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PMID: 9822384 Published · ppublish English Journal Article

Local GABA circuit control of experience-dependent plasticity in developing visual cortex.

Science (New York, N.Y.) ·Vol. 282 ·No. 5393 ·1998-11-20 ·Pages 1504-8

Hensch TK, Fagiolini M, Mataga N, Stryker MP, Baekkeskov S, Kash SF

Abstract

Sensory experience in early life shapes the mammalian brain. An impairment in the activity-dependent refinement of functional connections within developing visual cortex was identified here in a mouse model. Gene-targeted disruption of one isoform of glutamic acid decarboxylase prevented the competitive loss of responsiveness to an eye briefly deprived of vision, without affecting cooperative mechanisms of synapse modification in vitro. Selective, use-dependent enhancement of fast intracortical inhibitory transmission with benzodiazepines restored plasticity in vivo, rescuing the genetic defect. Specific networks of inhibitory interneurons intrinsic to visual cortex may detect perturbations in sensory input to drive experience-dependent plasticity during development.

MeSH Terms
Animals Diazepam/pharmacology GABA Modulators/pharmacology Gene Targeting Glutamate Decarboxylase/genetics,metabolism Interneurons/physiology Long-Term Potentiation Mice Mice, Inbred C57BL Mice, Knockout Neuronal Plasticity/drug effects Photic Stimulation Receptors, GABA-A/metabolism Synaptic Transmission Visual Cortex/cytology,metabolism,physiology Visual Pathways gamma-Aminobutyric Acid/metabolism
Chemicals
GABA Modulators Receptors, GABA-A gamma-Aminobutyric Acid Glutamate Decarboxylase Diazepam
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Hensch T K
Laboratory for Neuronal Circuit Development, Brain Science Institute RIKEN, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan. hensch@postman.riken.go.jp
Fagiolini M
Mataga N
Stryker M P
Baekkeskov S
Kash S F
References (78)
78 references, click to expand
  1. The benzodiazepine binding site of GABAA receptors.
    Trends Pharmacol Sci. 1997 Nov;18(11):425-9 PMID: 9426470
  2. Benzodiazepine ([3H]flunitrazepam) binding in cat visual cortex: ontogenesis of normal characteristics and the effects of dark rearing.
    Brain Res. 1987 Dec 15;465(1-2):67-76 PMID: 2830948
  3. Postnatal expression of glutamate decarboxylases in developing rat cerebellum.
    Neurochem Res. 1991 Mar;16(3):235-42 PMID: 1780026
  4. Spatiotemporally differential inhibition of pyramidal cells in the cat motor cortex.
    J Neurophysiol. 1994 Jan;71(1):280-93 PMID: 7908955
  5. Control of thalamocortical afferent rearrangement by postsynaptic activity in developing visual cortex.
    Science. 1994 Sep 16;265(5179):1732-5 PMID: 8085163
  6. Developmental down-regulation of LTD in cortical layer IV and its independence of modulation by inhibition.
    Neuron. 1996 Jun;16(6):1097-106 PMID: 8663986
  7. The GABA-ergic system: a locus of benzodiazepine action.
    Annu Rev Neurosci. 1985;8:21-44 PMID: 2858999
  8. Mechanisms of visual plasticity: Hebb synapses, NMDA receptors, and beyond.
    Physiol Rev. 1991 Apr;71(2):587-615 PMID: 1826058
  9. Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase.
    Proc Natl Acad Sci U S A. 1997 Jun 10;94(12):6496-9 PMID: 9177246
  10. Evidence for an enhanced role of GABA inhibition in visual cortical ocular dominance of cats reared with abnormal monocular experience.
    Brain Res Dev Brain Res. 1989 Feb 1;45(2):211-8 PMID: 2713980
  11. Neurotrophins and activity-dependent development of the neocortex.
    Curr Opin Neurobiol. 1996 Feb;6(1):119-26 PMID: 8794047
  12. Differences between somatic and dendritic inhibition in the hippocampus.
    Neuron. 1996 Apr;16(4):815-23 PMID: 8607999
  13. Penicillin-induced epileptiform activity does not prevent ocular dominance shifts in monocularly deprived kittens.
    Brain Res. 1986 Apr 16;371(1):1-8 PMID: 3708337
  14. Neurotrophin regulation of cortical dendritic growth requires activity.
    Neuron. 1996 Dec;17(6):1057-64 PMID: 8982155
  15. Different distributions of GAD65 and GAD67 mRNAs suggest that the two glutamate decarboxylases play distinctive functional roles.
    J Neurosci Res. 1993 Apr 15;34(6):689-706 PMID: 8315667
  16. Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat.
    J Neurosci. 1998 Jun 1;18(11):4255-70 PMID: 9592103
  17. Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region.
    Eur J Neurosci. 1993 Dec 1;5(12):1729-51 PMID: 8124523
  18. Biopharmacological data and high-performance liquid chromatographic analysis of 1,4-benzodiazepines in biological fluids: a review.
    J Pharm Biomed Anal. 1992 Feb-Mar;10(2-3):109-36 PMID: 1356446
  19. Interplay between glutamate and gamma-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10037-41 PMID: 1658793
  20. Differences in inhibitory synaptic input between layer II-III and layer V neurons of the cat neocortex.
    J Neurophysiol. 1995 Sep;74(3):1149-66 PMID: 7500140
  21. From GABAA receptor diversity emerges a unified vision of GABAergic inhibition.
    Annu Rev Pharmacol Toxicol. 1998;38:321-50 PMID: 9597158
  22. Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase.
    Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):14060-5 PMID: 9391152
  23. Hippocampal GABA(A) channel conductance increased by diazepam.
    Nature. 1997 Jul 3;388(6637):71-5 PMID: 9214504
  24. GABAA receptor-mediated currents in interneurons and pyramidal cells of rat visual cortex.
    J Physiol. 1998 Feb 1;506 ( Pt 3):715-30 PMID: 9503333
  25. Receptor subtypes involved in callosally-induced postsynaptic potentials in rat frontal agranular cortex in vitro.
    Exp Brain Res. 1992;88(1):33-40 PMID: 1347272
  26. GABA and pancreatic beta-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion.
    EMBO J. 1991 May;10(5):1275-84 PMID: 2022191
  27. Ocular dominance plasticity under metabotropic glutamate receptor blockade.
    Science. 1996 Apr 26;272(5261):554-7 PMID: 8614806
  28. GABAergic axon terminals at perisomatic and dendritic inhibitory sites show different immunoreactivities against two GAD isoforms, GAD67 and GAD65, in the mouse hippocampus: a digitized quantitative analysis.
    J Comp Neurol. 1998 Jun 1;395(2):177-94 PMID: 9603371
  29. Neurotrophins and neuronal plasticity.
    Science. 1995 Oct 27;270(5236):593-8 PMID: 7570017
  30. A subset of local interneurons generate slow inhibitory postsynaptic potentials in hippocampal neurons.
    Brain Res. 1990 Mar 12;511(1):163-4 PMID: 2158854
  31. Selective cholinergic modulation of cortical GABAergic cell subtypes.
    J Neurophysiol. 1997 Sep;78(3):1743-7 PMID: 9310461
  32. Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation.
    J Physiol. 1978 Aug;281:267-83 PMID: 702379
  33. Synaptic activity and the construction of cortical circuits.
    Science. 1996 Nov 15;274(5290):1133-8 PMID: 8895456
  34. GABAA receptor channels.
    Annu Rev Neurosci. 1994;17:569-602 PMID: 7516126
  35. Neocortical long-term potentiation.
    Curr Opin Neurobiol. 1993 Apr;3(2):197-202 PMID: 8513232
  36. Regulatory properties of brain glutamate decarboxylase (GAD): the apoenzyme of GAD is present principally as the smaller of two molecular forms of GAD in brain.
    J Neurosci. 1991 Sep;11(9):2725-31 PMID: 1880546
  37. Tonic inhibition originates from synapses close to the soma.
    Neuron. 1995 Jun;14(6):1273-83 PMID: 7605636
  38. GABAergic cell subtypes and their synaptic connections in rat frontal cortex.
    Cereb Cortex. 1997 Sep;7(6):476-86 PMID: 9276173
  39. Long-term potentiation and long-term depression in the neocortex.
    Prog Neurobiol. 1992 Aug;39(2):209-28 PMID: 1323860
  40. Nerve growth factor and brain-derived neurotrophic factor increase neurotransmitter release in the rat visual cortex.
    Eur J Neurosci. 1998 Jun;10(6):2185-91 PMID: 9753104
  41. Long-term potentiation and NMDA receptors in rat visual cortex.
    Nature. 1987 Dec 17-23;330(6149):649-52 PMID: 2446147
  42. Rapid restoration of functional input to the visual cortex of the cat after brief monocular deprivation.
    J Physiol. 1982 Jun;327:463-87 PMID: 7120147
  43. Two forms of the gamma-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions.
    J Neurochem. 1991 Feb;56(2):720-3 PMID: 1988566
  44. Diazepam and (--)-pentobarbital: fluctuation analysis reveals different mechanisms for potentiation of gamma-aminobutyric acid responses in cultured central neurons.
    Proc Natl Acad Sci U S A. 1981 Nov;78(11):7180-4 PMID: 6273918
  45. Constitutive expression of zif268 in neocortex is regulated by synaptic activity.
    Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5106-10 PMID: 1828891
  46. Neural plasticity without postsynaptic action potentials: less-active inputs become dominant when kitten visual cortical cells are pharmacologically inhibited.
    Proc Natl Acad Sci U S A. 1988 May;85(10):3623-7 PMID: 3285347
  47. Synaptic inputs to GABAA and GABAB receptors originate from discrete afferent neurons.
    Neurosci Lett. 1992 Jan 6;134(2):207-11 PMID: 1350333
  48. Synaptic economics: competition and cooperation in synaptic plasticity.
    Neuron. 1996 Sep;17(3):371-4 PMID: 8816700
  49. Postcritical-period reversal of effects of monocular deprivation on striate cortex cells in the cat.
    J Neurophysiol. 1976 May;39(3):501-11 PMID: 948005
  50. Progressive changes in kitten striate cortex during monocular vision.
    J Neurophysiol. 1975 Jan;38(1):26-32 PMID: 162944
  51. Three distinct families of GABAergic neurons in rat visual cortex.
    Cereb Cortex. 1997 Jun;7(4):347-58 PMID: 9177765
  52. Enhancement of mRNA expression of tissue-type plasminogen activator by L-threo-3,4-dihydroxyphenylserine in association with ocular dominance plasticity.
    Neurosci Lett. 1996 Nov 8;218(3):149-52 PMID: 8945750
  53. Experience-dependent modification of synaptic plasticity in visual cortex.
    Nature. 1996 Jun 6;381(6582):526-8 PMID: 8632826
  54. Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules.
    Cereb Cortex. 1993 Jul-Aug;3(4):273-89 PMID: 8104567
  55. Regulation of calcium-binding protein immunoreactivity in GABA neurons of macaque primary visual cortex.
    Cereb Cortex. 1996 Mar-Apr;6(2):271-87 PMID: 8670656
  56. Comparison of plasticity in vivo and in vitro in the developing visual cortex of normal and protein kinase A RIbeta-deficient mice.
    J Neurosci. 1998 Mar 15;18(6):2108-17 PMID: 9482797
  57. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse.
    J Neurosci. 1996 May 15;16(10):3274-86 PMID: 8627365
  58. Cleft palate in mice with a targeted mutation in the gamma-aminobutyric acid-producing enzyme glutamic acid decarboxylase 67.
    Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11451-5 PMID: 9326630
  59. Bicuculline reversal of deprivation amblyopia in the cat.
    Nature. 1976 Mar 18;260(5548):256-7 PMID: 1256565
  60. Expression of two forms of glutamic acid decarboxylase (GAD67 and GAD65) during postnatal development of the cat visual cortex.
    Brain Res Dev Brain Res. 1997 Nov 12;103(2):127-41 PMID: 9427477
  61. Mice lacking the 65 kDa isoform of glutamic acid decarboxylase (GAD65) maintain normal levels of GAD67 and GABA in their brains but are susceptible to seizures.
    Biochem Biophys Res Commun. 1996 Dec 24;229(3):891-5 PMID: 8954991
  62. The role of GABAergic inhibition in the cortical effects of monocular deprivation.
    Nature. 1981 May 28;291(5813):318-20 PMID: 7231550
  63. Noradrenergic excitation and inhibition of GABAergic cell types in rat frontal cortex.
    J Neurosci. 1998 Sep 1;18(17):6963-76 PMID: 9712665
  64. SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE.
    J Neurophysiol. 1963 Nov;26:1003-17 PMID: 14084161
  65. Rapid remodeling of axonal arbors in the visual cortex.
    Science. 1993 Jun 18;260(5115):1819-21 PMID: 8511592
  66. Postnatal maturation of the GABAergic system in rat neocortex.
    J Neurophysiol. 1991 Feb;65(2):247-63 PMID: 1673153
  67. Impulse activity and the patterning of connections during CNS development.
    Neuron. 1990 Dec;5(6):745-56 PMID: 2148486
  68. BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses.
    Neuron. 1998 Sep;21(3):521-30 PMID: 9768839
  69. Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites.
    Nature. 1994 Apr 28;368(6474):823-8 PMID: 8159242
  70. Two genes encode distinct glutamate decarboxylases.
    Neuron. 1991 Jul;7(1):91-100 PMID: 2069816
  71. Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex.
    J Physiol. 1997 May 1;500 ( Pt 3):715-38 PMID: 9161987
  72. Blockade of intracortical inhibition in kitten striate cortex: effects on receptive field properties and associated loss of ocular dominance plasticity.
    Exp Brain Res. 1988;73(2):285-96 PMID: 3215305
  73. Benzodiazepine and beta-carboline regulation of single GABAA receptor channels of mouse spinal neurones in culture.
    J Physiol. 1994 Feb 15;475(1):69-82 PMID: 7514665
  74. Transient increase in expression of a glutamate decarboxylase (GAD) mRNA during the postnatal development of the rat striatum.
    Dev Biol. 1992 Sep;153(1):158-64 PMID: 1516745
  75. Separate activation of fast and slow inhibitory postsynaptic potentials in rat neocortex in vitro.
    J Physiol. 1994 Apr 15;476(2):203-15 PMID: 7913968
  76. Cholinergic switching within neocortical inhibitory networks.
    Science. 1998 Aug 14;281(5379):985-8 PMID: 9703513
  77. Development and plasticity of cortical processing architectures.
    Science. 1995 Nov 3;270(5237):758-64 PMID: 7481762
  78. Sensory regulation of immediate-early gene expression in mammalian visual cortex: implications for functional mapping and neural plasticity.
    Brain Res Brain Res Rev. 1997 Apr;23(3):237-56 PMID: 9164673
Article Info
Journal
Science (New York, N.Y.)
Abbr.
Science
ISSN
0036-8075
Published
1998-11-20
Pages
1504-8
Language
English
Region
United States
NLM ID
0404511
PMCID
PMC2851625
Subset
IM
Grants
NEI NIH HHS · R37 EY002874 · United States
NEI NIH HHS · R37 EY002874-20 · United States
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