Contribution of metabotropic GABAB receptors to neuronal network construction

Pharmacology and Therapeutics

Volumn 132, Issue 2, 2011, Pages 170-179

  Gaiarsa, Jean Luc ^a,b   Kuczewski, Nicola ^a,b   Porcher, Christophe ^a,b  

^a Turing Center for Living Systems CENTURI Aix Marseille University   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Cell differentiation; Cell migration; Development; Neurotrophins; Plasticity; Synaptogenesis

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID B RECEPTOR; BACLOFEN; BICUCULLINE;

ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CENTRAL NERVOUS SYSTEM; ELECTROPHYSIOLOGY; GABAERGIC SYSTEM; GENE EXPRESSION REGULATION; HUMAN; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PERIPHERAL NERVE; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE; SYNAPTOGENESIS;

EID: 80052321425     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2011.06.004     Document Type: Review

References (142)

1. A. Balkowiec, and D.M. Katz Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons J Neurosci 22 2002 10399 10407 (Pubitemid 35416877)
2. B receptors negatively regulate transcription in cerebellar granular neurons through cyclic AMP responsive element binding protein-dependent mechanisms Neuroscience 70 1996 417 427
3. T.N. Behar, A.E. Schaffner, C.A. Colton, R. Somogyi, Z. Olah, C. Lehel, and J.L. Barker GABA-induced chemokinesis and NGF-induced chemotaxis of embryonic spinal cord neurons J Neurosci 14 1994 29 38 (Pubitemid 24022095)
4. B receptors J Neurosci Res 42 1995 97 108
5. T.B. Behar, Y.X. Li, H.T. Tran, W. Ma, V. Dunlap, C. Scott, and J.L. Barker GABA stimulates chemotaxis and chemokinesis of embryonic cortical neurons via calcium-dependent mechanisms J Neurosci 16 1996 1808 1818 (Pubitemid 26145957)
6. T.N. Behar, A.E. Schaffner, C.A. Scott, C. O'Connell, and J.L. Barker Differential response of cortical plate and ventricular zone cells to GABA as a migration stimulus J Neurosci 18 1998 6378 6387 (Pubitemid 28373243)
7. T.N. Behar, A.E. Schaffner, C.A. Scott, C.L. Greene, and J.L. Barker GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex Cereb Cortex 10 2000 899 909
8. T.N. Behar, S.V. Smith, R.T. Kennedy, J.M. McKenzie, I. Maric, and J.L. Barker GABA(B) receptors mediate motility signals for migrating embryonic cortical cells Cereb Cortex 11 2001 744 753 (Pubitemid 32718079)
9. Y. Ben Ari Developing networks play a similar melody Trends Neurosci 24 2001 353 360
10. Y. Ben Ari, J.L. Gaiarsa, R. Tyzio, and R. Khazipov GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations Physiol Rev 87 2007 1215 1284 (Pubitemid 350041471)
11. M.J. Berridge Inositol trisphosphate and calcium signalling Nature 361 1993 315 325 (Pubitemid 23041621)
12. M.S. Bianchi, V.A. Lux-Lantos, B. Bettler, and C. Libertun Expression of gamma-aminobutyric acid B receptor subunits in hypothalamus of male and female developing rats Brain Res Dev Brain Res 160 2005 124 129 (Pubitemid 41735119)
13. M. Bird, and A. Owen Neurite outgrowth-regulating properties of GABA and the effect of serum on mouse spinal cord neurons in culture J Anat 193 1998 503 508 (Pubitemid 29026950)
14. J.L. Blank, K.A. Brattain, and J.H. Exton Activation of cytosolic phosphoinositide phospholipase C by G-protein beta gamma subunits J Biol Chem 267 1992 23069 23075
15. L.N. Borodinsky, C.M. Root, J.A. Cronin, S.B. Sann, X. Gu, and N.C. Spitzer Activity-dependent homeostatic specification of transmitter expression in embryonic neurons Nature 429 2004 523 530 (Pubitemid 38737651)
16. B receptor pharmacology Annu Rev Pharmacol Toxicol 33 1993 109 147
17. B receptors cloned at last Trends Pharmacol Sci 18 1997 103 (Pubitemid 27168250)
18. N.G. Bowery, D.R. Hill, A.L. Hudson, A. Doble, D.N. Middlemiss, J. Shaw, and M. Turnbull (-)Baclofen decreases neurotransmitter release in the mammalian CNS by an action at a novel GABA receptor Nature 283 1980 92 94 (Pubitemid 10170892)
19. N.G. Bowery, B. Bettler, W. Froestl, J.P. Gallagher, F. Marshall, M. Raiteri, T.I. Bonner, and S.J. Enna International Union of Pharmacology. XXXIII. Mammalian gamma-aminobutyric acid(B) receptors: structure and function Pharmacol Rev 54 2002 247 264 (Pubitemid 34575715)
20. B receptor-mediated inhibition in the CA3 region of the rat hippocampus J Neurophysiol 79 1998 1341 1348 (Pubitemid 28125369)
21. L. Cancedda, H. Fiumelli, K. Chen, and M.M. Poo Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo J Neurosci 27 2007 5224 5235 (Pubitemid 46741781)
22. M. Canossa, A. Gartner, G. Campana, N. Inagaki, and H. Thoenen Regulated secretion of neurotrophins by metabotropic glutamate group I (mGluRI) and Trk receptor activation is mediated via phospholipase C signalling pathways EMBO J 20 2001 1640 1650 (Pubitemid 32299401)
23. B receptors regulate chick retinal calcium waves J Neurosci 21 2001 897 910 (Pubitemid 32163131)
24. E.H. Chang, V.C. Kotak, and D.H. Sanes Long-term depression of synaptic inhibition is expressed postsynaptically in the developing auditory system J Neurophysiol 90 2003 1479 1488 (Pubitemid 37129359)
25. B. Chattopadhyaya, G. Di Cristo, H. Higashiyama, G.W. Knott, S.J. Kuhlman, E. Welker, and Z.J. Huang Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period J Neurosci 24 2004 9598 9611 (Pubitemid 39441514)
26. B. Chattopadhyaya, G. Di Cristo, C.Z. Wu, G. Knott, S. Kuhlman, Y. Fu, R.D. Palmiter, and Z.J. Huang GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex Neuron 54 2007 889 903 (Pubitemid 46907499)
27. I. Chudotvorova, A. Ivanov, S. Rama, C.A. Hubner, C. Pellegrino, Y. Ben Ari, and I. Medina Early expression of KCC2 in rat hippocampal cultures augments expression of functional GABA synapses J Physiol 566 2005 671 679 (Pubitemid 41122653)
28. I. Colin-Le Brun, N. Ferrand, O. Caillard, P. Tosetti, Y. Ben Ari, and J.L. Gaïarsa Spontaneous synaptic activity is required for the formation of functional GABAergic synapses in the developing rat hippocampus J Physiol 559 2004 129 139 (Pubitemid 39206959)
29. B receptors: a new paradigm in G protein signaling Mol Cell Neurosci 16 2000 296 312
30. A.M. Davis, T.R. Henion, and S.A. Tobet Gamma-aminobutyric acidB receptors and the development of the ventromedial nucleus of the hypothalamus J Comp Neurol 449 2002 270 280 (Pubitemid 34734284)
31. B receptors in the central nervous system Nature 332 1988 156 158 (Pubitemid 18083559)
32. + channels overexpressed by adenovirus gene transfer inhibits the excitability of hippocampal neurons Proc Natl Acad Sci U S A 94 1997 7070 7075 (Pubitemid 27281992)
33. S.J. Enna, S.A. Reisman, and J.A. Stanford CGP 56999A, a GABA(B) receptor antagonist, enhances expression of brain-derived neurotrophic factor and attenuates dopamine depletion in the rat corpus striatum following a 6-hydroxydopamine lesion of the nigrostriatal pathway Neurosci Lett 406 2006 102 106 (Pubitemid 44278381)
34. S.C. Ferguson, and S. McFarlane GABA and development of the Xenopus optic projection J Neurobiol 51 2002 272 284 (Pubitemid 34538770)
35. H. Fiorentino, N. Kuczewski, D. Diabira, N. Ferrand, M.N. Pangalos, C. Porcher, and J.L. Gaiarsa GABA(B) receptor activation triggers BDNF release and promotes the maturation of GABAergic synapses J Neurosci 29 2009 11650 11661
36. B-receptor splice variants GB1a and GB1b in rat brain: developmental regulation, cellular distribution and extrasynaptic localization Eur J Neurosci 11 1999 761 768 (Pubitemid 29106037)
37. J.M. Fritschy, C. Sidler, F. Parpan, M. Gassmann, K. Kaupmann, B. Bettler, and D. Benke Independent maturation of the GABA(B) receptor subunits GABA(B1) and GABA(B2) during postnatal development in rodent brain J Comp Neurol 477 2004 235 252 (Pubitemid 39129610)
38. B inhibition in the rat somatosensory cortex J Neurophysiol 70 1993 448 452 (Pubitemid 23220328)
39. + current in voltage-clamped CA3 pyramidal cells in hippocampal cultures Proc Natl Acad Sci U S A 82 1985 1558 1562 (Pubitemid 15120584)
40. A and B-mediated inhibition in the CA3 hippocampal region of the rat J Neurobiol 26 1995 339 349
41. J.L. Gaïarsa, O. Caillard, and Y. Ben Ari Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance Trends Neurosci 25 2002 564 570 (Pubitemid 35254180)
42. A. Gartner, and V. Staiger Neurotrophin secretion from hippocampal neurons evoked by long-term-potentiation-inducing electrical stimulation patterns Proc Natl Acad Sci U S A 99 2002 6386 6391 (Pubitemid 34493321)
43. S. Ge, E.L. Goh, K.A. Sailor, Y. Kitabatake, G.L. Ming, and H. Song GABA regulates synaptic integration of newly generated neurons in the adult brain Nature 439 2006 589 593 (Pubitemid 43185382)
44. B receptor agonist baclofen Physiol Genomics 22 2005 93 98 (Pubitemid 41356711)
45. K. Gottmann, T. Mittmann, and V. Lessmann BDNF signaling in the formation, maturation and plasticity of glutamatergic and GABAergic synapses Exp Brain Res 199 2009 203 234
46. P. Gubellini, Y. Ben-Ari, and J.-L. Gaïarsa Activity- and age-dependent GABAergic synaptic plasticity in the developing rat hippocampus Eur J Neurosci 14 2001 1937 1946 (Pubitemid 35463680)
47. P. Gubellini, Y. Ben Ari, and J.L. Gaiarsa Endogenous neurotrophins are required for the induction of GABAergic long-term potentiation in the neonatal rat hippocampus J Neurosci 25 2005 5796 5802 (Pubitemid 40847892)
48. M. Hartmann, R. Heumann, and V. Lessmann Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses EMBO J 20 2001 5887 5897 (Pubitemid 33049264)
49. K. Heese, U. Otten, P. Mathivet, M. Raiteri, C. Marescaux, and R. Bernasconi GABA(B) receptor antagonists elevate both mRNA and protein levels of the neurotrophins nerve growth factor (NGF) and brain-derived neurotrophic factor (BDNF) but not neurotrophin-3 (NT-3) in brain and spinal cord of rats Neuropharmacology 39 2000 449 462 (Pubitemid 30052934)
50. M. Hirono, T. Yoshioka, and S. Konishi GABA(B) receptor activation enhances mGluR-mediated responses at cerebellar excitatory synapses Nat Neurosci 4 2001 1207 1216 (Pubitemid 33135626)
51. Z.J. Huang, G. Di Cristo, and F. Ango Development of GABA innervation in the cerebral and cerebellar cortices Nat Rev Neurosci 8 2007 673 686 (Pubitemid 47283143)
52. A.D. Huberman, and A.K. McAllister Neurotrophins and visual cortical plasticity Prog Brain Res 138 2002 39 51 (Pubitemid 35460906)
53. T. Inagaki, T. Begum, F. Reza, S. Horibe, M. Inaba, Y. Yoshimura, and Y. Komatsu Brain-derived neurotrophic factor-mediated retrograde signaling required for the induction of long-term potentiation at inhibitory synapses of visual cortical pyramidal neurons Neurosci Res 61 2008 192 200
54. J.S. Isaacson, and R.A. Nicoll Local and diffuse synaptic actions of GABA in the hippocampus Neuron 10 1993 165 175 (Pubitemid 23079539)
55. B receptor in cultured cerebellar granule cells J Neurochem 65 1995 75 83
56. K.A. Jones, B. Borowsky, J.A. Tamm, D.A. Craig, M.M. Durkin, M. Dai, W.J. Yao, M. Johnson, C. Gunwaldsen, L.Y. Huang, C. Tang, Q. Shen, J.A. Salon, K. Morse, T. Laz, K.E. Smith, D. Nagarathnam, S.A. Noble, T.A. Branchek, and C. Gerald GABA(B) receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GABA(B)R2 Nature 396 1998 674 679 (Pubitemid 29003945)
57. K. Kandler, and D.C. Gillespie Developmental refinement of inhibitory sound-localization circuits Trends Neurosci 28 2005 290 296 (Pubitemid 40775773)
58. B.A. Karpinski, G.D. Morle, J. Huggenvik, M.D. Uhler, and J.M. Leiden Molecular cloning of human CREB-2: an ATF/CREB transcription factor that can negatively regulate transcription from the cAMP response element Proc Natl Acad Sci U S A 89 1992 4820 4824
59. L.C. Katz, and C.J. Shatz Synaptic activity and the construction of cortical circuits Science 274 1996 1133 1138 (Pubitemid 26389269)
60. B receptors uncovers similarity to metabotropic glutamate receptors Nature 386 1997 239 246 (Pubitemid 27142503)
61. K. Kaupmann, B. Malitschek, V. Schuler, J. Heid, W. Froestl, P. Beck, J. Mosbacher, S. Bischoff, A. Kulik, R. Shigemoto, A. Karschin, and B. Bettler GABA(B)-receptor subtypes assemble into functional heteromeric complexes Nature 396 1998 683 687 (Pubitemid 29003947)
62. + channels Proc Natl Acad Sci U S A 95 1998 14991 14996 (Pubitemid 29003744)
63. I. Khalilov, M. Esclapez, I. Medina, D. Aggoun, K. Lamsa, X. Leinekugel, R. Khazipov, and Y. Ben-Ari A novel in vitro preparation: the intact hippocampal formation Neuron 19 1997 743 749 (Pubitemid 27471379)
64. R. Khazipov, and H.J. Luhmann Early patterns of electrical activity in the developing cerebral cortex of humans and rodents Trends Neurosci 29 2006 414 418 (Pubitemid 44108244)
65. A receptors clustered at neocortical synapses J Neurosci 22 2002 1328 1337 (Pubitemid 34163734)
66. M.O. Kim, S. Li, M.S. Park, and J.P. Hornung Early fetal expression of GABA(B1) and GABA(B2) receptor mRNAs on the development of the rat central nervous system Dev Brain Res 143 2003 47 55 (Pubitemid 36588682)
67. K. Kirmse, and S. Kirischuk Ambient GABA constrains the strength of GABAergic synapses at Cajal-Retzius cells in the developing visual cortex J Neurosci 26 2006 4216 4227 (Pubitemid 44315381)
68. R. Kolarow, T. Brigadski, and V. Lessmann Postsynaptic secretion of BDNF and NT-3 from hippocampal neurons depends on calcium calmodulin kinase II signaling and proceeds via delayed fusion pore opening J Neurosci 27 2007 10350 10364 (Pubitemid 47501996)
69. Y. Komatsu Age-dependent long-term potentiation of inhibitory synaptic transmission in rat visual cortex J Neurosci 14 1994 6488 6499 (Pubitemid 24333070)
70. 2+ release are involved in the induction of long-term potentiation at visual cortical inhibitory synapses J Neurosci 16 1996 6342 6352 (Pubitemid 26337358)
71. 2+ fluctuations J Neurobiol 37 1998 110 130 (Pubitemid 28453389)
72. V.C. Kotak, and D.H. Sanes Long-lasting inhibitory synaptic depression is age- and calcium-dependent J Neurosci 20 2000 5820 5826 (Pubitemid 30636911)
73. B and Trk receptor signaling mediates long-lasting inhibitory synaptic depression J Neurophysiol 86 2001 536 540 (Pubitemid 32623256)
74. N. Kuczewski, A. Langlois, H. Fiorentino, S. Bonnet, T. Marissal, D. Diabira, N. Ferrand, C. Porcher, and J.L. Gaiarsa Spontaneous glutamatergic activity induces a BDNF-dependent potentiation of GABAergic synapses in the newborn rat hippocampus J Physiol 586 2008 5119 5128
75. N. Kuczewski, C. Porcher, N. Ferrand, H. Fiorentino, C. Pellegrino, R. Kolarow, V. Lessmann, I. Medina, and J.L. Gaiarsa Backpropagating action potentials trigger dendritic release of BDNF during spontaneous network activity J Neurosci 28 2008 7013 7023
76. N. Kuczewski, C. Porcher, V. Lessmann, I. Medina, and J.L. Gaiarsa Activity-dependent dendritic release of BDNF and biological consequences Mol Neurobiol 39 2009 37 49
77. N. Kuczewski, C. Fuchs, N. Ferrand, J.N. Jovanovic, J.L. Gaiarsa, and C. Porcher Mechanism of GABA(B) receptor-induced BDNF secretion and promotion of GABA(A) receptor membrane expression J Neurochem 118 4 2011 533 545
78. A. Kulik, I. Vida, R. Lujan, C.A. Haas, G. Lopez-Bendito, R. Shigemoto, and M. Frotscher Subcellular localization of metabotropic GABA(B) receptor subunits GABA(B1a/b) and GABA(B2) in the rat hippocampus J Neurosci 23 2003 11026 11035 (Pubitemid 37548936)
79. V. Lessmann, and T. Brigadski Mechanisms, locations, and kinetics of synaptic BDNF secretion: an update Neurosci Res 65 2009 11 22
80. V. Lessmann, K. Gottmann, and M. Malcangio Neurotrophin secretion: current facts and future prospects Prog Neurobiol 69 2003 341 374 (Pubitemid 36645053)
81. G. Liang, and T. Hai Characterization of human activating transcription factor 4, a transcriptional activator that interacts with multiple domains of cAMP-responsive element-binding protein (CREB)-binding protein J Biol Chem 272 1997 24088 24095 (Pubitemid 27410995)
82. C.C. Lien, Y. Mu, M. Vargas-Caballero, and M.M. Poo Visual stimuli-induced LTD of GABAergic synapses mediated by presynaptic NMDA receptors Nat Neurosci 9 2006 372 380 (Pubitemid 43290967)
83. G. Lopez-Bendito, R. Shigemoto, A. Kulik, O. Paulsen, A. Fairen, and R. Lujan Expression and distribution of metabotropic GABA receptor subtypes GABABR1 and GABABR2 during rat neocortical development Eur J Neurosci 15 2002 1766 1778 (Pubitemid 35476895)
84. G. Lopez-Bendito, R. Lujan, R. Shigemoto, P. Ganter, O. Paulsen, and Z. Molnar Blockade of GABA(B) receptors alters the tangential migration of cortical neurons Cereb Cortex 13 2003 932 942 (Pubitemid 37064830)
85. B2 in the rat hippocampus during prenatal and postnatal development Hippocampus 14 2004 836 848 (Pubitemid 39517461)
86. J.J. LoTurco, D.F. Owens, M.J. Heath, M.B. Davis, and A.R. Kriegstein GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis Neuron 15 1995 1287 1298 (Pubitemid 26005367)
87. B. Lu, P.T. Pang, and N.H. Woo The yin and yang of neurotrophin action Nat Rev Neurosci 6 2005 603 614 (Pubitemid 41059335)
88. H.J. Luhmann, and D.A. Prince Postnatal maturation of the GABAergic system in rat neocortex J Neurophysiol 65 1991 247 263
89. B2 relative to synaptic sites in the rat developing cerebellum Eur J Neurosci 23 2006 1479 1490
90. K. Luyt, T.P. Slade, J.J. Dorward, C.F. Durant, Y. Wu, R. Shigemoto, S.J. Mundell, A. Varadi, and E. Molnar Developing oligodendrocytes express functional GABA(B) receptors that stimulate cell proliferation and migration J Neurochem 100 2007 822 840 (Pubitemid 46095631)
91. J.P. Magby, C. Bi, Z.Y. Chen, F.S. Lee, and M.R. Plummer Single-cell characterization of retrograde signaling by brain-derived neurotrophic factor J Neurosci 26 2006 13531 13536 (Pubitemid 46026485)
92. J.B. Manent, and A. Represa Neurotransmitters and brain maturation: early paracrine actions of GABA and glutamate modulate neuronal migration Neuroscientist 13 2007 268 279 (Pubitemid 46801760)
93. S.C. Martin, J.L. Steiger, M.C. Gravielle, H.R. Lyons, S.J. Russek, and D.H. Farb Differential expression of gamma-aminobutyric acid type B receptor subunit mRNAs in the developing nervous system and receptor coupling to adenylyl cyclase in embryonic neurons J Comp Neurol 473 2004 16 29 (Pubitemid 38507116)
94. B receptors role in cell migration and positioning within the ventromedial nucleus of the hypothalamus Neuroscience 151 2008 1119 1131
95. H.A. McLean, O. Caillard, Y. Ben-Ari, and J.-L. Gaïarsa Bidirectional plasticity expressed by GABAergic synapses in the neonatal rat hippocampus J Physiol 496 1996 471 477 (Pubitemid 26370918)
96. B receptors and controls network activity in the neonatal rat hippocampus J Neurophysiol 76 1996 1036 1046 (Pubitemid 26284587)
97. A. Michler Involvement of GABA receptors in the regulation of neurite growth in cultured embryonic chick tectum Int J Dev Neurosci 8 1990 463 472 (Pubitemid 20298954)
98. 2+ channels in central neurons Neuron 10 1993 889 898 (Pubitemid 23152044)
99. B receptor directly interacts with the activating transcription factor 4 J Biol Chem 275 2000 35185 35191
100. 2+ influx via store-operated channels in rat cortical neurons and transfected Chinese hamster ovary cells Neuroscience 137 2006 1347 1358 (Pubitemid 43133158)
101. S. Nurse, and J.C. Lacaille Late maturation of GABA(B) synaptic transmission in area CA1 of the rat hippocampus Neuropharmacology 38 1999 1733 1742 (Pubitemid 29430248)
102. B receptor-mediated inhibition of GABAA receptor calcium elevations in developing hypothalamic neurons J Neurophysiol 79 1998 1360 1370 (Pubitemid 28125371)
103. B receptor-mediated regulation of glutamate-activated calcium transients in hypothalamic and cortical neuron development J Neurophysiol 81 1999 94 102 (Pubitemid 29330064)
104. B receptors Eur J Pharmacol 187 1990 27 38 (Pubitemid 20323920)
105. D.F. Owens, and A.R. Kriegstein Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3 2002 715 727 (Pubitemid 135706677)
106. P. Panzanelli, G. Lopez-Bendito, R. Lujan, and M. Sassoe-Pognetto Localization and developmental expression of GABA(B) receptors in the rat olfactory bulb J Neurocytol 33 2004 87 99 (Pubitemid 38860221)
107. 2+ spikes in layer 5 somatosensory pyramidal neurons Neuron 50 2006 603 616
108. M.M. Poo Neurotrophins as synaptic modulators Nat Rev Neurosci 2 2001 24 32
109. B receptor expression and function in olfactory receptor neuron axon growth J Neurobiol 60 2004 154 165 (Pubitemid 39006989)
110. H.M. Prosser, C.H. Gill, W.D. Hirst, E. Grau, M. Robbins, A. Calver, E.M. Soffin, C.E. Farmer, C. Lanneau, J. Gray, E. Schenck, B.S. Warmerdam, C. Clapham, C. Reavill, D.C. Rogers, T. Stean, N. Upton, K. Humphreys, A. Randall, M. Geppert, C.H. Davies, and M.N. Pangalos Epileptogenesis and enhanced prepulse inhibition in GABA(B1)-deficient mice Mol Cell Neurosci 17 2001 1059 1070 (Pubitemid 32641874)
111. M.J. Rebecchi, and S.N. Pentyala Structure, function, and control of phosphoinositide-specific phospholipase C Physiol Rev 80 2000 1291 1335
112. X. Ren, and I. Mody gamma-Hydroxybutyrate induces cyclic AMP-responsive element-binding protein phosphorylation in mouse hippocampus: an involvement of GABA(B) receptors and cAMP-dependent protein kinase activation Neuroscience 141 2006 269 275
113. A. Represa, and Y. Ben Ari Trophic actions of GABA on neuronal development Trends Neurosci 28 2005 278 283 (Pubitemid 40775771)
114. A. Reynolds, E. Brustein, M. Liao, A. Mercado, E. Babilonia, D.B. Mount, and P. Drapeau Neurogenic role of the depolarizing chloride gradient revealed by global overexpression of KCC2 from the onset of development J Neurosci 28 2008 1588 1597 (Pubitemid 351287036)
115. C.M. Root, N.A. Velazquez-Ulloa, G.C. Monsalve, E. Minakova, and N.C. Spitzer Embryonically expressed GABA and glutamate drive electrical activity regulating neurotransmitter specification J Neurosci 28 2008 4777 4784
116. M. Scanziani GABA spillover activates postsynaptic GABA(B) receptors to control rhythmic hippocampal activity Neuron 25 2000 673 681
117. 2+ currents and synaptic transmission in cultured rat hippocampal neurones J Physiol 444 1991 669 686
118. F.J. Seil, and R. Drake-Baumann Reduced cortical inhibitory synaptogenesis in organotypic cerebellar cultures developing in the absence of neuronal activity J Comp Neurol 342 1994 366 377 (Pubitemid 24105094)
119. L.A. Selbie, and S.J. Hill G protein-coupled-receptor cross-talk: the fine-tuning of multiple receptor-signalling pathways Trends Pharmacol Sci 19 1998 87 93 (Pubitemid 28197809)
120. W. Shen, and M.M. Slaughter Metabotropic GABA receptors facilitate L-type and inhibit N-type calcium channels in single salamander retinal neurons J Physiol 516 1999 711 718 (Pubitemid 29201897)
121. H.J. Song, and M.M. Poo Signal transduction underlying growth cone guidance by diffusible factors Curr Opin Neurobiol 9 1999 355 363
122. N.C. Spitzer Electrical activity in early neuronal development Nature 444 2006 707 712 (Pubitemid 44949593)
123. J.L. Steiger, S. Bandyopadhyay, D.H. Farb, and S.J. Russek cAMP response element-binding protein, activating transcription factor-4, and upstream stimulatory factor differentially control hippocampal GABABR1a and GABABR1b subunit gene expression through alternative promoters J Neurosci 24 2004 6115 6126 (Pubitemid 38891102)
124. M. Tessier-Lavigne, and C.S. Goodman The molecular biology of axon guidance Science 274 1996 1123 1133 (Pubitemid 26389268)
125. H. Thoenen Neurotrophins and neuronal plasticity Science 270 1995 593 598
126. B-mediated inhibition and induction of epileptiform discharges in the neonatal rat hippocampus Eur J Neurosci 19 2004 3227 3234 (Pubitemid 38859540)
127. B receptor signalling in the developing rat hippocampus J Physiol 568 2005 951 966 (Pubitemid 41646034)
128. B-mediated effects on protein kinase C activity and immunoreactivity in neonatal and adult rat hippocampal slices J Neurochem 65 1995 863 870
129. B receptor-mediated-ERK1/2/CREB pathway in cerebellar neurons Cell Signal 19 2007 1996 2002 (Pubitemid 47086373)
130. B receptor activation protects neurons from apoptosis via IGF-1 receptor transactivation J Neurosci 30 2010 749 759
131. B binding in rat brain Neuroscience 62 1994 601 613
132. A.M. Vanhoose, M. Emery, L. Jimenez, and D.G. Winder ERK activation by G-protein-coupled receptors in mouse brain is receptor identity-specific J Biol Chem 277 2002 9049 9053 (Pubitemid 34952979)
133. J.A. Verheugen, D. Fricker, and R. Miles Noninvasive measurements of the membrane potential and GABAergic action in hippocampal interneurons J Neurosci 19 1999 2546 2555 (Pubitemid 29162403)
134. E. Vernon, G. Meyer, L. Pickard, K. Dev, E. Molnar, G.L. Collingridge, and J.M. Henley GABA(B) receptors couple directly to the transcription factor ATF4 Mol Cell Neurosci 17 2001 637 645 (Pubitemid 32430040)
135. B receptor variants Neuron 50 2006 589 601
136. D.D. Wang, and A.R. Kriegstein GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation J Neurosci 28 2008 5547 5558
137. J.H. White, A. Wise, M.J. Main, A. Green, N.J. Fraser, G.H. Disney, A.A. Barnes, P. Emson, S.M. Foord, and F.H. Marshall Heterodimerization is required for the formation of a functional GABA(B) receptor Nature 396 1998 679 682 (Pubitemid 29003946)
138. B receptor interacts directly with the related transcription factors CREB2 and ATFx Proc Natl Acad Sci U S A 97 2000 13967 13972
139. Y. Xiang, Y. Li, Z. Zhang, K. Cui, S. Wang, X.B. Yuan, C.P. Wu, M.M. Poo, and S. Duan Nerve growth cone guidance mediated by G protein-coupled receptors Nat Neurosci 5 2002 843 848 (Pubitemid 34976648)
140. C. Xu, M.X. Zhao, M.M. Poo, and X.H. Zhang GABA(B) receptor activation mediates frequency-dependent plasticity of developing GABAergic synapses Nat Neurosci 11 2008 1410 1418
141. H. Xu, V.C. Kotak, and D.H. Sanes Normal hearing is required for the emergence of long-lasting inhibitory potentiation in cortex J Neurosci 30 2010 331 341
142. L.I. Zhang, and M.M. Poo Electrical activity and development of neural circuits Nat Neurosci 4l 2001 1207 1214 (Pubitemid 33733110)