Two forms of synaptic plasticity with distinct dependence on age, experience, and NMDA receptor subtype in rat visual cortex

Journal of Neuroscience

Volumn 23, Issue 16, 2003, Pages 6557-6566

  Yoshimura, Yumiko ^a   Ohmura, Tomohisa ^b   Komatsu, Yukio ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Development; Long term depression; Long term potentiation; NMDA receptor; NR2 subunit; Synaptic plasticity; Visual cortex

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID NR2 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID NR2A RECEPTOR; N METHYL DEXTRO ASPARTIC ACID NR2B RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBTYPE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; EXCITATORY POSTSYNAPTIC POTENTIAL; EXPERIENCE; INHIBITORY POSTSYNAPTIC POTENTIAL; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RECEPTOR INTRINSIC ACTIVITY; VISUAL CORTEX;

EID: 0042343809     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-16-06557.2003     Document Type: Article

References (66)

1. Artola A, Singer W (1987) Long-term potentiation and NMDA receptors in rat visual cortex. Nature 330:649-652.
2. Barth AL, Malenka RC (2001) NMDAR EPSC kinetics do not regulate the critical period for LTP at thalamocortical synapses. Nat Neurosci 4:235-236.
3. Bear MF, Press WA, Connors BW (1992) Long-term potentiation in slices of kitten visual cortex and the effects of NMDA receptor blockade. J Neurophysiol 67:841-851.
4. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
5. Buller AL, Monaghan DT (1997) Pharmacological heterogeneity of NMDA receptors: characterization of NR1a/NR2D heteromers expressed in Xenopus oocytes. Eur J Pharmacol 320:87-94.
6. Caillard O, Ben-Ari Y, Gaïarsa J-L (1999) Mechanism of induction and expression of long-term depression at GABAergic synapses in the neonatal rat hippocampus. J Neurosci 19:7568-7577.
7. Carmignoto G, Vicini S (1992) Activity- dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258:1007-1011.
8. Castro-Alamancos MA, Connors BW (1997) Distinct forms of short-term plasticity at excitatory synapses of hippocampus and neocortex. Proc Natl Acad Sci USA 94:4161-4166.
9. Chenard BL, Menniti FS (1999) Antagonists selective for NMDA receptors containing NR2B subunit. Curr Pharm Des 5:381-404.
10. Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13:99-104.
11. Crair MC, Malenka RC (1995) A critical period for long-term potentiation at thalamocortical synapses. Nature 375:325-328.
12. Cull-Candy S, Brickley S, Ferrant M (2001) NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11:327-335.
13. Cynader M, Mitchell DE (1980) Prolonged sensitivity to monocular deprivation in dark-reared cats. J Neurophysiol 43:1026-1040.
14. Fagiolini M, Pizzorusso T, Berardi N, Domenici L, Maffei L (1994) Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res 34:709-720.
15. Feldman DE (2000) Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27:45-56.
16. Fischer G, Mutel V, Trube G, Malherbe P, Kew JNC, Mohacsi E, Heitz MP, Kemp JA (1997) Ro 25-6981, a highly potent and selective blocker of N-methyl-D-aspartate receptors containing the NR2B subunit. Characterization in vitro. J Pharmacol Exp Ther 283:1285-1292.
17. Flint AC, Maisch US, Weishaupt JH, Kriegstein AR, Monyer H (1997) NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J Neurosci 17:2469-2476.
18. Fox K, Daw NW (1993) Do NMDA receptors have a critical function in visual cortical plasticity? Trends Neurosci 16:116-122.
19. Frégnac Y, Imbert M (1984) Development of neuronal selectivity in primary visual cortex of cat. Physiol Rev 64:325-434.
20. Gilbert CD (1998) Adult cortical dynamics. Physiol Rev 78:467-485.
21. Gordon JA, Cioffi D, Silva AJ, Stryker MP (1996) Deficient plasticity in the primary visual cortex of α-calcium/calmodulin-dependent protein kinase II mutant mice. Neuron 17:491-499.
22. Hensch TK, Fagiolini M, Mataga N, Stryker MP, Baekkeskov S, Kash SF (1998a) Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282:1504-1508.
23. Hensch TK, Gordon JA, Brandon EP, McKnight GS, Idzerda RL, Stryker MP (1998b) Comparison of plasticity in vivo and in vitro in the developing visual cortex of normal and protein kinase A RIβ-deficient mice. J Neurosci 18:2108-2117.
24. Hestrin S (1992) Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature 357:686-689.
25. Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, Maffei L, Tonegawa S (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98:739-755.
26. Husi H, Ward MA, Choudhary JS, Blackstock WP, Grant SGN (2000) Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci 3:661-669.
27. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
28. Kimura F, Nishigori A, Shirokawa T, Tsumoto T (1989) Long-term potentiation and N-methyl-D-aspartate receptors in the visual cortex of young rats. J Physiol (Lond) 414:125-144.
29. Kirkwood A, Bear MF (1994) Hebbian synapses in visual cortex. J Neurosci 14:1634-1645.
30. Kirkwood A, Lee H-K, Bear MF (1995) Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience. Nature 375:328-331.
31. Kirkwood A, Silva A, Bear MF (1997) Age-dependent decrease of synaptic plasticity in the neocortex of αCaMKII mutant mice. Proc Natl Acad Sci USA 94:3380-3383.
32. Komatsu Y (1994) Age-dependent long-term potentiation of inhibitory synaptic transmission in rat visual cortex. J Neurosci 4:6488-6499.
33. Komatsu Y, Iwakiri M (1993) Long-term modification of inhibitory synaptic transmission in developing visual cortex. NeuroReport 4:907-910.
34. Komatsu Y, Nakajima S, Toyama K (1991) Induction of long-term potentiation without participation of N-methyl-D-aspartate receptors in kitten visual cortex. J Neurophysiol 65:20-32.
35. Llano I, Leresche N, Marty A (1991) Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron 6:565-574.
36. Lu H-C, Gonzalez E, Crair MC (2001) Barrel cortex critical period plasticity is independent of changes in NMDA receptor subunit composition. Neuron 32:619-634.
37. Lu YM, Mansuy IM, Kandel ER, Roder J (2000) Calcineurin-mediated LTD of GABAergic inhibition underlies the increased excitability of CA1 neurons associated with LTP. Neuron 26:197-205.
38. Luo J, Wang Y, Yasuda RP, Dunah AW, Wolfe BB (1997) The majority of N-methyl-D-aspartate receptor complexes in adult rat cerebral cortex contain at least three different subunits (Nr1/NR2A/NR2B). Mol Pharmacol 51:79-86.
39. Maejima T, Ohno-Shosaku T, Kano M (2001) Endogenous cannabinoid as a retrograde messenger from depolarized postsynaptic neurons to presynaptic terminals. Neurosci Res 40:205-210.
40. Malenka RC, Nicoll RA (1999) Long-term potentiation: A decade of progress? Science 285:1870-1874.
41. Mason A, Larkman A (1990) Correlation between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology. J Neurosci 10:1415-1428.
42. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
43. Mori H, Mishina M (1995) Structure and function of the NMDA receptor channel. Neuropharmacology 34:1219-1237.
44. 3H]Ro 25-6981, a potent and selective antagonist of NMDA receptors containing NR2B subunits. J Neurochem 70:2147-2155.
45. Nase G, Weishaupt J, Stern P, Singer W, Monyer H (1999) Genetic and epigenetic regulation of NMDA receptor expression in the rat visual cortex. Eur J Neurosci 11:4320-4326.
46. Philpot BD, Sekhar AK, Shouval HZ, Bear MF (2001) Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex. Neuron 29:157-169.
47. A responses in hippocampal pyramidal cells. J Neurosci 12:4122-4132.
48. Quinlan EM, Philpot BD, Huganir RL, Bear MF (1999) Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat Neurosci 2:352-357.
49. Regehr WG, Tank DW (1994) Dendritic calcium dynamics. Curr Opin Neurobiol 4:373-382.
50. Roberts EB, Ramoa AS (1999) Enhanced NR2A subunit expression and decreased NMDA receptor decay time at the onset of ocular dominance plasticity in the ferret. J Neurophysiol 81:2587-2591.
51. Seeburg PH (1993) The molecular biology of mammalian glutamate receptor channels. Trends Neurosci 16:359-365.
52. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY (1994) Changing sub-unit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368:144-147.
53. Shi J, Townsend M, Constantine-Paton M (2000) Activity-dependent induction of tonic calcineurin activity mediates a rapid developmental downregulation of NMDA receptor currents. Neuron 28:103-114.
54. Singer W (1995) Development and plasticity of cortical processing architectures. Science 270:758-764.
55. Sprengel R, Suchanek B, Amico C, Brusa R, Burnashev N, Rozov A, Hvalby O, Jensen V, Paulsen O, Andersen P, Kim JJ, Thompson RF, Sun W, Webster LC, Grant SGN, Eilers J, Konnerth A, Li J, McNamara JO, Seeburg PH (1998) Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo. Cell 92:279-289.
56. Stelzer A, Slater NT, Bruggencate GT (1987) Activation of NMDA receptors blocks GABAergic inhibition in an in vitro model of epilepsy. Nature 326:698-701.
57. Sun XJ, Tolbert LP, Hildebrand JG, Meinertzhagen IA (1998) A rapid method for combined laser scanning confocal microscopic and electron microscopic visualization of biocytin or neurobiotin-labeled neurons. J Histochem Cytochem 46:263-273.
58. Thomson AM, Deuchars J (1994) Temporal and spatial properties of local circuits in neocortex. Trends Neurosci 17:119-126.
59. Tovar KR, Westbrook GL (1999) The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 19:4180-4188.
60. Trachtenberg JT, Trepel C, Stryker MP (2000) Rapid extragranular plasticity in the absence of thalamocortical plasticity in the developing primary visual cortex. Science 287:2029-2032.
61. Vicini S, Wang JF, Li JH, Zhu WJ, Wang YH, Luo JH, Wolfe BB, Grayson DR (1998) Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J Neurophysiol 79:555-566.
62. Watanabe M, Inoue Y, Sakimura K, Mishina M (1992) Developmental changes in distribution of NMDA receptor subunit mRNAs. NeuroReport 3:1138-1140.
63. Wiesel TN (1982) Postnatal development of the visual cortex and the influence of environment. Nature 299:583-592.
64. Williams K, Russell SL, Shen YM, Molinoff PB (1993) Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro. Neuron 10:267-278.
65. Yoshimura Y, Tsumoto T (1994) Dependence of LTP induction on postsynaptic depolarization: a perforated patch-clamp study in visual cortical slices of young rats. J Neurophysiol 71:1638-1645.
66. Yoshimura Y, Sato H, Imamura K, Watanabe Y (2000) Properties of horizontal and vertical inputs to pyramidal cells in the superficial layers of the cat visual cortex. J Neurosci 20:1931-1940.