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Fast and Slow GABAergic Transmission in Hippocampal Circuits

  • Marlene Bartos
  • Jonas-Frederic Sauer
  • Imre Vida
  • Ákos Kulik
Part of the Springer Series in Computational Neuroscience book series (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.

Keywords

Pyramidal Cell Principal Cell Decay Time Constant Kir3 Channel Paired Recording 
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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Further Reading

  1. Alger BE, Nicoll RA (1979) GABA-mediated biphasic inhibitory responses in hippocampus. Nature 281:315–317.PubMedGoogle Scholar
  2. 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.PubMedGoogle Scholar
  3. 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.PubMedGoogle Scholar
  4. Avoli M, Biagini G, de Curtis M (2006) Do interictal spikes sustain seizures and epileptogenesis? Epilepsy Curr 6:203–207.PubMedGoogle Scholar
  5. Banke TG, McBain CJ (2006) GABAergic input onto CA3 hippocampal interneurons remains shunting throughout development. J Neurosci 26:11720–11725.PubMedGoogle Scholar
  6. Banks MI, Li TB, Pearce RA (1998) The synaptic basis of GABAA, slow. J Neurosci 18:1305–1317.PubMedGoogle Scholar
  7. 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.PubMedGoogle Scholar
  8. 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.PubMedGoogle Scholar
  9. Bartos M, Vida I, Jonas P (2007) Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8:45–56.PubMedGoogle Scholar
  10. Bettler B, Kaupmann K, Mosbacher J, Gassmann M (2004) Molecular structure and physiological functions of GABA(B) receptors. Physiol Rev 84:835–867.PubMedGoogle Scholar
  11. 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.PubMedGoogle Scholar
  12. 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.PubMedGoogle Scholar
  13. 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.PubMedGoogle Scholar
  14. Bowery NG, Brown DA (1997) The cloning of GABA(B) receptors. Nature 386:223–224.PubMedGoogle Scholar
  15. 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.PubMedGoogle Scholar
  16. 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.PubMedGoogle Scholar
  17. 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.PubMedGoogle Scholar
  18. Buzsáki G (1996) The hippocampo-neocortical dialogue. Cereb Cortex 6:81–92.PubMedGoogle Scholar
  19. Calver AR, Davies CH, Pangalos M (2002) GABA(B) receptors: From monogamy to promiscuity. Neurosignals 11:299–314.PubMedGoogle Scholar
  20. Chavas J, Marty A (2003) Coexistence of excitatory and inhibitory GABA synapses in the cerebellar interneuron network. J Neurosci 23:2019–2031.PubMedGoogle Scholar
  21. 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.PubMedGoogle Scholar
  22. 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.PubMedGoogle Scholar
  23. 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.PubMedGoogle Scholar
  24. Dascal N (1997) Signalling via the G protein-activated K+ channels. Cell Signal 9:551–573.PubMedGoogle Scholar
  25. Davies CH, Collingridge GL. (1993) The physiological regulation of synaptic inhibition by GABAB autoreceptors in rat hippocampus. J Physiol 1993 Dec;472:245–65.Google Scholar
  26. 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.PubMedGoogle Scholar
  27. Davies CH, Starkey SJ, Pozza MF, Collingridge GL (1991) GABA autoreceptors regulate the induction of LTP. Nature 349:609–611.PubMedGoogle Scholar
  28. 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.PubMedGoogle Scholar
  29. 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.PubMedGoogle Scholar
  30. Dutar P, Nicoll RA (1988) Pre- and postsynaptic GABAB receptors in the hippocampus have different pharmacological properties. Neuron 1:585–591.PubMedGoogle Scholar
  31. 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.PubMedGoogle Scholar
  32. 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.PubMedGoogle Scholar
  33. Freund TF (2003) Interneuron diversity series: Rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489–495.PubMedGoogle Scholar
  34. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347–470.PubMedGoogle Scholar
  35. 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.PubMedGoogle Scholar
  36. 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.PubMedGoogle Scholar
  37. 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.PubMedGoogle Scholar
  38. 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.PubMedGoogle Scholar
  39. 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.PubMedGoogle Scholar
  40. Glickfeld LL, Scanziani M (2006) Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells. Nat Neurosci 9:807–815.PubMedGoogle Scholar
  41. Glickfeld LL, Atallah BV, Scanziani M (2008) Complementary modulation of somatic inhibition by opioids and cannabinoids. J Neurosci 28:1824–1832.PubMedGoogle Scholar
  42. Glickfeld LL, Roberts JD, Somogyi P, Scanziani M (2009) Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis. Nat Neurosci 12:21–23.PubMedGoogle Scholar
  43. 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
  44. 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.PubMedGoogle Scholar
  45. Gulledge AT, Stuart GJ (2003) Excitatory actions of GABA in the cortex. Neuron 37:299–309.PubMedGoogle Scholar
  46. 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.PubMedGoogle Scholar
  47. 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.PubMedGoogle Scholar
  48. 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
  49. Harney SC, Jones MV (2002) Pre- and postsynaptic properties of somatic and dendritic inhibition in dentate gyrus. Neuropharmacology 43:584–594.PubMedGoogle Scholar
  50. Harrison NL (1990) On the presynaptic action of baclofen at inhibitory synapses between cultured rat hippocampal neurones. J Physiol Lond 422:433–446.PubMedGoogle Scholar
  51. Hefft S, Jonas P (2005) Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8:1319–1328.PubMedGoogle Scholar
  52. 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.PubMedGoogle Scholar
  53. 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.PubMedGoogle Scholar
  54. 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.PubMedGoogle Scholar
  55. Isaacson JS, Solís JM, Nicoll RA (1993) Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 10:165–175.PubMedGoogle Scholar
  56. 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.PubMedGoogle Scholar
  57. Johnston D, Brown TH (1983) Interpretation of voltage-clamp measurements in hippocampal neurons. J Neurophysiol 50:464–486.PubMedGoogle Scholar
  58. 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.PubMedGoogle Scholar
  59. Katona I, Acsády L, Freund TF (1999) Postsynaptic targets of somatostatin-immunoreactive interneurons in the rat hippocampus. Neuroscience 88:37–55.PubMedGoogle Scholar
  60. 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.PubMedGoogle Scholar
  61. 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.PubMedGoogle Scholar
  62. 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.PubMedGoogle Scholar
  63. Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: The unity of hippocampal circuit operations. Science.321:53–57.PubMedGoogle Scholar
  64. 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.PubMedGoogle Scholar
  65. 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.PubMedGoogle Scholar
  66. 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.PubMedGoogle Scholar
  67. 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.PubMedGoogle Scholar
  68. Kraushaar U, Jonas P (2000) Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse. J Neurosci 20:5594–5607.PubMedGoogle Scholar
  69. 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.PubMedGoogle Scholar
  70. 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.PubMedGoogle Scholar
  71. 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.PubMedGoogle Scholar
  72. 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.PubMedGoogle Scholar
  73. Kyrozis A, Reichling DB (1995) Perforated-patch recording with gramicidin avoids artifactual changes in intracellular chloride concentration. J Neurosci Methods 57:27–35.PubMedGoogle Scholar
  74. 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.PubMedGoogle Scholar
  75. 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.PubMedGoogle Scholar
  76. 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.PubMedGoogle Scholar
  77. 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.PubMedGoogle Scholar
  78. 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.PubMedGoogle Scholar
  79. 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.PubMedGoogle Scholar
  80. Ling DS, Benardo LS (1994) Properties of isolated GABAB-mediated inhibitory postsynaptic currents in hippocampal pyramidal cells. Neuroscience 63:937–944.PubMedGoogle Scholar
  81. 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.PubMedGoogle Scholar
  82. 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.PubMedGoogle Scholar
  83. 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.PubMedGoogle Scholar
  84. 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.PubMedGoogle Scholar
  85. Major G, Evans JD, Jack JJB (1993) Solutions for transients in arbitrarily branching cables: II. Voltage clamp theory. Biophys J 65:450–468.Google Scholar
  86. Malinow R, Tsien RW (1990) Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346:177–180.PubMedGoogle Scholar
  87. 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.PubMedGoogle Scholar
  88. 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.PubMedGoogle Scholar
  89. Marshall FH, White J, Main M, Green A, Wise A (1999) GABA(B) receptors function as heterodimers. Biochem Soc Trans 27:530–535.PubMedGoogle Scholar
  90. 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.PubMedGoogle Scholar
  91. 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.PubMedGoogle Scholar
  92. McBain CJ, Fisahn A (2001) Interneurons unbound. Nat Rev Neurosci 2:11–23.PubMedGoogle Scholar
  93. 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.PubMedGoogle Scholar
  94. Miles R, Tóth K, Gulyás AI, Hájos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815–823.PubMedGoogle Scholar
  95. Mitchell SJ, Silver RA (2003) Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38:433–445.PubMedGoogle Scholar
  96. Mittmann W, Koch U, Häusser M (2005) Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J Physiol Lond 563:369–378.PubMedGoogle Scholar
  97. Mott DD, Lewis DV (1991) Facilitation of the induction of long-term potentiation by GABAB receptors. Science 252:1718–1720.PubMedGoogle Scholar
  98. 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.PubMedGoogle Scholar
  99. 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.PubMedGoogle Scholar
  100. Newberry NR, Nicoll RA (1984) Direct hyperpolarizing action of baclofen on hippocampal pyramidal cells. Nature 308:450–452.PubMedGoogle Scholar
  101. 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.PubMedGoogle Scholar
  102. 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.PubMedGoogle Scholar
  103. Nusser Z, Mody I (2002) Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol 87:2624–2628.PubMedGoogle Scholar
  104. 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.PubMedGoogle Scholar
  105. 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.PubMedGoogle Scholar
  106. 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.PubMedGoogle Scholar
  107. Overstreet-Wadiche L, Bromberg DA, Bensen AL, Westbrook GL (2005) GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol 94:4528–4532.PubMedGoogle Scholar
  108. Pearce RA (1993) Physiological evidence for two distinct GABAA responses in rat hippocampus. Neuron 10:189–200.PubMedGoogle Scholar
  109. 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.PubMedGoogle Scholar
  110. Pouille F, Scanziani M (2001) Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293:1159–1163.PubMedGoogle Scholar
  111. 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.PubMedGoogle Scholar
  112. 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.PubMedGoogle Scholar
  113. 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
  114. 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.PubMedGoogle Scholar
  115. Sauer J-F, Bartos M (2010) Recruitment of early postnatal PV+ hippocampal interneurons by GABAergic excitation. J Neurosci, in press.Google Scholar
  116. Scanziani M (2000) GABA spillover activates postsynaptic GABAB receptors to control rhythmic hippocampal activity. Neuron 25:673–681.PubMedGoogle Scholar
  117. 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.PubMedGoogle Scholar
  118. 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.PubMedGoogle Scholar
  119. 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.PubMedGoogle Scholar
  120. 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.PubMedGoogle Scholar
  121. Sik A, Penttonen M, Ylinen A, Buzsáki G (1995) Hippocampal CA1 interneurons: An in vivo intracellular labeling study. J Neurosci 15:6651–6665.PubMedGoogle Scholar
  122. 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.PubMedGoogle Scholar
  123. 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.PubMedGoogle Scholar
  124. Sodickson DL, Bean BP (1996) GABAB receptor-activated inwardly rectifying potassium current in dissociated hippocampal CA3 neurons. J Neurosci 16:6374–6385.PubMedGoogle Scholar
  125. Sohal VS, Hasselmo ME (1998) GABA(B) modulation improves sequence disambiguation in computational models of hippocampal region CA3. Hippocampus 8:171–193.PubMedGoogle Scholar
  126. 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.PubMedGoogle Scholar
  127. 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.PubMedGoogle Scholar
  128. 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.PubMedGoogle Scholar
  129. 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.PubMedGoogle Scholar
  130. 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.PubMedGoogle Scholar
  131. 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.PubMedGoogle Scholar
  132. 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.PubMedGoogle Scholar
  133. Tamás G, Lorincz A, Simon A, Szabadics J (2003) Identified sources and targets of slow inhibition in the neocortex. Science 299:1902–1905.PubMedGoogle Scholar
  134. 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.PubMedGoogle Scholar
  135. 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.PubMedGoogle Scholar
  136. 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.PubMedGoogle Scholar
  137. 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
  138. 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.PubMedGoogle Scholar
  139. Vida I, Frotscher M (2000) A hippocampal interneuron associated with the mossy fiber system. Proc Natl Acad Sci USA 97:1275–1280.PubMedGoogle Scholar
  140. 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.PubMedGoogle Scholar
  141. 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.PubMedGoogle Scholar
  142. 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.PubMedGoogle Scholar
  143. 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.PubMedGoogle Scholar
  144. 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.PubMedGoogle Scholar
  145. 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.Google Scholar
  146. 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.PubMedGoogle Scholar
  147. 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.PubMedGoogle Scholar
  148. 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.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Marlene Bartos
    • 1
  • Jonas-Frederic Sauer
    • 2
  • Imre Vida
    • 3
  • Ákos Kulik
    • 4
  1. 1.School of Medicine, Institute of Medical Sciences (IMS)University of AberdeenAberdeenUK
  2. 2.Institute of Medical SciencesUniversity of AberdeenAberdeenUK
  3. 3.Neuroscience and Molecular Pharmacology, Faculty of Biomedical and Life SciencesUniversity of GlasgowGlasgowUK
  4. 4.Department of Anatomy and Cell BiologyUniversity of FreiburgFreiburgGermany

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