in the molecular understanding of GABAB receptors. Trends Neurosci 24:277–282.

    CAS  PubMed  Google Scholar 

  • Bischoff S, Leonhard S, Reymann N, Schuler V, Shigemoto R, Kaupmann K, Bettler B (1999) Spatial distribution of GABA(B)R1 receptor mRNA and binding sites in the rat brain. J Comp Neurol 412:1–16.

    CAS  PubMed  Google Scholar 

  • Blasco-Ibáñez JM, Freund TF (1995) Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CA1 subfield: structural basis of feed-back activation. Eur J Neurosci 7:2170–2180.

    PubMed  Google Scholar 

  • Bowery NG, Brown DA (1997) The cloning of GABA(B) receptors. Nature 386:223–224.

    CAS  PubMed  Google Scholar 

  • Bucurenciu I, Kulik A, Schwaller B, Frotscher M, Jonas P (2008) Nanodomain coupling between Ca2+ channels and Ca2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse. Neuron 57:536–545.

    CAS  PubMed  Google Scholar 

  • Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823–828.

    CAS  PubMed  Google Scholar 

  • Buhl EH, Cobb SR, Halasy K, Somogyi P (1995) Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. Eur J Neurosci 7:1989–2004.

    CAS  PubMed  Google Scholar 

  • Buzsáki G (1996) The hippocampo-neocortical dialogue. Cereb Cortex 6:81–92.

    PubMed  Google Scholar 

  • Calver AR, Davies CH, Pangalos M (2002) GABA(B) receptors: From monogamy to promiscuity. Neurosignals 11:299–314.

    CAS  PubMed  Google Scholar 

  • Chavas J, Marty A (2003) Coexistence of excitatory and inhibitory GABA synapses in the cerebellar interneuron network. J Neurosci 23:2019–2031.

    CAS  PubMed  Google Scholar 

  • Chu DCM, Albin RL, Young AB, Penney JB (1990) Distribution and kinetics of GABAB binding sites in rat central nervous system: A quantitative autoradiographic study. Neuroscience 34:341–357.

    CAS  PubMed  Google Scholar 

  • Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75–78.

    CAS  PubMed  Google Scholar 

  • Cope DW, Halbsguth C, Karayannis T, Wulff P, Ferraguti F, Hoeger H, Leppä E, Linden AM, Oberto A, Ogris W, Korpi ER, Sieghart W, Somogyi P, Wisden W, Capogna M (2005) Loss of zolpidem efficacy in the hippocampus of mice with the GABAA receptor gamma2 F77I point mutation. Eur J Neurosci 21:3002–3016.

    CAS  PubMed  Google Scholar 

  • Dascal N (1997) Signalling via the G protein-activated K+ channels. Cell Signal 9:551–573.

    CAS  PubMed  Google Scholar 

  • Davies CH, Collingridge GL. (1993) The physiological regulation of synaptic inhibition by GABAB autoreceptors in rat hippocampus. J Physiol 1993 Dec;472:245–65.

    CAS  Google Scholar 

  • Davies CH, Davies SN, Collingridge GL (1990) Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. J Physiol Lond 424:513–531.

    CAS  PubMed  Google Scholar 

  • Davies CH, Starkey SJ, Pozza MF, Collingridge GL (1991) GABA autoreceptors regulate the induction of LTP. Nature 349:609–611.

    CAS  PubMed  Google Scholar 

  • Doischer D, Hosp JA, Yanagawa Y, Obata K, Jonas P, Vida I, Bartos M (2008) Postnatal differentiation of basket cells from slow to fast signaling devices. J Neurosci 28:12956–12968.

    CAS  PubMed  Google Scholar 

  • Duprat F, Lesage F, Guillemare E, Fink M, Hugnot J-P, Bigay J, Lazdunski M, Romey G, Barhanin J (1995) Heterologous multimeric assembly is essential for K+ channel activity of neuronal and cardiac G-protein-activated inward rectifiers. Biochem Biophys Res Commun 212:657–663.

    CAS  PubMed  Google Scholar 

  • Dutar P, Nicoll RA (1988) Pre- and postsynaptic GABAB receptors in the hippocampus have different pharmacological properties. Neuron 1:585–591.

    CAS  PubMed  Google Scholar 

  • Elfant D, Pál BZ, Emptage N, Capogna M (2008) Specific inhibitory synapses shift the balance from feedforward to feedback inhibition of hippocampal CA1 pyramidal cells. Eur J Neurosci 27:104–113.

    PubMed  Google Scholar 

  • Földy C, Neu A, Jones MV, Soltesz I (2006) Presynaptic, activity-dependent modulation of cannabinoid type 1 receptor-mediated inhibition of GABA release. J Neurosci 26:1465–1469.

    PubMed  Google Scholar 

  • Freund TF (2003) Interneuron diversity series: Rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489–495.

    CAS  PubMed  Google Scholar 

  • Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347–470.

    CAS  PubMed  Google Scholar 

  • Fritschy J-M, Möhler H (1995) GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359:154–194.

    CAS  PubMed  Google Scholar 

  • Fritschy JM, Meskenaite V, Weinmann O, Honer M, Benke D, Möhler H (1999) GABAB-receptor splice variants GB1a and GB1b in rat brain: Developmental regulation, cellular distribution and extrasynaptic localization. Eur J Neurosci 11:761–768.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Gao B, Fritschy JM (1994) Selective allocation of GABAA receptors containing the alpha 1 subunit to neurochemically distinct subpopulations rat hippocampal interneurons. Eur J Neurosci 6:837–853.

    CAS  PubMed  Google Scholar 

  • Geiger JR, Jonas P (2000) Dynamic control of presynaptic Ca2+ inflow by fast-activating K+ channels in hippocampal mossy fiber boutons. Neuron 28:927–939.

    CAS  PubMed  Google Scholar 

  • Glickfeld LL, Scanziani M (2006) Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells. Nat Neurosci 9:807–815.

    CAS  PubMed  Google Scholar 

  • Glickfeld LL, Atallah BV, Scanziani M (2008) Complementary modulation of somatic inhibition by opioids and cannabinoids. J Neurosci 28:1824–1832.

    CAS  PubMed  Google Scholar 

  • Glickfeld LL, Roberts JD, Somogyi P, Scanziani M (2009) Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis. Nat Neurosci 12:21–23.

    CAS  PubMed  Google Scholar 

  • Glykys J, Mann EO, Mody I (2008) Which GABA(A) receptor subunits are necessary for tonic inhibition in the hippocampus? J Neurosci 6:1421–1426.

    Google Scholar 

  • Guetg N, Seddik R, Vigot R, Turecek R, Gassmann M, Vogt KE, Bräuner-Osborne H, Shigemoto R, Kretz O, Frotscher M, Kulik A, Bettler B (2009) The GABAB1a isoform mediatesheterosynaptic depression at hippocampal mossy fiber synapses. J Neurosci 29:1414–1423.

    CAS  PubMed  Google Scholar 

  • Gulledge AT, Stuart GJ (2003) Excitatory actions of GABA in the cortex. Neuron 37:299–309.

    CAS  PubMed  Google Scholar 

  • Gulyás AI, Miles R, Hájos N, Freund TF (1993) Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur J Neurosci 5:1729–1751.

    PubMed  Google Scholar 

  • Häusser M, Roth A (1997) Estimating the time course of the excitatory synaptic conductance in neocortical pyramidal cells using a novel voltage jump method. J Neurosci 17: 7606–7625.

    PubMed  Google Scholar 

  • Han Z, Buhl E, Lörinczi Z, Somogyi P (1993) A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Euro J Neurosci 5:396–410.

    Google Scholar 

  • Harney SC, Jones MV (2002) Pre- and postsynaptic properties of somatic and dendritic inhibition in dentate gyrus. Neuropharmacology 43:584–594.

    CAS  PubMed  Google Scholar 

  • Harrison NL (1990) On the presynaptic action of baclofen at inhibitory synapses between cultured rat hippocampal neurones. J Physiol Lond 422:433–446.

    CAS  PubMed  Google Scholar 

  • Hefft S, Jonas P (2005) Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8:1319–1328.

    CAS  PubMed  Google Scholar 

  • Huang CS, Shi S-H, Ule J, Ruggiu M, Barker LA, Darnell RB, Jan YN, Jan LY (2005) Common molecular pathways mediate long-term potentiation of synaptic excitation and slow synaptic inhibition. Cell 123:105–118.

    CAS  PubMed  Google Scholar 

  • Inanobe A, Ito H, Ito M, Hosoya Y, Kurachi Y (1995) Immunological and physical characterization of the brain G protein-gated muscarinic potassium channel. Biochem Biophys Res Commun 217:1238–1244.

    CAS  PubMed  Google Scholar 

  • Inanobe A, Yoshimoto Y, Horio Y, Morishige K-I, Hibino H, Matsumoto S, Tokunaga Y, Maeda T, Hata Y, Takai Y, Kurachi Y (1999) Characterization of G-protein-gated K+ channels composed of Kir3.2 subunits in dopaminergic neurons of the substantia nigra. J Neurosci 19:1006–1013.

    CAS  PubMed  Google Scholar 

  • Isaacson JS, Solís JM, Nicoll RA (1993) Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 10:165–175.

    CAS  PubMed  Google Scholar 

  • Isomoto S, Kaibara M, Sakurai-Yamashita Y, Nagayama Y, Uezono Y, Yano K, Taniyama K (1998) Cloning and tissue distribution of novel splice variants of the rat GABAB receptor. Biochem Biophys Res Commun 253:10–15.

    CAS  PubMed  Google Scholar 

  • Johnston D, Brown TH (1983) Interpretation of voltage-clamp measurements in hippocampal neurons. J Neurophysiol 50:464–486.

    CAS  PubMed  Google Scholar 

  • Jones KA, Borowsky B, Tamm JA, Craig DA, Durkin MM, Dai M, Yao WJ, Johnson M, Gunwaldsen C, Huang LY, Tang C, Shen Q, Salon JA, Morse K, Laz T, Smith KE, Nagarathnam D, Noble SA, Branchek TA, Gerald C (1998) GABA(B) receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GABA(B)R2. Nature 396:674–679.

    CAS  PubMed  Google Scholar 

  • Katona I, Acsády L, Freund TF (1999) Postsynaptic targets of somatostatin-immunoreactive interneurons in the rat hippocampus. Neuroscience 88:37–55.

    CAS  PubMed  Google Scholar 

  • Kaupmann K, Huggel K, Heid J, Flor PJ, Bischoff S, Mickel SJ, McMaster G, Angst C, Bittiger H, Froestl W, Bettler B (1997) Expression cloning of GABA(B) receptors uncovers similarity to metabotropic glutamate receptors. Nature 386:239–246.

    CAS  PubMed  Google Scholar 

  • Kaupmann K, Malitschek B, Schuler V, Heid J, Froestl W, Beck P, Mosbacher J, Bischoff S, Kulik A, Shigemoto R, Karschin A, Bettler B (1998) GABA(B)-receptor subtypes assemble into functional heteromeric complexes. Nature 396:683–687.

    CAS  PubMed  Google Scholar 

  • Khazipov R, Congar P, Ben-Ari Y (1995) Hippocampal CA1 lacunosum-moleculare interneurons: Modulation of monosynaptic GABAergic IPSCs by presynaptic GABAB receptors. J Neurophysiol 74:2126–2137.

    CAS  PubMed  Google Scholar 

  • Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: The unity of hippocampal circuit operations. Science.321:53–57.

    CAS  PubMed  Google Scholar 

  • Klausberger T, David J, Roberts B, Somogyi P (2002). Cell type- and input-specific differences in the number and subtypes of synaptic GABAA receptors in the hippocampus. J Neurosci 22:2513–2521.

    CAS  PubMed  Google Scholar 

  • Kofuji P, Davidson N, Lester HA (1995) Evidence that neuronal G-protein-gated inwardly rectifying K+ channels are activated by G beta gamma subunits and function as heteromultimers. Proc Natl Acad Sci USA 92:6542–6546.

    CAS  PubMed  Google Scholar 

  • Koyrakh L, Luján R, Colón J, Karschin C, Kurachi Y, Karschin A, Wickman K (2005) Molecular and cellular diversity of neuronal G-protein-gated potassium channels. J Neurosci 25:11468–11478.

    CAS  PubMed  Google Scholar 

  • Krapivinsky G, Gordon EA, Wickman K, Velimirović B, Krapivinsky L, Clapham DE (1995) The G-protein-gated atrial K+ channel IKACh is a heteromultimer of two inwardly rectifying K(+)-channel proteins. Nature 374:135–141.

    CAS  PubMed  Google Scholar 

  • Kraushaar U, Jonas P (2000) Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse. J Neurosci 20:5594–5607.

    CAS  PubMed  Google Scholar 

  • Kulik A, Nakadate K, Nyíri G, Notomi T, Malitschek B, Bettler B, Shigemoto R (2002) Distinct localization of GABA(B) receptors relative to synaptic sites in the rat cerebellum and ventrobasal thalamus. Eur J Neurosci 15:291–307.

    PubMed  Google Scholar 

  • Kulik A, Vida I, Luján R, Haas CA, López-Bendito G, Shigemoto R, Frotscher M (2003) Subcellular localization of metabotropic GABAB receptor subunits GABAB1a/b and GABAB2 in the rat hippocampus. J Neurosci 23:11026–11035.

    CAS  PubMed  Google Scholar 

  • Kulik A, Vida I, Fukazawa Y, Guetg N, Kasugai Y, Marker CL, Rigato F, Bettler B, Wickman K, Frotscher M, Shigemoto R (2006) Compartment-dependent colocalization of Kir3.2-containing K+ channels and GABAB receptors in hippocampal pyramidal cells. J Neurosci 26:4289–4297.

    CAS  PubMed  Google Scholar 

  • Kuner R, Köhr G, Grünewald S, Eisenhardt G, Bach A, Kornau HC (1999) Role of heteromer formation in GABAB receptor function. Science 283:74–77.

    CAS  PubMed  Google Scholar 

  • Kyrozis A, Reichling DB (1995) Perforated-patch recording with gramicidin avoids artifactual changes in intracellular chloride concentration. J Neurosci Methods 57:27–35.

    CAS  PubMed  Google Scholar 

  • Lamsa K, Taira T (2003) Use-dependent shift from inhibitory to excitatory GABAA receptor action in SP-O interneurons in the rat hippocampal CA3 area. J Neurophysiol 90:1983–1995.

    CAS  PubMed  Google Scholar 

  • Lavoie AM, Tingey JJ, Harrison NL, Pritchett DB, Twyman RE (1997) Activation and deactivation rates of recombinant GABAA receptor channels are dependent on alpha-subunit isoform. Biophys J 73:2518–2526.

    CAS  PubMed  Google Scholar 

  • Leaney JL (2003) Contribution of Kir3.1, Kir3.2A and Kir3.2C subunits to native G protein-gated inwardly rectifying potassium currents in cultured hippocampal neurons. Eur J Neurosci 18:2110–2118.

    PubMed  Google Scholar 

  • Lei S, McBain CJ (2003) GABA B receptor modulation of excitatory and inhibitory synaptic transmission onto rat CA3 hippocampal interneurons. J Physiol Lond 546:439–453.

    CAS  PubMed  Google Scholar 

  • Lesage F, Guillemare E, Fink M, Duprat F, Heurteaux C, Fosset M, Roemy G, Barhanin J, Lazdunski M (1995) Molecular properties of neuronal G-protein-activated inwardly rectifying K+ channels. J Biol Chem 270:28660–28667.

    CAS  PubMed  Google Scholar 

  • Liao YJ, Jan YN, Jan LY (1996) Heteromultimerization of G-protein-gated inwardly rectifying K+ channel proteins GIRK1 and GIRK2 and their altered expression in weaver brain. J Neurosci 16:7137–7150.

    CAS  PubMed  Google Scholar 

  • Ling DS, Benardo LS (1994) Properties of isolated GABAB-mediated inhibitory postsynaptic currents in hippocampal pyramidal cells. Neuroscience 63:937–944.

    CAS  PubMed  Google Scholar 

  • Losonczy A, Biró AA, Nusser Z (2004) Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons. Proc Natl Acad Sci USA 101:1362–1367.

    CAS  PubMed  Google Scholar 

  • Lüscher C, Jan LY, Stoffel M, Malenka RC, Nicoll RA (1997) G protein-coupled inwardly rectifying K+ channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19:687–695.

    PubMed  Google Scholar 

  • Ma D, Zerrangue N, Raab-Graham K, Fried SR, Jan YN, Jan LY (2002) Diverse trafficking patterns due to multiple traffic motifs in G protein-activated inwardly rectifying potassium channels from brain and heart. Neuron 33:715–729.

    CAS  PubMed  Google Scholar 

  • Maccaferri G, Roberts JD, Szucs P, Cottingham CA, Somogyi P (2000) Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J Physiol Lond 524:91–116.

    CAS  PubMed  Google Scholar 

  • Major G, Evans JD, Jack JJB (1993) Solutions for transients in arbitrarily branching cables: II. Voltage clamp theory. Biophys J 65:450–468.

    CAS  Google Scholar 

  • Malinow R, Tsien RW (1990) Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346:177–180.

    CAS  PubMed  Google Scholar 

  • Mann EO, Suckling JM, Hajos N, Greenfield SA, Paulsen O (2005) Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro. Neuron 45:105–117.

    CAS  PubMed  Google Scholar 

  • Margeta-Mitrovic M, Mitrovic I, Riley RC, Jan LY, Basbaum AI (1999) Immunohistochemical localization of GABA(B) receptors in the rat central nervous system. J Comp Neurol 405:299–321.

    CAS  PubMed  Google Scholar 

  • Marshall FH, White J, Main M, Green A, Wise A (1999) GABA(B) receptors function as heterodimers. Biochem Soc Trans 27:530–535.

    CAS  PubMed  Google Scholar 

  • Martina M, Royer S, Paré D (2001) Cell-type-specific GABA responses and chloride homeostasis in the cortex and amygdala. J Neurophysiol 86:2887–2895.

    CAS  PubMed  Google Scholar 

  • Mátyás F, Freund TF, Gulyás AI (2004) Immunocytochemically defined interneuron populations in the hippocampus of mouse strains used in transgenic technology. Hippocampus.14:460–481.

    PubMed  Google Scholar 

  • McBain CJ, Fisahn A (2001) Interneurons unbound. Nat Rev Neurosci 2:11–23.

    CAS  PubMed  Google Scholar 

  • Megías M, Emri Z, Freund TF, Gulyás AI (2001) Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102:527–540.

    PubMed  Google Scholar 

  • Miles R, Tóth K, Gulyás AI, Hájos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815–823.

    CAS  PubMed  Google Scholar 

  • Mitchell SJ, Silver RA (2003) Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38:433–445.

    CAS  PubMed  Google Scholar 

  • Mittmann W, Koch U, Häusser M (2005) Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J Physiol Lond 563:369–378.

    CAS  PubMed  Google Scholar 

  • Mott DD, Lewis DV (1991) Facilitation of the induction of long-term potentiation by GABAB receptors. Science 252:1718–1720.

    CAS  PubMed  Google Scholar 

  • Mott DD, Li Q, Okazaki MM, Turner DA, Lewis DV (1999) GABAB-receptor-mediated currents in interneurons of the dentate-hilus border. J Neurophysiol 82:1438–1450.

    CAS  PubMed  Google Scholar 

  • Neu A, Földy C, Soltesz I (2007) Postsynaptic origin of CB1-dependent tonic inhibition of GABA release at cholecystokinin-positive basket cell to pyramidal cell synapses in the CA1 region of the rat hippocampus. J Physiol Lond 578:233–247.

    CAS  PubMed  Google Scholar 

  • Newberry NR, Nicoll RA (1984) Direct hyperpolarizing action of baclofen on hippocampal pyramidal cells. Nature 308:450–452.

    CAS  PubMed  Google Scholar 

  • Newberry NR, Nicoll RA (1985) Comparison of the action of baclofen with γ–aminobutyric acid on rat hippocampal pyramidal cells in vitro. J Physiol Lond 360:161–185.

    CAS  PubMed  Google Scholar 

  • Nusser Z, Somogyi P (1997) Compartmentalised distribution of GABAA and glutamate receptors in relation to transmitter release sites on the surface of cerebellar neurones. Prog Brain Res 114:109–127.

    CAS  PubMed  Google Scholar 

  • Nusser Z, Mody I (2002) Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol 87:2624–2628.

    CAS  PubMed  Google Scholar 

  • Nyíri G, Freund TF, Somogyi P (2001) Input-dependent synaptic targeting of alpha(2)-subunit-containing GABA(A) receptors in synapses of hippocampal pyramidal cells of the rat. Eur J Neurosci 13:428–442.

    PubMed  Google Scholar 

  • Otis TS, De Koninck Y, Mody I (1993) Characterization of synaptically elicited GABAB responses using patch-clamp recordings in rat hippocampal slices. J Physiol Lond 463:391–407.

    CAS  PubMed  Google Scholar 

  • Otmakhova NA, Lisman JE (2004) Contribution of Ih and GABAB to synaptically induced afterhyperpolarizations in CA1: A brake on the NMDA response. J Neurophysiol 92:2027–2039.

    CAS  PubMed  Google Scholar 

  • Overstreet-Wadiche L, Bromberg DA, Bensen AL, Westbrook GL (2005) GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol 94:4528–4532.

    PubMed  Google Scholar 

  • Pearce RA (1993) Physiological evidence for two distinct GABAA responses in rat hippocampus. Neuron 10:189–200.

    CAS  PubMed  Google Scholar 

  • Pfaff T, Malitschek B, Kaupmann K, Prézeau L, Pin JP, Bettler B, Karschin A (1999) Alternative splicing generates a novel isoform of the rat metabotropic GABA(B)R1 receptor. Eur J Neurosci 11:2874–2882.

    CAS  PubMed  Google Scholar 

  • Pouille F, Scanziani M (2001) Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293:1159–1163.

    CAS  PubMed  Google Scholar 

  • Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R, Capogna M (2005) Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 25:6775–6786.

    CAS  PubMed  Google Scholar 

  • Price CJ, Scott R, Rusakov DA, Capogna M (2008) GABA(B) receptor modulation of feedforward inhibition through hippocampal neurogliaform cells. J Neurosci 28:6974–6982.

    CAS  PubMed  Google Scholar 

  • Rall W, Segev I (1985) Space-clamp problems when voltage clamping branched neurons with intracellular microelectrodes. In: Smith Jr TG, Lecar H, Redman SJ, Gage P (eds) Voltage and patch clamping with microelectrodes, pp 191–215. American Physiological Society, Bethesda, MD.

    Google Scholar 

  • Riekki R, Pavlov I, Tornberg J, Lauri SE, Airaksinen MS, Taira T (2008) Altered synaptic dynamics and hippocampal excitability but normal long-term plasticity in mice lackinghyperpolarizing GABA A receptor-mediated inhibition in CA1 pyramidal neurons. J Neurophysiol 99:3075–3089.

    PubMed  Google Scholar 

  • Sauer J-F, Bartos M (2010) Recruitment of early postnatal PV+ hippocampal interneurons by GABAergic excitation. J Neurosci, in press.

    Google Scholar 

  • Scanziani M (2000) GABA spillover activates postsynaptic GABAB receptors to control rhythmic hippocampal activity. Neuron 25:673–681.

    CAS  PubMed  Google Scholar 

  • Scholz KP, Miller RJ (1991) GABAB receptor-mediated inhibition of Ca2+ currents and synaptic transmission in cultured rat hippocampal neurones. J Physiol Lond 444:669–686.

    CAS  PubMed  Google Scholar 

  • Schwarz DA, Barry G, Eliasof SD, Petroski RE, Conlon PJ, Maki RA (2000) Characterization of γ-aminobutyric acid receptor GABAB(1e), a GABAB(1) splice variant encoding a truncated receptor. J Biol Chem 275:32174–32181.

    CAS  PubMed  Google Scholar 

  • Scimemi A, Semyanov A, Sperk G, Kullmann DM, Walker MC. (2005) Multiple and plastic receptors mediate tonic GABAA receptor currents in the hippocampus. J Neurosci 25:10016–24.

    CAS  PubMed  Google Scholar 

  • Signorini S, Liao YJ, Duncan SA, Jan LY, Stoffel M (1997) Normal cerebellar development but susceptibility to seizures in mice lacking G protein-coupled, inwardly rectifying K+ channel GIRK2. Proc Natl Acad Sci USA 94:923–927.

    CAS  PubMed  Google Scholar 

  • Sik A, Penttonen M, Ylinen A, Buzsáki G (1995) Hippocampal CA1 interneurons: An in vivo intracellular labeling study. J Neurosci 15:6651–6665.

    CAS  PubMed  Google Scholar 

  • Slesinger PA, Patil N, Liao J, Jan YN, Jan LY, Cox DR (1996) Functional effects of the mouse weaver mutation on G protein-gated inwardly rectifying K+ channels. Neuron 16:321–331.

    CAS  PubMed  Google Scholar 

  • Sloviter RS, Ali-Akbarian L, Elliott RC, Bowery BJ, Bowery NG (1999) Localization of GABA(B) (R1) receptors in the rat hippocampus by immunocytochemistry and high resolution autoradiography, with specific reference to its localization in identified hippocampal interneuron subpopulations. Neuropharmacology 38:1707–1721.

    CAS  PubMed  Google Scholar 

  • Sodickson DL, Bean BP (1996) GABAB receptor-activated inwardly rectifying potassium current in dissociated hippocampal CA3 neurons. J Neurosci 16:6374–6385.

    CAS  PubMed  Google Scholar 

  • Sohal VS, Hasselmo ME (1998) GABA(B) modulation improves sequence disambiguation in computational models of hippocampal region CA3. Hippocampus 8:171–193.

    CAS  PubMed  Google Scholar 

  • Solís JM, Nicoll RA (1992) Pharmacological characterization of GABAB-mediated responses in the CA1 region of the rat hippocampal slice. J Neurosci 12:3466–3472.

    PubMed  Google Scholar 

  • Somogyi P, Freund TF, Hodgson AJ, Somogyi J, Beroukas D, Chubb IW (1985) Identified axo-axonic cells are immunoreactive for GABA in the hippocampus and visual cortex of cat. Brain Res 332:143–149.

    CAS  PubMed  Google Scholar 

  • Soriano E, Nitsch R, Frotscher M (1990) Axo-axonic chandelier cells in the rat fascia dentata: Golgi-electron microscopy and immunocytochemical studies. J Comp Neurol 293:1–25.

    CAS  PubMed  Google Scholar 

  • Spauschus A, Lentes KU, Wischmeyer E, Dissmann E, Karschin C, Karschin A (1996) A G-protein-activated inwardly rectifying K+ channel (GIRK4) from human hippocampus associates with other GIRK channels. J Neurosci 16:930–938.

    CAS  PubMed  Google Scholar 

  • Staley KJ, Mody I (1992) Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor-mediated postsynaptic conductance. J Neurophysiol 68:197–212.

    CAS  PubMed  Google Scholar 

  • Szabadics J, Varga C, Molnár G, Oláh S, Barzó P, Tamás G (2006) Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311:233–235.

    CAS  PubMed  Google Scholar 

  • Szabadics J, Tamás G, Soltesz I (2007) Different transmitter transients underlie presynaptic cell type specificity of GABAA,slow and GABAA,fast. Proc Natl Acad Sci USA 104:14831–14836.

    CAS  PubMed  Google Scholar 

  • Tamás G, Lorincz A, Simon A, Szabadics J (2003) Identified sources and targets of slow inhibition in the neocortex. Science 299:1902–1905.

    PubMed  Google Scholar 

  • Takahashi T, Kajikawa Y, Tsujimoto T (1998) G-protein coupled modulation of presynaptic calcium currents and transmitter release by a GABAB receptor. J Neurosci 18:3138–3146.

    CAS  PubMed  Google Scholar 

  • Thompson SM, Gähwiler BH (1992) Comparison of the actions of baclofen at pre- and postsynaptic receptors in the rat hippocampus in vitro. J Physiol Lond 451:329–345.

    CAS  PubMed  Google Scholar 

  • Thomson AM, Bannister AP, Hughes DI, Pawelzik H (2000) Differential sensitivity to zolpidem of IPSPs activated by morphologically identified CA1 interneurons in slices of rat hippocampus. Eur J Neurosci 12:425–436.

    CAS  PubMed  Google Scholar 

  • Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 6:803–815.

    Google Scholar 

  • Tyzio R, Minlebaev M, Rheims S, Ivanov A, Jorquera I, Holmes GL, Zilberter Y, Ben-Ari Y, Khazipov R (2008) Postnatal changes in somatic γ-aminobutyric acid signalling in the rat hippocampus. Eur J Neurosci 27:2515–2528.

    PubMed  Google Scholar 

  • Vida I, Frotscher M (2000) A hippocampal interneuron associated with the mossy fiber system. Proc Natl Acad Sci USA 97:1275–1280.

    CAS  PubMed  Google Scholar 

  • Vida I, Halasy K, Szinyei C, Somogyi P, Buhl EH (1998) Unitary IPSPs evoked by interneurons at the stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J Physiol 506:755–773.

    CAS  PubMed  Google Scholar 

  • Vida I, Bartos M, Jonas P (2006) Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 49:107–117.

    CAS  PubMed  Google Scholar 

  • Vigot R, Barbieri S, Bräuner-Osborne H, Turecek R, Shigemoto R, Zhang YP, Luján R, Jacobson LH, Biermann B, Fritschy JM, Vacher CM, Müller M, Sansig G, Guetg N, Cryan JF, Kaupmann K, Gassmann M, Oertner TG, Bettler B (2006) Differential compartmentalization and distinct functions of GABAB receptor variants. Neuron 50:589–601.

    CAS  PubMed  Google Scholar 

  • Vogt KE, Nicoll RA (1999) Glutamate and γ-aminobutyric acid mediate a heterosynaptic depression at mossy fiber synapses in the hippocampus. Proc Natl Acad Sci USA 96:1118–1122.

    CAS  PubMed  Google Scholar 

  • White JH, Wise A, Main MJ, Green A, Fraser NJ, Disney GH, Barnes AA, Emson P, Foord SM, Marshall FH (1998) Heterodimerization is required for the formation of a functional GABA(B) receptor. Nature 396:679–682.

    CAS  PubMed  Google Scholar 

  • Wei K, Jia Z, Wang YT, Yang J, Liu CC, Snead OC III (2001) Cloning and characterization of a novel variant of rat GABA-BR1 with a truncated C-terminus. Brain Res 89:103–110.

    CAS  Google Scholar 

  • Wischmeyer E, Döring F, Wischmeyer E, Spauschus A, Thomzig A, Veh R, Karschin A (1997) Subunit interactions in the assembly of neuronal Kir3.0 inwardly rectifying K+ channels. Mol Cell Neurosci 9:194–206.

    CAS  PubMed  Google Scholar 

  • Woodin MA, Ganguly K, Poo MM (2003) Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl− transporter activity. Neuron 39:807–820.

    CAS  PubMed  Google Scholar 

  • Wu LG, Saggau P (1995) GABAB receptor-mediated presynaptic inhibition in guinea-pig hippocampus is caused by reduction of presynaptic Ca2+ influx. J Physiol Lond 485:649–657.

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. School of Medicine, Institute of Medical Sciences (IMS), University of Aberdeen, Foresterhill, Aberdeen, AB25 2ZD, Scotland, UK

    Marlene Bartos

  2. Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen, AB25 2ZD, UK

    Jonas-Frederic Sauer

  3. Neuroscience and Molecular Pharmacology, Faculty of Biomedical and Life Sciences, University of Glasgow, Glasgow, G12 8QQ, UK

    Imre Vida

  4. Department of Anatomy and Cell Biology, University of Freiburg, Albertstraße 17, Freiburg, Germany

    Ákos Kulik

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  1. Marlene Bartos
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  2. Jonas-Frederic Sauer
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  3. Imre Vida
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  4. Ákos Kulik
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Correspondence to Marlene Bartos .

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  1. Department of Computing Science and Mathematics, University of Stirling, Stirling, FK9 4LA, UK

    Vassilis Cutsuridis  & Bruce Graham  & 

  2. Neuroscience & Molecular Pharmacology, Faculty of Biomedical and Life Sciences, University of Glasgow, Glasgow, G12 8QQ, UK

    Stuart Cobb  & Imre Vida  & 

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Bartos, M., Sauer, JF., Vida, I., Kulik, Á. (2010). Fast and Slow GABAergic Transmission in Hippocampal Circuits. In: Cutsuridis, V., Graham, B., Cobb, S., Vida, I. (eds) Hippocampal Microcircuits. Springer Series in Computational Neuroscience, vol 5. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0996-1_5

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