title: Spontaneous glutamatergic activity induces a BDNF-dependent potentiation of GABAergic synapses in the newborn rat hippocampus.
abstract: Spontaneous ongoing synaptic activity is thought to play an instructive role in the maturation of the neuronal circuits. However the type of synaptic activity involved and how this activity is translated into structural and functional changes is not fully understood. Here we show that ongoing glutamatergic synaptic activity triggers a long-lasting potentiation of gamma-aminobutyric acid (GABA) mediated synaptic activity (LLP(GABA-A)) in the developing rat hippocampus. LLP(GABA-A) induction requires (i) the activation of AMPA receptors and L-type voltage-dependent calcium channels, (ii) the release of endogenous brain-derived neurotrophic factor (BDNF), and (iii) the activation of postsynaptic tropomyosin-related kinase receptors B (TrkB). We found that spontaneous glutamatergic activity is required to maintain a high level of native BDNF in the newborn rat hippocampus and that application of exogenous BDNF induced LLP(GABA-A) in the absence of glutamatergic activity. These results suggest that ongoing glutamatergic synaptic activity plays a pivotal role in the functional maturation of hippocampal GABAergic synapses by means of a cascade involving BDNF release and downstream signalling through postsynaptic TrkB receptor activation.
authors.affiliation: INSERM U901 (Institut National de la Santé et de la Recherche Médicale Unité 901), Marseille 13009, France.
authors.forename: Nicola
authors.initials: N
authors.lastname: Kuczewski
authors.forename: Anais
authors.initials: A
authors.lastname: Langlois
authors.forename: Hervé
authors.initials: H
authors.lastname: Fiorentino
authors.forename: Stéphanie
authors.initials: S
authors.lastname: Bonnet
authors.forename: Thomas
authors.initials: T
authors.lastname: Marissal
authors.forename: Diabe
authors.initials: D
authors.lastname: Diabira
authors.forename: Nadine
authors.initials: N
authors.lastname: Ferrand
authors.forename: Christophe
authors.initials: C
authors.lastname: Porcher
authors.forename: Jean-Luc
authors.initials: JL
authors.lastname: Gaiarsa
mesh_terms: D000200:Action Potentials / Q000502:physiology; D000818:Animals; D000831:Animals, Newborn; D019208:Brain-Derived Neurotrophic Factor / Q000378:metabolism*; D002118:Calcium / Q000378:metabolism; D020746:Calcium Channels, L-Type / Q000502:physiology; D018698:Glutamic Acid / Q000378:metabolism*; D006624:Hippocampus / Q000166:cytology* / Q000502:physiology; D051381:Rats; D017208:Rats, Wistar; D020813:Receptor, trkB / Q000502:physiology; D018091:Receptors, AMPA / Q000502:physiology; D011963:Receptors, GABA-A / Q000502:physiology; D013569:Synapses / Q000378:metabolism*; D005680:gamma-Aminobutyric Acid / Q000378:metabolism*
chemical_list: D019208:Brain-Derived Neurotrophic Factor; D020746:Calcium Channels, L-Type; D018091:Receptors, AMPA; D011963:Receptors, GABA-A; D018698:Glutamic Acid; D005680:gamma-Aminobutyric Acid; D020813:Receptor, trkB; D002118:Calcium
references.citation: J Neurosci. 1997 May 1;17(9):2959-66
references.pmid: 9096132
references.citation: J Physiol. 1989 Sep;416:303-25
references.pmid: 2575165
references.citation: J Neurosci. 2000 Nov 1;20(21):8087-95
references.pmid: 11050130
references.citation: EMBO J. 2001 Nov 1;20(21):5887-97
references.pmid: 11689429
references.citation: J Physiol. 2004 Aug 15;559(Pt 1):129-39
references.pmid: 15218067
references.citation: Eur J Neurosci. 1999 Apr;11(4):1179-90
references.pmid: 10103114
references.citation: Nat Neurosci. 2007 May;10(5):559-67
references.pmid: 17396124
references.citation: Neuron. 1990 Oct;5(4):511-26
references.pmid: 2206535
references.citation: Proc Natl Acad Sci U S A. 2004 Mar 16;101(11):3967-72
references.pmid: 15007179
references.citation: J Neurosci. 1998 Dec 15;18(24):10231-40
references.pmid: 9852560
references.citation: Development. 2003 Apr;130(7):1267-80
references.pmid: 12588844
references.citation: Nat Neurosci. 2001 Nov;4 Suppl:1207-14
references.pmid: 11687831
references.citation: Prog Neurobiol. 2003 Apr;69(5):341-74
references.pmid: 12787574
references.citation: J Physiol. 1999 Jul 1;518(Pt 1):109-19
references.pmid: 10373693
references.citation: Brain Res. 1995 Aug 21;689(2):172-82
references.pmid: 7583320
references.citation: J Neurosci. 2000 May 1;20(9):3221-32
references.pmid: 10777787
references.citation: J Neurosci Res. 2005 Mar 1;79(5):616-27
references.pmid: 15672445
references.citation: Proc Natl Acad Sci U S A. 1997 Nov 25;94(24):13279-86
references.pmid: 9371837
references.citation: J Neurosci. 2002 Dec 1;22(23):10399-407
references.pmid: 12451139
references.citation: Neuron. 1996 Mar;16(3):565-70
references.pmid: 8785053
references.citation: J Neurosci. 2008 Jul 2;28(27):7013-23
references.pmid: 18596175
references.citation: Cereb Cortex. 2005 Mar;15(3):291-8
references.pmid: 15238431
references.citation: Science. 2001 Mar 23;291(5512):2419-23
references.pmid: 11264540
references.citation: J Neurosci. 2002 Feb 15;22(4):1328-37
references.pmid: 11850460
references.citation: J Neurosci. 2007 Sep 26;27(39):10350-64
references.pmid: 17898207
references.citation: Neuron. 1999 Sep;24(1):261-73
references.pmid: 10677043
references.citation: Proc Natl Acad Sci U S A. 2007 Aug 7;104(32):13176-81
references.pmid: 17656555
references.citation: J Neurosci. 2004 Dec 15;24(50):11346-55
references.pmid: 15601941
references.citation: J Neurosci. 2003 Jul 2;23(13):5662-73
references.pmid: 12843269
references.citation: Pharmacol Ther. 2007 Feb;113(2):394-409
references.pmid: 17118456
references.citation: Trends Neurosci. 2002 Nov;25(11):564-70
references.pmid: 12392931
references.citation: J Neurosci. 2004 Oct 27;24(43):9598-611
references.pmid: 15509747
references.citation: J Neurosci. 2006 Dec 27;26(52):13531-6
references.pmid: 17192436
references.citation: J Neurosci. 2000 Jul 15;20(14):5367-73
references.pmid: 10884321
references.citation: J Neurosci. 2005 Aug 17;25(33):7601-14
references.pmid: 16107647
references.citation: Neuron. 1996 Dec;17(6):1057-64
references.pmid: 8982155
references.citation: Cereb Cortex. 2006 Jan;16(1):47-63
references.pmid: 15829735
references.citation: J Neurosci. 2005 Jun 15;25(24):5796-802
references.pmid: 15958746
references.citation: J Neurosci. 2002 Feb 1;22(3):931-45
references.pmid: 11826122
references.citation: J Neurosci. 1995 Jan;15(1 Pt 2):477-91
references.pmid: 7823156
references.citation: J Neurosci. 1997 Jun 15;17(12):4527-35
references.pmid: 9169513
references.citation: J Physiol. 1996 Oct 15;496 ( Pt 2):471-7
references.pmid: 8910230