Modular competition driven by NMDA receptor subtypes in spike-timing-dependent plasticity

Journal of Neurophysiology

Volumn 97, Issue 4, 2007, Pages 2851-2862

  Gerkin, Richard C ^a   Lau, Pak Ming ^b   Nauen, David W ^a   Yu, Tian Wang ^c   Bi, Guo Qiang ^a,b  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CANNABINOID 1 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DISSOCIATION; HIPPOCAMPUS; NERVE CELL PLASTICITY; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPIKE WAVE;

ALGORITHMS; ANIMALS; BINDING, COMPETITIVE; CELLS, CULTURED; EXCITATORY AMINO ACID ANTAGONISTS; LINEAR MODELS; MODELS, NEUROLOGICAL; MODELS, STATISTICAL; NEURONAL PLASTICITY; QUINOXALINES; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY;

EID: 34147149549     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00860.2006     Document Type: Article

References (72)

1. Abbott LF, Nelson SB. Synaptic plasticity: taming the beast. Nat Neurosci Suppl 3: 1178-1183, 2000.
2. Artola A, Singer W. Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci 16: 480-487, 1993.
3. Bagal AA, Kao JP, Tang CM, Thompson SM. Long-term potentiation of exogenous glutamate responses at single dendritic spines. Proc Natl Acad Sci USA 102: 14434-14439, 2005.
4. Barria A, Malinow R. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48: 289-301, 2005.
5. Bayer KU, De Koninck P, Leonard AS, Hell JW, Schulman H. Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 411: 801-805, 2001.
6. Bender VA, Bender KJ, Brasier DJ, Feldman DE. Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J Neurosci 26: 4166-4177, 2006.
7. Berberich S, Punnakkal P, Jensen V, Pawlak V, Seeburg PH, Hvalby O, Kohr G. Lack of NMDA receptor subtype selectivity for hippocampal long-term potentiation. J Neurosci 25: 6907-6910, 2005.
8. Bi GQ, Poo MM. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18: 10464-10472, 1998.
9. Bi GQ, Poo MM. Synaptic modification by correlated activity: Hebb's postulate revisited. Annu Rev Neurosci 24: 139-166, 2001.
10. Bi GQ, Rubin JE. Timing in synaptic plasticity: from detection to integration. Trends Neurosci 28: 222-228, 2005.
11. Blackstone C, Sheng M. Postsynaptic calcium signaling microdomains in neurons. Front Biosci 7: d872-d885, 2002.
12. Bliss T, Schoepfer R. Neuroscience. Controlling the ups and downs of synaptic strength. Science 304: 973-974, 2004.
13. Bliss TV, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39, 1993.
14. 2+/calmodulin-dependent protein kinase II-protein phosphatase 1 switch facilitates specificity in postsynaptic calcium signaling. Proc Natl Acad Sci USA 100: 10512-10517, 2003.
15. Brimecombe JC, Boeckman FA, Aizenman E. Functional consequences of NR2 subunit composition in single recombinant N-methyl-D-aspartate receptors. Proc Natl Acad Sci USA 94: 11019-11024, 1997.
16. Cai Y, Gavornik JP, Cooper LN, Yeung LC, Shouval HZ. Effect of stochastic synaptic and dendritic dynamics on synaptic plasticity in visual cortex and hippocampus. J Neurophysiol 97: 375-386, 2006.
17. Chen N, Luo T, Raymond LA. Subtype-dependence of NMDA receptor channel open probability. J Neurosci 19: 6844-6854, 1999.
18. Clarke R, Johnson J. Voltage-dependent gating of NMDA receptors in the presence and absence of magnesium. SFN Annual Meeting 721.726, 2005.
19. Constantine-Paton M, Cline HT, Debski E. Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annu Rev Neurosci 13: 129-154, 1990.
20. Cull-Candy S, Brickley S, Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11: 327-335, 2001.
21. Dan Y, Poo MM. Spike timing-dependent plasticity of neural circuits. Neuron 44: 23-30, 2004.
22. Duguid I, Sjostrom PJ. Novel presynaptic mechanisms for coincidence detection in synaptic plasticity. Curr Opin Neurobiol 16: 312-322, 2006.
23. Erreger K, Dravid SM, Banke TG, Wyllie DJ, Traynelis SF. Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signalling profiles. J Physiol 563: 345-358, 2005.
24. Faber DS, Korn H. Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys J 60: 1288-1294, 1991.
25. Feng B, Tse HW, Skifter DA, Morley R, Jane DE, Monaghan DT. Structure-activity analysis of a novel NR2C/NR2D-preferring NMDA receptor antagonist: 1-(phenanthrene-2-carbonyl) piperazine-2,3-dicarboxylic acid. Br J Pharmacol 141: 508-516, 2004.
26. Fischer G, Mutel V, Trube G, Malherbe P, Kew JN, Mohacsi E, Heitz MP, Kemp JA. 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, 1997.
27. Froemke RC, Dan Y. Spike-timing-dependent synaptic modification induced by natural spike trains. Nature 416: 433-438, 2002.
28. Hajos N, Ledent C, Freund TF. Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience 106: 1-4, 2001.
29. Hatton CJ, Paoletti P. Modulation of triheteromeric NMDA receptors by N-terminal domain ligands. Neuron 46: 261-274, 2005.
30. Hebb DO. The Organization of Behavior. New York: Wiley, 1949.
31. Hoffman AF, Macgill AM, Smith D, Oz M, Lupica CR. Species and strain differences in the expression of a novel glutamate-modulating cannabinoid receptor in the rodent hippocampus. Eur J Neurosci 22: 2387-2391, 2005.
32. Janssens N, Lesage AS. Glutamate receptor subunit expression in primary neuronal and secondary glial cultures. J Neurochem 77: 1457-1474, 2001.
33. 2+ unblock of NMDA receptors: implications for spike-timing dependent synaptic plasticity. J Physiol 556: 337-345, 2004.
34. Kennedy MB, Beale HC, Carlisle HJ, Washburn LR. Integration of biochemical signalling in spines. Nat Rev Neurosci 6: 423-434, 2005.
35. Kew JN, Richards JG, Mutel V, Kemp JA. Developmental changes in NMDA receptor glycine affinity and ifenprodil sensitivity reveal three distinct populations of NMDA receptors in individual rat cortical neurons. J Neurosci 18: 1935-1943, 1998.
36. Kim MJ, Dunah AW, Wang YT, Sheng M. Differential roles of NR2A- and NR2B-containing NMDA receptors in Ras-ERK signaling and AMPA receptor trafficking. Neuron 46: 745-760, 2005.
37. 2+ block in NMDA receptor channels. J Neurosci 16: 3549-3558, 1996.
38. Kutsuwada T, Kashiwabuchi N, Mori H, Sakimura K, Kushiya E, Araki K, Meguro H, Masaki H, Kumanishi T, Arakawa M, Mishina M. Molecular diversity of the NMDA receptor channel. Nature 358: 36-41, 1992.
39. Lester RA, Quarum ML, Parker JD, Weber E, Jahr CE. Interaction of 6-cyano-7-nitroquinoxaline-2,3-dione with the N-methyl-D- aspartate receptor-associated glycine binding site. Mol Pharmacol 35: 565-570, 1989.
40. Li S, Tian X, Hartley D, Feig L. Distinct roles for Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) and Ras-GRF2 in the induction of long-term potentiation and long-term depression. J Neurosci 26: 1721-1729, 2006.
41. Lisman J. A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc Natl Acad Sci USA 86: 9574-9578, 1989.
42. Lisman J, Schulman H, Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3: 175-190, 2002.
43. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, Auberson YP, Wang YT. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304: 1021-1024, 2004.
44. Malenka RC, Nicoll RA. Long-term potentiation - a decade of progress. Science 285: 1870-1874, 1999.
45. Mallon AP, Auberson YP, Stone TW. Selective subunit antagonists suggest an inhibitory relationship between NR2B and NR2A-subunit containing N-methyl-D-aspartate receptors in hippocampal slices. Exp Brain Res 162: 374-383, 2005.
46. Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, Molnar E, Collingridge GL, Bashir ZI. Differential roles of NR2A- and NR2B-containing NMDA receptors in cortical long-term potentiation and longterm depression. J Neurosci 24: 7821-7828, 2004.
47. Miyashiro K, Dichter M, Eberwine J. On the nature and differential distribution of mRNAs in hippocampal neurites: implications for neuronal functioning. Proc Natl Acad Sci USA 91: 10800-10804, 1994.
48. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12: 529-540, 1994.
49. Morishita W, Lu W, Smith GB, Nicoll RA, Bear MF, Malenka RC. Activation of NR2B-containing NMDA receptors is not required for NMDA receptor-dependent long-term depression. Neuropharmacology 52: 71-76, 2007.
50. 2+ signals evoked by coincident EPSPs and backpropagating action potentials in spiny stellate cells of layer 4 in the juvenile rat somatosensory barrel cortex. J Neurosci 24: 1689-1699, 2004.
51. 2+ signaling in spike-timing-dependent plasticity. J Neurosci 26: 11001-11013, 2006.
52. Neyton J, Paoletti P. Relating NMDA receptor function to receptor subunit composition: limitations of the pharmacological approach. J Neurosci 26: 1331-1333, 2006.
53. 2+ channels. J Gen Physiol 108: 143-155, 1996.
54. Okada M, Corfas G. Neuregulin1 downregulates postsynaptic GABAA receptors at the hippocampal inhibitory synapse. Hippocampus 14: 337-344, 2004.
55. Palmer MJ, Isaac JT, Collingridge GL. Multiple, developmentally regulated expression mechanisms of long-term potentiation at CA1 synapses. J Neurosci 24: 4903-4911, 2004.
56. Rubin JE, Gerkin RC, Bi GQ, Chow CC. Calcium time course as a signal for spike-timing-dependent plasticity. J Neurophysiol 93: 2600-2613, 2005.
57. Shouval HZ, Bear MF, Cooper LN. A unified model of NMDA receptor-dependent bidirectional synaptic plasticity. Proc Natl Acad Sci USA 99: 10831-10836, 2002.
58. Shouval HZ, Kalantzis G. Stochastic properties of synaptic transmission affect the shape of spike time-dependent plasticity curves. J Neurophysiol 93: 1069-1073, 2005.
59. Sjostrom PJ, Nelson SB. Spike timing, calcium signals and synaptic plasticity. Curr Opin Neurobiol 12: 305-314, 2002.
60. Sjostrom PJ, Turrigiano GG, Nelson SB. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32: 1149-1164, 2001.
61. Sjostrom PJ, Turrigiano GG, Nelson SB. Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39: 641-654, 2003.
62. Stemmer PM, Klee CB. Dual calcium ion regulation of calcineurin by calmodulin and calcineurin B. Biochemistry 33: 6859-6866, 1994.
63. Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, Liu G, Tsien JZ. Genetic enhancement of learning and memory in mice. Nature 401: 63-69, 1999.
64. Tigaret CM, Thalhammer A, Rast GF, Specht CG, Auberson YP, Stewart MG, Schoepfer R. Subunit dependencies of N-methyl-D-aspartate (NMDA) receptor-induced alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor internalization. Mol Pharmacol 69: 1251-1259, 2006.
65. Vicini S, Wang JF, Li JH, Zhu WJ, Wang YH, Luo JH, Wolfe BB, Grayson DR. Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J Neurophysiol 79: 555-566, 1998.
66. Wang HX, Gerkin RC, Nauen DW, Bi GQ. Coactivation and timing-dependent integration of synaptic potentiation and depression. Nat Neurosci 8: 187-193, 2005.
67. Weitlauf C, Honse Y, Auberson YP, Mishina M, Lovinger DM, Winder DG. Activation of NR2A-containing NMDA receptors is not obligatory for NMDA receptor-dependent long-term potentiation. J Neurosci 25: 8386-8390, 2005.
68. Wilcox KS, Buchhalter J, Dichter MA. Properties of inhibitory and excitatory synapses between hippocampal neurons in very low density cultures. Synapse 18: 128-151, 1994.
69. i elevation. J Neurophysiol 81: 781-787, 1999.
70. Yang Y, Ge W, Chen Y, Zhang Z, Shen W, Wu C, Poo M, Duan S. Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine. Proc Natl Acad Sci USA 100: 15194-15199, 2003.
71. Zhao MG, Toyoda H, Lee YS, Wu LJ, Ko SW, Zhang XH, Jia Y, Shum F, Xu H, Li BM, Kaang BK, Zhuo M. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 47: 859-872, 2005.
72. 2+ transients by broadening postsynaptic action potentials enhances timing-dependent synaptic depression. Proc Natl Acad Sci USA 102: 19121-19125, 2005.