title: A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex.
abstract: Early sensory experience instructs the maturation of neural circuitry in the cortex. This has been studied extensively in the primary visual cortex, in which loss of vision to one eye permanently degrades cortical responsiveness to that eye, a phenomenon known as ocular dominance plasticity (ODP). Cortical inhibition mediates this process, but the precise role of specific classes of inhibitory neurons in ODP is controversial. Here we report that evoked firing rates of binocular excitatory neurons in the primary visual cortex immediately drop by half when vision is restricted to one eye, but gradually return to normal over the following twenty-four hours, despite the fact that vision remains restricted to one eye. This restoration of binocular-like excitatory firing rates after monocular deprivation results from a rapid, although transient, reduction in the firing rates of fast-spiking, parvalbumin-positive (PV) interneurons, which in turn can be attributed to a decrease in local excitatory circuit input onto PV interneurons. This reduction in PV-cell-evoked responses after monocular lid suture is restricted to the critical period for ODP and appears to be necessary for subsequent shifts in excitatory ODP. Pharmacologically enhancing inhibition at the time of sight deprivation blocks ODP and, conversely, pharmacogenetic reduction of PV cell firing rates can extend the critical period for ODP. These findings define the microcircuit changes initiating competitive plasticity during critical periods of cortical development. Moreover, they show that the restoration of evoked firing rates of layer 2/3 pyramidal neurons by PV-specific disinhibition is a key step in the progression of ODP.
authors: Department of Neurobiology, David Geffen School of Medicine, University of California, Los Angeles, California 90048, USA.
authors: Sandra J
authors: SJ
authors: Kuhlman
authors: Nicholas D
authors: ND
authors: Olivas
authors: Elaine
authors: E
authors: Tring
authors: Taruna
authors: T
authors: Ikrar
authors: Xiangmin
authors: X
authors: Xu
authors: Joshua T
authors: JT
authors: Trachtenberg
mesh_terms: D000818:Animals; D003423:Critical Period, Psychological; D023882:Dominance, Ocular / Q000187:drug effects / Q000502:physiology*; D005260:Female; D007395:Interneurons / Q000166:cytology / Q000187:drug effects; D007834:Lasers; D008297:Male; D051379:Mice; D009433:Neural Inhibition / Q000187:drug effects; D009473:Neuronal Plasticity / Q000187:drug effects / Q000502:physiology*; D010320:Parvalbumins / Q000378:metabolism; D010775:Photic Stimulation; D012683:Sensory Deprivation / Q000502:physiology; D015348:Vision, Binocular / Q000187:drug effects / Q000502:physiology; D015349:Vision, Monocular / Q000187:drug effects / Q000502:physiology*; D014793:Visual Cortex / Q000166:cytology / Q000187:drug effects / Q000502:physiology*
chemical_list: D010320:Parvalbumins
references: Nat Neurosci. 2005 Nov;8(11):1552-9
references: 16222228
references: J Neurosci. 1996 May 15;16(10):3274-86
references: 8627365
references: Nat Neurosci. 2011 Jul 12;14(9):1121-3
references: 21750548
references: Nat Neurosci. 2011 Jan;14(1):22-4
references: 21131952
references: Nature. 2013 Apr 4;496(7443):96-100
references: 23552948
references: Proc Natl Acad Sci U S A. 2007 Mar 20;104(12):5163-8
references: 17360345
references: J Neurosci. 1999 Jun 1;19(11):4388-406
references: 10341241
references: Nature. 2007 Nov 15;450(7168):425-9
references: 18004384
references: Trends Neurosci. 2011 Apr;34(4):177-87
references: 21397343
references: J Neurosci. 2010 Jan 6;30(1):361-71
references: 20053917
references: Neuron. 2012 Jul 12;75(1):121-32
references: 22794266
references: Arch Ophthalmol. 2011 Nov;129(11):1451-7
references: 21746970
references: Neuron. 2007 Oct 4;56(1):43-57
references: 17920014
references: Nat Methods. 2004 Oct;1(1):31-7
references: 15782150
references: J Neurosci. 2010 Jan 27;30(4):1551-9
references: 20107082
references: Mol Biosyst. 2010 Aug;6(8):1376-80
references: 20532295
references: PLoS Biol. 2011 Jan 04;9(1):e1000572
references: 21245906
references: J Neurosci. 2005 Jun 15;25(24):5670-9
references: 15958733
references: Nat Rev Neurosci. 2005 Nov;6(11):877-88
references: 16261181
references: Prog Brain Res. 2011;191:119-31
references: 21741548
references: Biomed Eng Online. 2003 May 17;2:13
references: 12801419
references: Nat Neurosci. 2008 Mar;11(3):360-6
references: 18246064
references: Nat Rev Neurosci. 2009 Sep;10(9):647-58
references: 19693029
references: J Neurophysiol. 1963 Nov;26:1003-17
references: 14084161
references: Pharmacol Rev. 2011 Jun;63(2):291-315
references: 21415127
references: Int Ophthalmol. 2011 Jun;31(3):249-56
references: 21424553
references: Neuron. 2009 Jul 16;63(1):27-39
references: 19607790
references: Neuron. 2007 Oct 25;56(2):327-38
references: 17964249
references: Nature. 2011 Dec 07;480(7377):331-5
references: 22158104
references: Nature. 2009 Nov 12;462(7270):218-21
references: 19907494
references: Nature. 2013 Jul 18;499(7458):295-300
references: 23868258
references: J Neurosci. 2013 May 15;33(20):8810-9
references: 23678123
references: PLoS One. 2010 Nov 24;5(11):e15517
references: 21124805
references: Nat Protoc. 2009;4(8):1128-44
references: 19617885
references: Neuron. 2003 Apr 24;38(2):277-89
references: 12718861
references: Brain Res Brain Res Rev. 2005 Dec 1;50(1):126-33
references: 16024085
references: J Neurophysiol. 2010 Apr;103(4):2301-12
references: 20130040
references: Neuron. 2007 Jun 21;54(6):961-72
references: 17582335
references: Proc Natl Acad Sci U S A. 2003 Jun 10;100(12):7319-24
references: 12777621
references: Proc Natl Acad Sci U S A. 2008 Oct 28;105(43):16797-802
references: 18940923
references: IEEE Trans Image Process. 1998;7(3):359-69
references: 18276256
references: Clin Exp Optom. 2005 Nov;88(6):365-75
references: 16329744
references: Nat Neurosci. 2013 Mar;16(3):332-9
references: 23354330
references: Annu Rev Neurosci. 2012;35:309-30
references: 22462544
references: Front Neural Circuits. 2010 Aug 26;4:100
references: 21960959