title: Rebound potentiation of inhibition in juvenile visual cortex requires vision-induced BDNF expression.
abstract: The developmental increase in the strength of inhibitory synaptic circuits defines the time window of the critical period for plasticity in sensory cortices. Conceptually, plasticity of inhibitory synapses is an attractive mechanism to allow for homeostatic adaptation to the sensory environment. However, a brief duration of visual deprivation that causes maximal change in excitatory synapses produces minimal change in inhibitory synaptic transmission. Here we examined developmental and experience-dependent changes in inhibition by measuring miniature IPSCs (mIPSCs) in layer 2/3 pyramidal neurons of mouse visual cortex. During development from postnatal day 21 (P21) to P35, GABAA receptor function changed from fewer higher-conductance channels to more numerous lower-conductance channels without altering the average mIPSC amplitude. Although a week of visual deprivation did not alter the average mIPSC amplitude, a subsequent 2 h exposure to light produced a rapid rebound potentiation. This form of plasticity is restricted to a critical period before the developmental change in GABAergic synaptic properties is completed, and hence is absent by P35. Visual experience-dependent rebound potentiation of mIPSCs is accompanied by an increase in the open channel number and requires activity-dependent transcription of brain-derived neurotrophic factor (BDNF). Mice lacking BDNF transcription through promoter IV did not show developmental changes in inhibition and lacked rebound potentiation. Our results suggest that sensory experience may have distinct functional consequences in normal versus deprived sensory cortices, and that experience-dependent BDNF expression controls the plasticity of inhibitory synaptic transmission particularly when recovering vision during the critical period.
authors.affiliation: The Solomon H. Snyder Department of Neuroscience, The Zanvyl-Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, Maryland 21218, Department of Biology, University of Maryland, College Park, Maryland 20742.
authors.forename: Ming
authors.initials: M
authors.lastname: Gao
authors.affiliation: Lieber Institute for Brain Development, Baltimore, Maryland 21205, and.
authors.forename: Kristen R
authors.initials: KR
authors.lastname: Maynard
authors.affiliation: The Solomon H. Snyder Department of Neuroscience, The Zanvyl-Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, Maryland 21218.
authors.forename: Varun
authors.initials: V
authors.lastname: Chokshi
authors.affiliation: The Solomon H. Snyder Department of Neuroscience, The Zanvyl-Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, Maryland 21218, Department of Biology, University of Maryland, College Park, Maryland 20742.
authors.forename: Lihua
authors.initials: L
authors.lastname: Song
authors.affiliation: Department of Biology, University of Maryland, College Park, Maryland 20742.
authors.forename: Cara
authors.initials: C
authors.lastname: Jacobs
authors.affiliation: The Solomon H. Snyder Department of Neuroscience, The Zanvyl-Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, Maryland 21218.
authors.forename: Hui
authors.initials: H
authors.lastname: Wang
authors.affiliation: The Solomon H. Snyder Department of Neuroscience, The Zanvyl-Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, Maryland 21218.
authors.forename: Trinh
authors.initials: T
authors.lastname: Tran
authors.affiliation: Lieber Institute for Brain Development, Baltimore, Maryland 21205, and Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205.
authors.forename: Keri
authors.identifier: http://orcid.org/0000-0002-5237-0789
authors.initials: K
authors.lastname: Martinowich
authors.affiliation: The Solomon H. Snyder Department of Neuroscience, The Zanvyl-Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, Maryland 21218, Department of Biology, University of Maryland, College Park, Maryland 20742, heykyounglee@jhu.edu.
authors.forename: Hey-Kyoung
authors.initials: HK
authors.lastname: Lee
mesh_terms: D000367:Age Factors; D000818:Animals; D000831:Animals, Newborn; D001703:Biophysics; D019208:Brain-Derived Neurotrophic Factor / Q000235:genetics / Q000378:metabolism*; D004558:Electric Stimulation; D018507:Gene Expression Regulation, Developmental / Q000235:genetics; D005968:Glutamate Decarboxylase / Q000378:metabolism; D066298:In Vitro Techniques; D053444:Inhibitory Postsynaptic Potentials / Q000187:drug effects / Q000235:genetics; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D018613:Microscopy, Confocal; D009433:Neural Inhibition / Q000187:drug effects / Q000235:genetics / Q000502:physiology*; D009474:Neurons / Q000187:drug effects / Q000502:physiology*; D018408:Patch-Clamp Techniques; D012683:Sensory Deprivation / Q000502:physiology; D014785:Vision, Ocular / Q000502:physiology*; D014793:Visual Cortex / Q000166:cytology*
chemical_list: D019208:Brain-Derived Neurotrophic Factor; D005968:Glutamate Decarboxylase; C401141:glutamate decarboxylase 2
keywords: BDNF; activity-dependent; critical period; mIPSC; potentiation; visual cortex
references.citation: J Neurosci. 2007 Sep 5;27(36):9648-52
references.pmid: 17804625
references.citation: J Neurosci. 2007 Jun 20;27(25):6692-700
references.pmid: 17581956
references.citation: Neuron. 2001 Jan;29(1):157-69
references.pmid: 11182088
references.citation: Neuron. 2012 Jul 26;75(2):230-49
references.pmid: 22841309
references.citation: PLoS One. 2011 Mar 31;6(3):e18264
references.pmid: 21483826
references.citation: J Neurosci. 2013 Jul 10;33(28):11440-50
references.pmid: 23843516
references.citation: Neuron. 2010 Apr 29;66(2):248-59
references.pmid: 20435001
references.citation: Nat Neurosci. 2006 May;9(5):642-9
references.pmid: 16582905
references.citation: Neuron. 2003 Jun 19;38(6):977-85
references.pmid: 12818182
references.citation: Cell. 1999 Sep 17;98(6):739-55
references.pmid: 10499792
references.citation: PLoS One. 2008 Aug 20;3(8):e2979
references.pmid: 18714334
references.citation: Nat Neurosci. 1999 Apr;2(4):352-7
references.pmid: 10204542
references.citation: J Neurosci. 1996 May 15;16(10):3274-86
references.pmid: 8627365
references.citation: J Neurosci. 2010 May 26;30(21):7168-78
references.pmid: 20505084
references.citation: Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12876-80
references.pmid: 10536016
references.citation: Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):12486-91
references.pmid: 14514885
references.citation: Neuron. 2008 Nov 26;60(4):610-24
references.pmid: 19038219
references.citation: Mol Brain. 2011 Mar 09;4:11
references.pmid: 21388527
references.citation: J Neurosci. 2012 Mar 21;32(12):3981-91
references.pmid: 22442065
references.citation: Nat Neurosci. 2006 Aug;9(8):1001-3
references.pmid: 16819524
references.citation: Neuron. 1990 Oct;5(4):501-9
references.pmid: 1688327
references.citation: J Neurosci Res. 2007 Feb 15;85(3):525-35
references.pmid: 17149751
references.citation: J Neurosci. 2010 Oct 20;30(42):14261-72
references.pmid: 20962247
references.citation: J Neurophysiol. 1994 Apr;71(4):1318-35
references.pmid: 8035217
references.citation: J Neurosci. 2004 Oct 27;24(43):9598-611
references.pmid: 15509747
references.citation: Mol Cell Neurosci. 2006 Mar;31(3):481-92
references.pmid: 16330218
references.citation: Brain Res Brain Res Rev. 2005 Dec 1;50(1):126-33
references.pmid: 16024085
references.citation: Nat Protoc. 2007;2(2):434-48
references.pmid: 17406605
references.citation: Proc Natl Acad Sci U S A. 2013 Sep 10;110(37):15103-8
references.pmid: 23980178
references.citation: Proc Natl Acad Sci U S A. 2009 Apr 7;106(14):5942-7
references.pmid: 19293383
references.citation: Cell Tissue Res. 2006 Nov;326(2):505-16
references.pmid: 16937111
references.citation: Nat Neurosci. 2008 Apr;11(4):497-504
references.pmid: 18311133
references.citation: Annu Rev Neurosci. 2012;35:309-30
references.pmid: 22462544
references.citation: Proc Natl Acad Sci U S A. 2011 Jul 19;108(29):12131-6
references.pmid: 21730187
references.citation: Nature. 2008 Oct 30;455(7217):1198-204
references.pmid: 18815592
references.citation: J Neurosci. 2002 Sep 15;22(18):8084-90
references.pmid: 12223562
references.citation: Neural Plast. 2009;2009:415135
references.pmid: 19503840
references.citation: Nat Neurosci. 2010 May;13(5):592-600
references.pmid: 20348918