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PMID: 11805343 Published · ppublish English Journal Article

Experience-dependent plasticity without long-term depression by type 2 metabotropic glutamate receptors in developing visual cortex.

Renger JJ, Hartman KN, Tsuchimoto Y, Yokoi M, Nakanishi S, Hensch TK

Abstract

Synaptic depression is thought to underlie the loss of cortical responsiveness to an eye deprived of vision. Here, we establish a fundamental role for type 2 metabotropic glutamate receptors (mGluR2) in long-term depression (LTD) of synaptic transmission within primary visual cortex. Direct mGluR2 activation by (2S,2'R,3'R-2-(2',3'-dicarboxycyclopropyl)glycine (DCG-IV) persistently depressed layer 2/3 field potentials in slices of mouse binocular zone when stimulated concomitantly. Chemical LTD was independent of N-methyl-d-aspartate (NMDA) receptors but occluded conventional LTD by low-frequency stimulation, indicating shared downstream events. Antagonists or targeted disruption of mGluR2 conversely prevented LTD induction by electrical low-frequency stimulation to layer 4. In contrast, Schaeffer collateral synapses did not exhibit chemical LTD, revealing hippocampal area CA1, naturally devoid of mGluR2, to be an inappropriate model for neocortical plasticity. Moreover, monocular deprivation remained effective in mice lacking mGluR2, and receptor expression levels were unchanged during the critical period in wild-type mice, indicating that experience-dependent plasticity is independent of LTD induction in visual cortex. Short-term depression that was unaffected by mGluR2 deletion may better reflect circuit refinement in vivo.

MeSH Terms
Animals Immunohistochemistry In Vitro Techniques Mice Mice, Knockout Models, Neurological Neuronal Plasticity/physiology Receptors, Metabotropic Glutamate/deficiency,genetics,physiology Synaptic Transmission/physiology Visual Cortex/anatomy & histology,growth & development,physiology
Chemicals
Receptors, Metabotropic Glutamate metabotropic glutamate receptor 2
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Renger John J
Laboratory for Neuronal Circuit Development, Institute of Physical and Chemical Research (RIKEN), Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan.
Hartman Kenichi N
Tsuchimoto Yoshiko
Yokoi Mineto
Nakanishi Shigetada
Hensch Takao K
References (88)
88 references, click to expand
  1. Long-term depression at thalamocortical synapses in developing rat somatosensory cortex.
    Neuron. 1998 Aug;21(2):347-57 PMID: 9728916
  2. Local GABA circuit control of experience-dependent plasticity in developing visual cortex.
    Science. 1998 Nov 20;282(5393):1504-8 PMID: 9822384
  3. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein.
    Nature. 1998 Dec 3;396(6710):433-9 PMID: 9853749
  4. Priming of group 2 metabotropic glutamate receptors facilitates induction of long-term depression in the dentate gyrus of freely moving rats.
    Neuropharmacology. 1998 Dec;37(12):1459-64 PMID: 9886668
  5. The role of presynaptic activity in monocular deprivation: comparison of homosynaptic and heterosynaptic mechanisms.
    Proc Natl Acad Sci U S A. 1999 Feb 2;96(3):1083-7 PMID: 9927697
  6. Monocular deprivation induces homosynaptic long-term depression in visual cortex.
    Nature. 1999 Jan 28;397(6717):347-50 PMID: 9950426
  7. Activation of the extracellular signal-regulated kinase 2 by metabotropic glutamate receptors.
    Eur J Neurosci. 1999 Jun;11(6):2073-2082 PMID: 10336676
  8. Anatomical correlates of functional plasticity in mouse visual cortex.
    J Neurosci. 1999 Jun 1;19(11):4388-406 PMID: 10341241
  9. Effect of the group II metabotropic glutamate agonist, 2R,4R-APDC, varies with age, layer, and visual experience in the visual cortex.
    J Neurophysiol. 1999 Jul;82(1):86-93 PMID: 10400937
  10. Sensory experience modifies the short-term dynamics of neocortical synapses.
    Nature. 1999 Jul 22;400(6742):367-71 PMID: 10432115
  11. Common forms of synaptic plasticity in the hippocampus and neocortex in vitro.
    Science. 1993 Jun 4;260(5113):1518-21 PMID: 8502997
  12. (2s,1'R,2'R,3'R)-2-(2,3-Dicarboxycyclopropyl) glycine enhances quisqualate-stimulated inositol phospholipid hydrolysis in hippocampal slices.
    Eur J Pharmacol. 1993 May 15;245(3):297-8 PMID: 7687561
  13. Metabotropic glutamate receptors trigger postsynaptic protein synthesis.
    Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7168-71 PMID: 8102206
  14. Metabotropic glutamate receptors contribute to the induction of long-term depression in the CA1 region of the hippocampus.
    Eur J Pharmacol. 1993 Aug 3;239(1-3):265-6 PMID: 8223907
  15. Presynaptic inhibitory action of a metabotropic glutamate receptor agonist on excitatory transmission in visual cortical neurons.
    Proc Biol Sci. 1993 Sep 22;253(1338):297-303 PMID: 8234367
  16. Role of a metabotropic glutamate receptor in synaptic modulation in the accessory olfactory bulb.
    Nature. 1993 Dec 16;366(6456):687-90 PMID: 7903116
  17. Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation.
    Trends Neurosci. 1993 Nov;16(11):480-7 PMID: 7507622
  18. Postsynaptic induction and presynaptic expression of hippocampal long-term depression.
    Science. 1994 May 20;264(5162):1148-52 PMID: 7909958
  19. Homosynaptic long-term depression in the visual cortex.
    J Neurosci. 1994 May;14(5 Pt 2):3404-12 PMID: 8182481
  20. Antibodies inactivating mGluR1 metabotropic glutamate receptor block long-term depression in cultured Purkinje cells.
    Neuron. 1994 Jun;12(6):1245-55 PMID: 7912091
  21. Modulation of cyclic AMP formation by putative metabotropic receptor agonists.
    Br J Pharmacol. 1994 Jan;111(1):364-9 PMID: 8012720
  22. Molecular diversity and functions of glutamate receptors.
    Annu Rev Biophys Biomol Struct. 1994;23:319-48 PMID: 7919785
  23. Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1.
    Nature. 1994 Nov 17;372(6503):237-43 PMID: 7969468
  24. Induction of LTD but not LTP through metabotropic glutamate receptors in visual cortex.
    Neuroreport. 1994 Sep 8;5(14):1829-32 PMID: 7827342
  25. A new form of long-term depression in the perirhinal cortex.
    Nat Neurosci. 2000 Feb;3(2):150-6 PMID: 10649570
  26. Complex interactions between mGluRs, intracellular Ca2+ stores and ion channels in neurons.
    Trends Neurosci. 2000 Feb;23(2):80-8 PMID: 10652549
  27. Inhibitory threshold for critical-period activation in primary visual cortex.
    Nature. 2000 Mar 9;404(6774):183-6 PMID: 10724170
  28. Modulation of synaptic transmission in the rat ventral septal area by the pharmacological activation of metabotropic glutamate receptors.
    Eur J Neurosci. 2000 May;12(5):1843-7 PMID: 10792461
  29. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression.
    Science. 2000 May 19;288(5469):1254-7 PMID: 10818003
  30. Hebb and homeostasis in neuronal plasticity.
    Curr Opin Neurobiol. 2000 Jun;10(3):358-64 PMID: 10851171
  31. Proteomic analysis of NMDA receptor-adhesion protein signaling complexes.
    Nat Neurosci. 2000 Jul;3(7):661-9 PMID: 10862698
  32. Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity.
    Nature. 2000 Jun 22;405(6789):955-9 PMID: 10879537
  33. Developmental and sensory-dependent changes of group II metabotropic glutamate receptors.
    J Comp Neurol. 2001 Jan 8;429(2):270-6 PMID: 11116219
  34. Calcium stores regulate the polarity and input specificity of synaptic modification.
    Nature. 2000 Nov 30;408(6812):584-8 PMID: 11117745
  35. Requirement of ERK activation for visual cortical plasticity.
    Science. 2001 Jun 22;292(5525):2337-40 PMID: 11423664
  36. D-cycloserine: a ligand for the N-methyl-D-aspartate coupled glycine receptor has partial agonist characteristics.
    Neurosci Lett. 1989 Mar 13;98(1):91-5 PMID: 2540460
  37. Visual responses in adult cat visual cortex depend on N-methyl-D-aspartate receptors.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):5183-7 PMID: 2567996
  38. A biochemical correlate of the critical period for synaptic modification in the visual cortex.
    Science. 1989 Nov 3;246(4930):673-5 PMID: 2573152
  39. Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist.
    J Neurosci. 1990 Mar;10(3):909-25 PMID: 1969466
  40. Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex.
    Nature. 1990 Sep 6;347(6288):69-72 PMID: 1975639
  41. Long-term depression but not potentiation is induced in Ca(2+)-chelated visual cortex neurons.
    Neuroreport. 1990 Sep;1(1):65-8 PMID: 2129860
  42. Input-specific induction of long-term depression in Ca(2+)-chelated visual cortex neurons.
    Neuroreport. 1991 Jul;2(7):393-6 PMID: 1912472
  43. Blockade of NMDA receptors unmasks a long-term depression in synaptic efficacy in rat prefrontal neurons in vitro.
    Exp Brain Res. 1991;85(3):621-4 PMID: 1680738
  44. Dependence of long-term depression on postsynaptic metabotropic glutamate receptors in visual cortex.
    Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3650-4 PMID: 8097320
  45. Frequency detection and temporally dispersed synaptic signal association through a metabotropic glutamate receptor pathway.
    Nature. 1997 Jan 2;385(6611):74-7 PMID: 8985249
  46. Impaired learning in mice with abnormal short-lived plasticity.
    Curr Biol. 1996 Nov 1;6(11):1509-18 PMID: 8939606
  47. Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors.
    Nature. 1997 Feb 13;385(6617):630-4 PMID: 9024660
  48. Age-dependent decrease of synaptic plasticity in the neocortex of alphaCaMKII mutant mice.
    Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3380-3 PMID: 9096402
  49. DCG-IV inhibits synaptic transmission by activation of NMDA receptors in area CA1 of rat hippocampus.
    Eur J Pharmacol. 1997 Mar 19;322(2-3):173-8 PMID: 9098684
  50. mGluR II agonist inhibition of LTP induction, and mGluR II antagonist inhibition of LTD induction, in the dentate gyrus in vitro.
    Neuroreport. 1997 Feb 10;8(3):687-93 PMID: 9106748
  51. Distinct forms of short-term plasticity at excitatory synapses of hippocampus and neocortex.
    Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):4161-6 PMID: 9108122
  52. Pharmacology and functions of metabotropic glutamate receptors.
    Annu Rev Pharmacol Toxicol. 1997;37:205-37 PMID: 9131252
  53. Class I mGlu receptor antagonist 1-aminoindan-1,5-dicarboxylic acid blocks contextual but not cue conditioning in rats.
    Eur J Pharmacol. 1997 May 20;326(2-3):105-8 PMID: 9196260
  54. Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation.
    Science. 1997 Jun 27;276(5321):2042-5 PMID: 9197267
  55. Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells.
    Neuron. 1997 Jun;18(6):969-82 PMID: 9208864
  56. Heterogeneity of release probability, facilitation, and depletion at central synapses.
    Neuron. 1997 Jun;18(6):995-1008 PMID: 9208866
  57. Long-term depression requiring tACPD-receptor activation and NMDA-receptor blockade.
    Brain Res. 1994 Nov 28;665(1):158-60 PMID: 7882011
  58. 1-Aminoindan-1,5-dicarboxylic acid: a novel antagonist at phospholipase C-linked metabotropic glutamate receptors.
    J Med Chem. 1995 Sep 15;38(19):3717-9 PMID: 7562903
  59. Pharmacological characterization of MCCG and MAP4 at the mGluR1b, mGluR2 and mGluR4a human metabotropic glutamate receptor subtypes.
    Neuropharmacology. 1995 Aug;34(8):1099-102 PMID: 8532159
  60. Reexamination of the effects of MCPG on hippocampal LTP, LTD, and depotentiation.
    J Neurophysiol. 1995 Sep;74(3):1075-82 PMID: 7500133
  61. Ocular dominance plasticity under metabotropic glutamate receptor blockade.
    Science. 1996 Apr 26;272(5261):554-7 PMID: 8614806
  62. 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
  63. Characterization of metabotropic glutamate receptor-mediated facilitation of N-methyl-D-aspartate depolarization of neocortical neurones.
    Br J Pharmacol. 1996 Feb;117(4):675-83 PMID: 8646413
  64. 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
  65. Long-term depression in rat visual cortex is associated with a lower rise of postsynaptic calcium than long-term potentiation.
    Neurosci Res. 1996 Feb;24(3):265-74 PMID: 8815446
  66. The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations.
    Neuroscience. 1996 Apr;71(4):949-76 PMID: 8684625
  67. Short-term synaptic plasticity in the visual cortex during development.
    Cereb Cortex. 1996 Jul-Aug;6(4):640-6 PMID: 8670689
  68. Impairment of hippocampal mossy fiber LTD in mice lacking mGluR2.
    Science. 1996 Aug 2;273(5275):645-7 PMID: 8662555
  69. Redistribution of synaptic efficacy between neocortical pyramidal neurons.
    Nature. 1996 Aug 29;382(6594):807-10 PMID: 8752273
  70. (1 S,3 R)-1-aminocyclopentane-1,3-dicarboxylic acid-induced increases in cyclic AMP formation in the neonatal rat hippocampus are mediated by a synergistic interaction between phosphoinositide- and inhibitory cyclic AMP-coupled mGluRs.
    J Neurochem. 1996 May;66(5):1981-5 PMID: 8780026
  71. Pre- and postsynaptic localization of a metabotropic glutamate receptor, mGluR2, in the rat brain: an immunohistochemical study with a monoclonal antibody.
    Neurosci Lett. 1996 Jan 5;202(3):197-200 PMID: 8848265
  72. Calcium-induced long-term depression in the visual cortex of the rat in vitro.
    J Neurophysiol. 1996 Aug;76(2):984-94 PMID: 8871213
  73. cAMP levels increased by activation of metabotropic glutamate receptors correlate with visual plasticity.
    J Neurosci. 1996 Dec 1;16(23):7619-26 PMID: 8922418
  74. Synaptic depression and cortical gain control.
    Science. 1997 Jan 10;275(5297):220-4 PMID: 8985017
  75. Distinct functional types of associative long-term potentiation in neocortical and hippocampal pyramidal neurons.
    J Neurosci. 1999 Aug 15;19(16):6748-54 PMID: 10436032
  76. Synaptic depression induced by pharmacological activation of metabotropic glutamate receptors in the perirhinal cortex in vitro.
    Neuroscience. 1999;93(3):977-84 PMID: 10473262
  77. SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE.
    J Neurophysiol. 1963 Nov;26:1003-17 PMID: 14084161
  78. Dopamine receptors and groups I and II mGluRs cooperate for long-term depression induction in rat prefrontal cortex through converging postsynaptic activation of MAP kinases.
    J Neurosci. 1999 Nov 15;19(22):9788-802 PMID: 10559388
  79. Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex.
    Nat Neurosci. 1999 Dec;2(12):1098-105 PMID: 10570487
  80. Induction of NMDA receptor-dependent long-term depression in visual cortex does not require metabotropic glutamate receptors.
    J Neurophysiol. 1999 Dec;82(6):3594-7 PMID: 10601487
  81. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus.
    J Neurosci. 1997 Oct 1;17(19):7503-22 PMID: 9295396
  82. A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex.
    J Neurosci. 1997 Oct 15;17(20):7926-40 PMID: 9315911
  83. Differential plasma membrane distribution of metabotropic glutamate receptors mGluR1 alpha, mGluR2 and mGluR5, relative to neurotransmitter release sites.
    J Chem Neuroanat. 1997 Oct;13(4):219-41 PMID: 9412905
  84. Effects of the metabotropic glutamate receptor antagonist MCPG on phosphoinositide turnover and synaptic plasticity in visual cortex.
    J Neurosci. 1998 Jan 1;18(1):1-9 PMID: 9412480
  85. Relation between dendritic Ca2+ levels and the polarity of synaptic long-term modifications in rat visual cortex neurons.
    Eur J Neurosci. 1997 Nov;9(11):2309-22 PMID: 9464925
  86. 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
  87. Regulation of phosphoinositide turnover in neonatal rat cerebral cortex by group I- and II- selective metabotropic glutamate receptor agonists.
    Br J Pharmacol. 1998 Feb;123(3):581-9 PMID: 9504400
  88. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles.
    Nature. 1998 Jul 23;394(6691):384-8 PMID: 9690475
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2002-01-22
Pages
1041-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC117426
Subset
IM
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