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In the Developing Hippocampus Kainate Receptors Control the Release of GABA from Mossy Fiber Terminals via a Metabotropic Type of Action

  • Enrico CherubiniEmail author
  • Maddalena D. Caiati
  • Sudhir Sivakumaran
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 717)

Abstract

Kainate receptors (KARs) are glutamate-gated ion channels assembled from various combinations of GluK1-GluK5 subunits with different physiological and pharmacological properties. In the hippocampus, KARs expressed at postsynaptic sites mediate a small component of excitatory postsynaptic currents while at presynaptic sites they exert a powerful control on transmitter release at both excitatory and inhibitory connections. KARs are developmentally regulated and play a key role in several developmental processes including neuronal migration, differentiation and synapse formation. Interestingly, they can signal through a canonical ionotropic pathway but also through a noncanonical modality involving pertussis toxin-sensitive G proteins and downstream signaling molecules.

In this Chapter some of our recent data concerning the functional role of presynaptic KARs in regulation of transmitter release from immature mossy fiber terminals and in synaptic plasticity processes will be reviewed. Early in postnatal development, MFs release into their targeted neurons mainly GABA which is depolarizing and excitatory. Endogenous activation of GluK1 KARs localized on MF terminals by glutamate present in the extracellular space down regulates GABA release, leading sometimes to synapse silencing. The depressant effect of GluK1 on MF responses is mediated by a metabotropic process, sensitive to pertussis toxin and phospholipase C (PLC) along the transduction pathway downstream to G protein activation. Blocking PLC with the selective antagonist U73122, unmasks the potentiating effect of GluK1 on MF-evoked GABAergic currents, which probably depend on the ionotropic type of action of these receptors.

In addition, GluK1 KARs dynamically regulate the direction of spike-time dependent plasticity, a particular form of Hebbian type of learning which consists in bidirectional modifications in synaptic strength according to the temporal order of pre and postsynaptic spiking. At immature MF-CA3 synapses pairing MF stimulation with postsynaptic spiking and vice versa induces long term depression of MF-evoked GABAergic currents. In the case of positive pairing synaptic depression can be switched into spike-time dependent potentiation by blocking GluK1 KARs with UBP 302. The depressant action exerted by GluK1 KARs on MF responses would prevent the excessive activation of the CA3 associative network by the excitatory action of GABA early in postnatal development.

Keywords

Gaba Release Kainate Receptor Postsynaptic Spike Silent Synapse Mossy Fiber Terminal 
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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References

  1. 1.
    Nisticó R, Dargan S, Fitzjohn SM et al. GLUK1 receptor antagonists and hippocampal mossy fiber function. Int Rev Neurobiol 2009; 85:13–27.PubMedCrossRefGoogle Scholar
  2. 2.
    Huettner JE. Kainate receptors and synaptic transmission. Prog Neurobiol 2003; 70:387–407.PubMedCrossRefGoogle Scholar
  3. 3.
    Collingridge GL, Olsen RW, Peters J et al. A nomenclature for ligand-gated ion channels. Neuropharm 2009; 56:2–5.CrossRefGoogle Scholar
  4. 4.
    Egebjerg J, Bettler B, Hermans-Borgmeyer I et al. Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not by AMPA. Nature 1991; 351:745–748.PubMedCrossRefGoogle Scholar
  5. 5.
    Schiffer HH, Swanson GT, Heinemann SE Rat GluR7 and a carboxy-terminal splice variant, GluR7b, are functional kainate receptor subunits with a low sensitivity to glutamate. Neuron 1997; 19:1141–1146.PubMedCrossRefGoogle Scholar
  6. 6.
    Sommer B, Burnashev N, Verdoorn TA et al. A glutamate receptor channel with high affinity for domoate and kainate. EMBO J 1992; 11:1651–1656.PubMedGoogle Scholar
  7. 7.
    Herb A, Burnashev N, Werner P et al. The KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels with distantly related subunits. Neuron 1992; 8:775–785.PubMedCrossRefGoogle Scholar
  8. 8.
    Werner P, Voigt M, Keinänen K et al. Cloning of a putative high-affinity kainate receptor expressed predominantly in hippocampal CA3 cells. Nature 1991; 351:742–744.PubMedCrossRefGoogle Scholar
  9. 9.
    Lerma J. Roles and rules of kainate receptors in synaptic transmission. Nat Rev Neurosci 2003; 4:481–495.PubMedCrossRefGoogle Scholar
  10. 10.
    Castillo PE, Malenka RC, Nicoll RA. Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 1997; 388:182–186.PubMedCrossRefGoogle Scholar
  11. 11.
    Vignes M, Collingridge GL. The synaptic activation of kainate receptors. Nature 1997; 388:179–182.PubMedCrossRefGoogle Scholar
  12. 12.
    Mulle C, Sailer A, Pérez-Otaño I et al. Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 1998; 392:601–615.PubMedCrossRefGoogle Scholar
  13. 13.
    Fernandes HB, Catches JS, Petralia RS et al. High-affinity kainate receptor subunits are necessary for ionotropic but not metabotropic signaling. Neuron 2009; 63:818–829.PubMedCrossRefGoogle Scholar
  14. 14.
    Mulle C, Sailer A, Swanson GT et al. Subunit composition of kainate receptors in hippocampal interneurons. Neuron 2000; 28:475–484.PubMedCrossRefGoogle Scholar
  15. 15.
    Contractor A, Swanson G, Heinemann SF. Kainate receptors are involved in short-and long-term plasticity at mossy fiber synapses in the hippocampus. Neuron 2001; 29:209–216.PubMedCrossRefGoogle Scholar
  16. 16.
    Lauri SE, Bortolotto ZA, Bleakman D et al. A critical role of a facilitatory presynaptic kainate receptor in mossy fiber LTP. Neuron 2001; 32:697–709.PubMedCrossRefGoogle Scholar
  17. 17.
    Pinheiro PS, Perrais D, Coussen F et al. GluR7 is an essential subunit of presynaptic kainate autoreceptors at hippocampal mossy fiber synapses. Proc Natl Acad Sei USA 2007; 104:12181–12186.CrossRefGoogle Scholar
  18. 18.
    Kwon HB, Castillo PE. Role of glutamate autoreceptors at hippocampal mossy fiber synapses. Neuron 2008; 60:1082–1094.PubMedCrossRefGoogle Scholar
  19. 19.
    Lerma J. Kainate receptor physiology. Curr Opin Pharmacol 2006; 6:89–97.PubMedCrossRefGoogle Scholar
  20. 20.
    Kamiya H, Ozawa S, Manabe T. Kainate receptor-dependent short-term plasticity of presynaptic Ca2+ influx at the hippocampal mossy fiber synapses. J Neurosci 2002; 22:9237–9243.PubMedGoogle Scholar
  21. 21.
    Nicoll RA, Schmitz D. Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci 2005; 6:863–876.PubMedCrossRefGoogle Scholar
  22. 22.
    Scott R, Lalic T, Kullmann DM et al. Target-cell specificity of kainate autoreceptor and Ca2+-store-dependent short-term plasticity at hippocampal mossy fiber synapses. J Neurosci 2008; 28:13139–13149.PubMedCrossRefGoogle Scholar
  23. 23.
    Clarke VR, Ballyk BA, Hoo KH et al. A hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission. Nature 1997; 389:599–603.PubMedCrossRefGoogle Scholar
  24. 24.
    Rodríguez-Moreno A, Herreras O, Lerma J. Kainate receptors presynaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 1997; 19:893–901.PubMedCrossRefGoogle Scholar
  25. 25.
    Rodríguez-Moreno A, Lerma J. Kainate receptor modulation of GABA release involves a metabotropic function. Neuron 1998; 20:1211–1218.PubMedCrossRefGoogle Scholar
  26. 26.
    Cossart R, Tyzio R, Dinocourt C et al. Presynaptic kainate receptors that enhance the release of GABA on CA1 hippocampal interneurons. Neuron 2001; 29:497–508.PubMedCrossRefGoogle Scholar
  27. 27.
    Maingret F, Lauri SE, Taira T et al. Profound regulation of neonatal CA1 rat hippocampal GABAergic transmission by functionally distinct kainate receptor populations. J Physiol 2005; 567(Pt 1): 131–142.PubMedCrossRefGoogle Scholar
  28. 28.
    Cunha RA, Constantino MD, Ribeiro JA. Inhibition of [3H] gamma-aminobutyric acid release by kainate receptor activation in rat hippocampal synaptosomes. Eur J Pharmacol 1997; 323:167–172.PubMedCrossRefGoogle Scholar
  29. 29.
    Cunha RA, Malva JO, Ribeiro JA. Pertussis toxin prevents presynaptic inhibition by kainate receptors of rat hippocampal [(3)H]GABA release. FEBS Lett 2000; 469:159–162.PubMedCrossRefGoogle Scholar
  30. 30.
    Frerking M, Schmitz D, Zhou Q et al. Kainate receptors depress excitatory synaptic transmission at CA3→CA1 synapses in the hippocampus via a direct presynaptic action. J Neurosci 2001; 21:2958–2966.PubMedGoogle Scholar
  31. 31.
    Kamiya H, Ozawa S. Kainate receptor-mediated presynaptic inhibition at the mouse hippocampal mossy fibre synapse. J Physiol 2000; 523(Pt 3):653–665.PubMedCrossRefGoogle Scholar
  32. 32.
    Schmitz D, Mellor J, Frerking M et al. Presynaptic kainate receptors at hippocampal mossy fiber synapses. Proc Natl Acad Sci USA 2001; 98:11003–11008.PubMedCrossRefGoogle Scholar
  33. 33.
    Negrete-Diaz JV, Sihra TS, Delgado-García JM et al. Kainate receptor-mediated inhibition of glutamate release involves protein kinase A in the mouse hippocampus. J Neurophysiol 2006; 96:1829–1837.PubMedCrossRefGoogle Scholar
  34. 34.
    Bortolotto ZA, Nistico R, More JC. Kainate receptors and mossy fiber LTP. Neurotoxicology 2005; 26:769–777.PubMedCrossRefGoogle Scholar
  35. 35.
    Negrete-Díaz JV, Sihra TS, Delgado-García JM. Kainate receptor-mediated presynaptic inhibition converges with presynaptic inhibition mediated by Group II mGluRs and long-term depression at the hippocampal mossy fiber-CA3 synapse. J Neural Transm 2007; 114:1425–1431.PubMedCrossRefGoogle Scholar
  36. 36.
    Gho M, King AE, Ben-Ari Y et al. Kainate reduces two voltage-dependent potassium conductances in rat hippocampal neurons in vitro. Brain Res 1986; 385:411–414.PubMedCrossRefGoogle Scholar
  37. 37.
    Melyan Z, Wheal HV, Lancaster B. Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 2002; 34:107–114.PubMedCrossRefGoogle Scholar
  38. 38.
    Fisahn A, Heinemann SF, McBain CJ. The kainate receptor subunit GluR6 mediates metabotropic regulation of the slow and medium AHP currents in mouse hippocampal neurones. J Physiol 2005; 562(Pt l):199–203.PubMedCrossRefGoogle Scholar
  39. 39.
    Ruiz A, Sachidhanandam S, Utvik JK et al. Distinct subunits in heteromeric kainate receptors mediate ionotropic and metabotropic function at hippocampal mossy fiber synapses. J Neurosci 2005; 25:11710–11718.PubMedCrossRefGoogle Scholar
  40. 40.
    Vincent P, Mulle C. Kainate receptors in epilepsy and excitotoxicity. Neuroscience 2009; 158:309–323.PubMedCrossRefGoogle Scholar
  41. 41.
    Rivera R, Rozas JL, Lerma J. PKC-dependent autoregulation of membrane kainate receptors. EMBO J 2007; 26:4359–4367PubMedCrossRefGoogle Scholar
  42. 42.
    Miller LP, Johnson AE, Gelhard RE et al. The ontogeny of excitatory amino acid receptors in the rat forebrain—II. Kainic acid receptors. Neuroscience 1990; 35:45–51.PubMedCrossRefGoogle Scholar
  43. 43.
    Ultsch A, Schuster CM, Laube B et al. Glutamate receptors of Drosophila melanogaster: cloning of a kainate-selective subunit expressed in the central nervous system. Proc Natl Acad Sei USA 1992; 89:10484–10488.CrossRefGoogle Scholar
  44. 44.
    Bettler B, Boulter J, Hermans-Borgmeyer I et al. Cloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development. Neuron 1990;5:583–595.PubMedCrossRefGoogle Scholar
  45. 45.
    Bahn S, Volk B, Wisden W. Kainate receptor gene expression in the developing rat brain. J Neurosci 1994; 14:5525–5547.PubMedGoogle Scholar
  46. 46.
    Ritter LM, Vazquez DM, Meador-Woodruff JH. Ontogeny of ionotropic glutamate receptor subunit expression in the rat hippocampus. Brain Res Dev Brain Res 2002; 139:227–236PubMedCrossRefGoogle Scholar
  47. 47.
    Schlaggar BL, Fox K, O’Leary DD. Postsynaptic control of plasticity in developing somatosensory cortex. Nature 1993; 364:623–626.PubMedCrossRefGoogle Scholar
  48. 48.
    Represa A, Tremblay E, Ben-Ari Y. Kainate binding sites in the hippocampal mossy fibers: localization and plasticity. Neuroscience 1987; 20:739–748.PubMedCrossRefGoogle Scholar
  49. 49.
    Acsády L, Kamondi A, Sík A et al. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci 1998; 18:3386–3403.PubMedGoogle Scholar
  50. 50.
    Tashiro A, Dunaevsky A, Blazeski R et al. Bidirectional regulation of hippocampal mossy fiber filopodial motility by kainate receptors: a two-step model of synaptogenesis. Neuron 2003; 38:773–784.PubMedCrossRefGoogle Scholar
  51. 51.
    Feller MB, Butts DA, Aaron HL et al. Dynamic processes shape spatiotemporal properties of retinal waves. Neuron 1997; 19:293–306.PubMedCrossRefGoogle Scholar
  52. 52.
    Yuste R, Katz LC. Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 1991; 6:333–344.PubMedCrossRefGoogle Scholar
  53. 53.
    Owens DF, Boyce LH, Davis MB et al. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci 1996; 16:6414–6423.PubMedGoogle Scholar
  54. 54.
    Dammerman RS, Flint AC, Noctor S et al. An excitatory GABAergic plexus in developing neocortical layer 1. J Neurophysiol 2000; 84:428–434.PubMedGoogle Scholar
  55. 55.
    Marie D, Liu QY, Marie I et al. GABA expression dominates neuronal lineage progression in the embryonic rat neocortex and facilitates neurite outgrowth via GABA(A) autoreceptor/Clchannels. J Neurosci 2001; 21:2343–2360.Google Scholar
  56. 56.
    Chen G, Trombley PQ, van den Pol AN. Excitatory actions of GABA in developing rat hypothalamic neurones. J Physiol 1996; 494(Pt 2):451–464.PubMedGoogle Scholar
  57. 57.
    Eilers J, Plant TD, Marandi N et al. GABA-mediated Ca2+ signalling in developing rat cerebellar Purkinje neurones. J Physiol 2001; 536(Pt 2):429–437.PubMedCrossRefGoogle Scholar
  58. 58.
    Wang J, Reichling DB, Kyrozis A et al. Developmental loss of GABA-and glycine-induced depolarization and Ca2+ transients in embryonic rat dorsal horn neurons in culture. Eur J Neurosci 1994; 6:1275–1280.PubMedCrossRefGoogle Scholar
  59. 59.
    O’Donovan MJ. The origin of spontaneous activity in developing networks of the vertebrate nervous system. Curr Opin Neurobiol 1999; 9:94–104.PubMedCrossRefGoogle Scholar
  60. 60.
    Cherubini E, Gaiarsa JL, Ben-Ari Y. GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 1991; 14:515–519.PubMedCrossRefGoogle Scholar
  61. 61.
    Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 2002; 3:728–739.PubMedCrossRefGoogle Scholar
  62. 62.
    Leinekugel X, Khazipov R, Cannon R et al. Correlated bursts of activity in the neonatal hippocampus in vivo. Science 2002; 296:2049–2052.PubMedCrossRefGoogle Scholar
  63. 63.
    Buzsáki G, Draguhn A. Neuronal oscillations in cortical networks. Science 2004; 304:1926–1929.PubMedCrossRefGoogle Scholar
  64. 64.
    Vesikansa A, Sallert M, Taira T et al. Activation of kainate receptors controls the number of functional glutamatergic synapses in the area CA1 of rat hippocampus. J Physiol 2007; 583(Pt 1): 145–157.PubMedCrossRefGoogle Scholar
  65. 65.
    Lauri SE, Segerstråle M, Vesikansa A et al. Endogenous activation of kainate receptors regulates glutamate release and network activity in the developing hippocampus. J Neurosci 2005; 25:4473–4484.PubMedCrossRefGoogle Scholar
  66. 66.
    Lauri SE, Vesikansa A, Segerstråle M et al. Functional maturation of CA1 synapses involves activity-dependent loss of tonic kainate receptor mediated inhibition of glutamate release. Neuron 2006; 50:415–429.PubMedCrossRefGoogle Scholar
  67. 67.
    McBain CJ, Fisahn A. Interneurons unbound. Nat Rev Neurosci 2001; 2:11–23.PubMedCrossRefGoogle Scholar
  68. 68.
    Ben-Ari Y, Khalilov I, Represa A et al. Interneurons set the tune of developing networks. Trends Neurosci 2004; 27:422–427.PubMedCrossRefGoogle Scholar
  69. 69.
    Maccaferri G, McBain CJ. Long-term potentiation in distinct subtypes of hippocampal nonpyramidal neurons. J Neurosci 1996; 16:5334–5343.PubMedGoogle Scholar
  70. 70.
    Hestrin S, Galarreta M. Electrical synapses define networks of neocortical GABAergic neurons. Trends Neurosci 2005; 28:304–309.PubMedCrossRefGoogle Scholar
  71. 71.
    Zsiros V, Maccaferri G. Electrical coupling between interneurons with different excitable properties in the stratum lacunosum-moleculare of the juvenile CAl rat hippocampus. J Neurosci 2005; 25:8686–8695.PubMedCrossRefGoogle Scholar
  72. 72.
    Minneci F, Janahmadi M, Migliore M et al. Signaling properties of stratum oriens interneurons in the hippocampus of transgenic mice expressing EGFP in a subset of somatostatin-containing cells. Hippocampus 2007; 17:538–553.PubMedCrossRefGoogle Scholar
  73. 73.
    Segerstråle M, Juuri J, Lanore F et al. High firing rate of neonatal hippocampal interneurons is caused by attenuation of afterhyperpolarizing potassium currents by tonically active kainate receptors. J Neurosci 2010; 30:6507–6514.PubMedCrossRefGoogle Scholar
  74. 74.
    Caiati MD, Sivakumaran S, Cherubini E. In the developing rat hippocampus, endogenous activation of presynaptic kainate receptors reduces GABA release from mossy fiber terminals. J Neurosci 2010; 30:1750–1759.PubMedCrossRefGoogle Scholar
  75. 75.
    Marchai C, Mulle C. Postnatal maturation of mossy fibre excitatory transmission in mouse CA3 pyramidal cells: a potential role for kainate receptors. J Physiol 2004; 561(Pt l):27–37.CrossRefGoogle Scholar
  76. 76.
    Cossart R, Epsztein J, Tyzio R et al. Quantal release of glutamate generates pure kainate and mixed AMPA/kainate EPSCs in hippocampal neurons. Neuron 2002; 35:147–159.PubMedCrossRefGoogle Scholar
  77. 77.
    Coussen F, Normand E, Marchai C et al. Recruitment of the kainate receptor subunit glutamate receptor 6 by cadherin/catenin complexes. J Neurosci 2002; 22:6426–6436.PubMedGoogle Scholar
  78. 78.
    Mizoguchi A, Nakanishi H, Kimura K et al. Nectin: an adhesion molecule involved in formation of synapses. J Cell Biol 2002; 156:555–565.PubMedCrossRefGoogle Scholar
  79. 79.
    Gutiérrez R, Heinemann U. Kindling induces transient fast inhibition in the dentate gyrus-CA3 projection. Eur J Neurosci 2001; 13:1371–1379.PubMedCrossRefGoogle Scholar
  80. 80.
    Jaffe DB, Gutiérrez R. Mossy fiber synaptic transmission: communication from the dentate gyrus to area CA3. Prog Brain Res 2007; 163:109–132PubMedCrossRefGoogle Scholar
  81. 81.
    Schwarzer C, Sperk G. Hippocampal granule cells express glutamic acid decarboxylase-67 after limbic seizures in the rat. Neuroscience 1995; 69:705–709.PubMedCrossRefGoogle Scholar
  82. 82.
    Sloviter RS, Dichter MA, Rachinsky TL et al. Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus. J Comp Neurol 1996; 373:593–618.PubMedCrossRefGoogle Scholar
  83. 83.
    Lamas M, Gómez-Lira G, Gutiérrez R. Vesicular GABA transporter mRNA expression in the dentate gyrus and in mossy fiber synaptosomes. Brain Res Mol Brain Res 2001; 93:209–214.PubMedCrossRefGoogle Scholar
  84. 84.
    Rao A, Cha EM, Craig AM. Mismatched appositions of presynaptic and postsynaptic components in isolated hippocampal neurons. J Neurosci 2000; 20:8344–8353.PubMedGoogle Scholar
  85. 85.
    Walker MC, Ruiz A, Kullmann DM. Monosynaptic GABAergic signaling from dentate to CA3 with a pharmacological and physiological profile typical of mossy fiber synapses. Neuron 2001; 29:703–715.PubMedCrossRefGoogle Scholar
  86. 86.
    Gutierrez R, Romo-Parra H, Maqueda J et al. Plasticity of the GABAergic phenotype of the “glutamatergic” granule cells of the rat dentate gyrus. J Neurosci 2003; 23:5594–5598.PubMedGoogle Scholar
  87. 87.
    Bergersen L, Ruiz A, Bjaalie JG et al. GABA and GABAA receptors at hippocampal mossy fibre synapses. Eur J Neurosci 2003; 18:931–941.PubMedCrossRefGoogle Scholar
  88. 88.
    Gómez-Lira G, Lamas M, Romo-Parra H et al. Programmed and induced phenotype of the hippocampal granule cells. J Neurosci 2005; 25:6939–6946.PubMedCrossRefGoogle Scholar
  89. 89.
    Zander JF, Münster-Wandowski A, Brunk I et al. Synaptic and vesicular coexistence of VGLUT and VGAT in selected excitatory and inhibitory synapses. J Neurosci 2010; 30:7634–7645.PubMedCrossRefGoogle Scholar
  90. 90.
    Safiulina VF, Fattorini G, Conti F et al. GABAergic signaling at mossy fiber synapses in neonatal rat hippocampus. J Neurosci 2006; 26:597–608.PubMedCrossRefGoogle Scholar
  91. 91.
    Sivakumaran S, Mohajerani MH, Cherubini E. At immature mossy-fiber-CA3 synapses, correlated presynaptic and postsynaptic activity persistently enhances GABA release and network excitability via BDNF and cAMP-dependent PKA. J Neurosci 2009; 29:2637–2647.PubMedCrossRefGoogle Scholar
  92. 92.
    Dzhala VI, Talos DM, Sdrulla DA et al. NKCC1 transporter facilitates seizures in the developing brain. Nat Med 2005; 11:1205–1213.PubMedCrossRefGoogle Scholar
  93. 93.
    Sipilä ST, Schuchmann S, Voipio J et al. The cation-chloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus. J Physiol 2006; 573(Pt 3):765–773.PubMedCrossRefGoogle Scholar
  94. 94.
    Ben-Ari Y, Gaiarsa JL, Tyzio R et al. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 2007; 87:1215–1284.PubMedCrossRefGoogle Scholar
  95. 95.
    Voronin LL, Cherubini E. ‘Deaf, mute and whispering’ silent synapses: their role in synaptic plasticity J Physiol 2004; 557(Pt 1):3–12.PubMedCrossRefGoogle Scholar
  96. 96.
    Durand GM, Kovalchuk Y, Konnerth A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 1996; 381:71–75.PubMedCrossRefGoogle Scholar
  97. 97.
    Danbolt NC. Glutamate uptake. Prog Neurobiol 2001; 65:1–105.PubMedCrossRefGoogle Scholar
  98. 98.
    Rozas JL, Paternain AV, Lerma J. Noncanonical signaling by ionotropic kainate receptors. Neuron 2003; 39:543–553.PubMedCrossRefGoogle Scholar
  99. 99.
    Rodríguez-Moreno A, Sihra TS. Metabotropic actions of kainate receptors in the CNS. J Neurochem 2007; 10:2121–2135.CrossRefGoogle Scholar
  100. 100.
    Fletcher EJ, Lodge D. New developments in the molecular pharmacology of alphaamino-3-hy-droxy-5-methyl-4-isoxazole propionate and kainate receptors. Pharmacol Ther 1996; 70:65–89.PubMedCrossRefGoogle Scholar
  101. 101.
    Semyanov A, Kullmann DM. Kainate receptor-dependent axonal depolarization and action potential initiation in interneurons. Nat Neurosci 2001; 4:718–723.PubMedCrossRefGoogle Scholar
  102. 102.
    Amaral DG, Dent JA. Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 1981; 195:51–86.PubMedCrossRefGoogle Scholar
  103. 103.
    Dan Y, Poo MM. Spike timing-dependent plasticity: from synapse to perception. Physiol Rev 2006; 86:1033–1048.PubMedCrossRefGoogle Scholar
  104. 104.
    Caporale N, Dan Y. Spike timing dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci 2008; 31:25–46.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Enrico Cherubini
    • 1
    Email author
  • Maddalena D. Caiati
  • Sudhir Sivakumaran
  1. 1.Neurobiology Sector and IIT UnitInternationa School of Advanced Studies (SISSA)Basovizza, TriesteItaly

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