A model for synaptic development regulated by NMDA receptor subunit expression

Journal of Computational Neuroscience

Volumn 24, Issue 1, 2008, Pages 1-20

  Kubota, Shigeru ^a   Kitajima, Tatsuo ^a  

^a YAMAGATA UNIVERSITY   (Japan)

Author keywords

Development; NMDA; Plasticity; STDP; Synaptic competition

Indexed keywords

SYNTHESIS (CHEMICAL);

'CURRENT; DEVELOPMENT; DEVELOPMENTAL SWITCH; NMDA; NMDA RECEPTOR; PHYSIOLOGICAL ROLES; STDP; SYNAPTIC COMPETITION; SYNAPTIC PLASTICITY; SYNAPTIC TRANSMISSION;

NEURONS;

CALCIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; LONG TERM POTENTIATION; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIMULATION; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 38549108997     PISSN: 09295313     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10827-007-0036-8     Document Type: Article

References (114)

1. Abarbanel, H. D. I., Gibb, L., Huerta, R., & Rabinovich, M. I. (2003). Biophysical model of synaptic plasticity dynamics. Biological Cybernetics, 89, 214-226.
2. Abbott, L. F., & Nelson, S. B. (2000). Synaptic plasticity: Taming the beast. Nature Neuroscience, 3 (Suppl), 1178-1183.
3. Ahmed, B., Anderson, J. C., Douglas, R. J., Martin, K. A. C., & Whitteridge, D. (1998). Estimates of the net excitatory currents evoked by visual stimulation of identified neurons in cat visual cortex. Cerebral Cortex, 8, 462-476.
4. Artola, A., & Singer, W. (1993). Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends in Neurosciences, 16, 480-487.
5. Bear M. F., Cooper L. N., & Ebner F. F. (1987). A physiological basis for a theory of synapse modification. Science, 237, 42-48.
6. Berberich, S., Punnakkal, P., Jensen, V., Pawlak, V., Seeburg, P. H., Hvalby, O., et al. (2005). Lack of NMDA receptor subtype selectivity for hippocampal long-term potentiation. Journal of Neuroscience, 25, 6907-6910.
7. Bernander, O., Douglas, R. J., Martin, K. A. C., & Koch, C. (1991). Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proceedings of the National Academy of Sciences of the United States of America, 88, 11569-11573.
8. Bhalla, U. S., & Iyengar, R. (1999). Emergent properties of networks of biological signaling pathways. Science, 283, 381-387.
9. Bi, G. Q., & Poo, M. M. (1998). Synaptic modifications in cultured hippocampal neurons: Dependence on spike timing, synaptic strength, and postsynaptic cell type. Journal of Neuroscience, 18, 10464-10472.
10. Bi, G. Q., & Rubin, J. (2005). Timing in synaptic plasticity: From detection to integration. Trends in Neurosciences, 28, 222-228.
11. Blitzer, R. D., Connor, J. H., Brown, G. P., Wong, T., Shenolikar, S., & Iyengar, R., et al. (1998). Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science, 280, 1940-1943.
12. Bush, P. C., & Sejnowski, T. J. (1993). Reduced compartmental models of neocortical pyramidal cells. Journal of Neuroscience Methods, 46, 159-166.
13. Callaway, J. C., & Ross, W. N. (1995). Frequency-dependent propagation of sodium action potentials in dendrites of hippocampal CA1 pyramidal neurons. Journal of Neurophysiology, 74, 1395-1403.
14. Carmignoto, G., & Vicini, S. (1992). Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science, 258, 1007-1011.
15. 2+ and synaptic plasticity. Cell Calcium, 38, 355-367.
16. Crair, M. C., & Malenka, R. C. (1995). A critical period for long-term potentiation at thalamocortical synapses. Nature, 375, 325-328.
17. Daw, N. W., Gordon, B., Fox, K. D., Flavin, H. J., Kirsch, J. D., Beaver, C. J., et al. (1999). Injection of MK-801 affects ocular dominance shifts more than visual activity. Journal of Neurophysiology, 81, 204-215.
18. Debanne, D., Gähwiler, B. H., & Thompson, S. M. (1998). Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. Journal of Physiology (London), 507.1, 237-247.
19. Dumas, T. C. (2005). Developmental regulation of cognitive abilities: Modified composition of a molecular switch turns on associative learning. Progress in Neurobiology, 76, 189-211.
20. Erreger, K., Dravid, S. M., Banke, T. G., Wyllie, D. J. A., & Traynelis, S. F. (2005). Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signalling profiles. Journal of Physiology (London), 563.2, 345-358.
21. 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 Research, 34, 709-720.
22. Feldman, D. E. (2000). Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron, 27, 45-56.
23. Feldman, D. E., Nicoll, R. A., Malenka, R. C., & Isaac, J. T. R. (1998). Long-term depression at thalamocortical synapses in developing rat somatosensory cortex. Neuron, 21, 347-357.
24. Flint, A. C., Maisch, U. S., Weishaupt, J. H., Kriegstein, A. R., & Monyer, H. (1997). NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. Journal of Neuroscience, 17, 2469-2476.
25. Froemke, R. C., Poo, M. M., & Dan, Y. (2005). Spike-timing-dependent synaptic plasticity depends on dendritic location. Nature, 434, 221-225.
26. Gerstner, W., & Kistler, W. M. (2002). Spiking neuron models: Single neurons, populations, plasticity. Cambridge: Cambridge University Press.
27. Goodman, C. S., & Shatz, C. J. (1993). Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72 / Neuron, 10 (Suppl.), 77-98.
28. Harris, K. M., Jansen, F. E., & Tsao, B. (1992). Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: Implications for the maturation of synaptic physiology and long-term potentiation. Journal of Neuroscience, 12, 2685-2705.
29. 2+ signaling in dendrites of pyramidal neurons. Biophysical Journal, 70, 1069-1081.
30. Hessler, N. A., Shirke, A. M., & Mallnow, R. (1993). The probability of transmitter release at a mammalian central synapse. Nature, 366, 569-572.
31. Holmes. (2000). Models of calmodulin trapping and CaM kinase II activation in a dendritic spine. Journal of Computational Neuroscience, 8, 65-85.
32. Huh, K. H., & Wenthold, R. J. (1999). Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-Methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. Journal of Biological Chemistry, 274, 151-157.
33. Iannella, N., & Tanaka, S. (2006). Synaptic efficacy cluster formation across the dendrite via STDP. Neuroscience Letters, 403, 24-29.
34. Issac, J. T. R., Crair, M. C., Nicoll, R. A., & Malenka, R. C. (1997). Silent synapses during development of thalamocortical inputs. Neuron, 18, 269-280.
35. Jahr, C. E., & Stevens, C. F. (1990a). Quantitative description of NMDA receptor-channel kinetic behavior. Journal of Neuroscience, 10, 1830-1837.
36. Jahr, C. E., & Stevens, C. F. (1990b). Voltage dependence of NMDA-activated macroscopic conductances predicted by single-channel kinetics. Journal of Neuroscience, 10, 3178-3182.
37. Kaas, J. H. (1997). Topographic maps are fundamental to sensory processing. Brain Research Bulletin, 44, 107-112.
38. Karmarkar, U. R., & Buonomano, D. V. (2002). A model of spike-timing dependent plasticity: One or two coincidence detectors? Journal of Neurophysiology, 88, 507-513.
39. Karmarkar, U. R., Najarian, M. T., & Buonomano, D. V. (2002). Mechanisms and significance of spike-timing dependent plasticity. Biological Cybernetics, 87, 373-382.
40. 2+ block of N-methyl-D-aspartate receptor-mediated synaptic potentials in developing visual cortex. Proceedings of the National Academy of Sciences of the United States of America, 90, 7114-7118.
41. Katz, L. C., & Shatz, C. J. (1996). Synaptic activity and the construction of cortical circuits. Science, 274, 1133-1138.
42. Kepecs, A., van Rossum, M. C. W., Song, S., & Tegner, J. (2002). Spike-timing-dependent plasticity: Common themes and divergent vistas. Biological Cybernetics, 87, 446-458.
43. Kirson, E. D., Schirra, C., Konnerth, A., & Yaari, Y. (1999). Early postnatal switch in magnesium sensitivity of NMDA receptors in rat CA1 pyramidal cells. Journal of Physiology (London), 521.1, 99-111.
44. Kitajima, T., & Hara, K. (2000). A generalized Hebbian rule for activity-dependent synaptic modifications. Neural Networks, 13, 445-454.
45. Koch, C. (1999). Biophysics of computation. Information processing in single neurons. New York: Oxford University Press.
46. 2+ signals in spines of hippocampal neurons. Journal of Neuroscience, 20, 1791-1799.
47. Krupp, J. J., Vissel, B., Heinemann, S. F., & Westbrook, G. L. (1996). Calcium-dependent inactivation of recombinant N-methyl-D-aspartate receptors is NR2 subunit specific. Molecular Pharmacology, 50, 1680-1688.
48. 2+ block in NMDA receptor channels. Journal of Neuroscience, 16, 3549-3558.
49. + current in rat hippocampal neurons. Journal of Physiology (London), 475.2, 229-239.
50. Lisman, J. (1989). A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proceedings of the National Academy of Sciences of the United States of America, 86, 9574-9578.
51. Lisman, J. (1994). The CaM kinase II hypothesis for the storage of synaptic memory. Trends in Neurosciences, 17, 406-412.
52. Lisman, J. E., & Zhabotinsky, A. M. (2001). A model of synaptic memory: A CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron, 31, 191-201.
53. Liu, L., Wong, T. P., Pozza, M. F., Lingenhoehl, K., Wang, Y., Sheng, M., et al. (2004). Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science, 304, 1021-1024.
54. Liu, Y. H., & Wang, X. J. (2001). Spike-frequency adaptation of a generalized leaky integrate-and-fire model neuron. Journal of Computational Neuroscience, 10, 25-45.
55. Llinas, R. R. (1988). The intrinsic electrophysiological properties of mammalian neurons: Insights into central nervous system function. Science, 242, 1654-1664.
56. Lu, H. C., Gonzalez, E., & Crair, M. C. (2001). Barrel cortex critical period plasticity is independent of changes in NMDA receptor subunit composition. Neuron, 32, 619-634.
57. Mainen, Z. F., & Sejnowski, T. J. (1996). Influence of dendritic structure on firing pattern in model neocortical neurons. Nature, 382, 363-366.
58. Markram, H., Lubke, J., Frotscher, M., & Sakmann, B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science, 275, 213-215.
59. Massey, P. V., Johnson, B. E., Moult, P. R., Auberson, Y. P., Brown, M. W., Molnar, E., et al. (2004). Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. Journal of Neuroscience, 24, 7821-7828.
60. McCormick, D. A., Connors, B. W., Lighthall, J. W., & Prince, D. A. (1985). Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. Journal of Neurophysiology, 54, 782-806.
61. McHugh, T. J., Blum, K. I., Tsien, J. Z., Tonegawa, S., & Wilson, M. A. (1996). Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell, 87, 1339-1349.
62. Micheva, K. D., & Beaulieu, C. (1996). Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry. Journal of Comparative Neurology, 373, 340-354.
63. Mierau, S. B., Meredith, R. M., Upton, A. L., & Paulsen, O. (2004). Dissociation of experience-dependent and -independent changes in excitatory synaptic transmission during development of barrel cortex. Proceedings of the National Academy of Sciences of the United States of America, 101, 15518-15523.
64. Mizuno, T., Kanazawa, I., & Sakurai, M. (2001). Differential induction of LTP and LTD is not determined solely by instantaneous calcium concentration: An essential involvement of a temporal factor. European Journal of Neuroscience, 14, 701-708.
65. Monyer, H., Burnashev, N., Laurie, D. J., Sakmann, B., & Seeburg, P. H. (1994). Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron, 12, 529-540.
66. Morishita, W., Lu, W., Smith, G. B., Nicoll, R. A., Bear, M. F., & Malenka, R. C. (2007). Activation of NR2B-containing NMDA receptors is not required for NMDA receptor-dependent long-term depression. Neuropharmacology, 52, 71-76.
67. Nishiyama, M., Hong, K., Mikoshiba, K., Poo, M. M., & Kato, K. (2000). Calcium stores regulate the polarity and input specificity of synaptic modification. Nature, 408, 584-588.
68. Philpot, B. D., Sekhar, A. K., Shouval, H. Z., & Bear, M. F. (2001). Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex. Neuron, 29, 157-169.
69. 2+-dependent regulation of guinea pig brain adenylate cyclase. Journal of Biological Chemistry, 255, 4176-4181.
70. Press, W. H., Flannery, B. P., Teukolsky, S. A., & Vetterling, W. T. (1988). Numerical recipes in C. Cambridge: Cambridge University Press.
71. Prybylowski, K., Fu, Z., Losi, G., Hawkins, L. M., Luo, J., Chang, K., et al. (2002). Relationship between availability of NMDA receptor subunits and their expression at the synapse. Journal of Neuroscience, 22, 8902-8910.
72. Puyal, J., Grassi, S., Dieni, C., Frondaroli, A., Demêmes, D., Raymond, J., et al. (2003). Developmental shift from long-term depression to long-term potentiation in the rat medial vestibular nuclei: Role of group I metabotropic glutamate receptors. Journal of Physiology (London), 553.2, 427-443.
73. Quinlan, E. M., Olstein, D. H., & Bear, M. F. (1999a). Bidirectional, experience-dependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proceedings of the National Academy of Sciences of the United States of America, 96, 12876-12880.
74. Quinlan, E. M., Philpot, B. D., Huganir, R. L., & Bear, M. F. (1999b). Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nature Neuroscience, 2, 352-357.
75. Rema, V., Armstrong-James, M., & Ebner, F. F. (1998). Experience-dependent plasticity of adult rat S1 cortex requires local NMDA receptor activation. Journal of Neuroscience, 18, 10196-10206.
76. Risken, H. (1989). The Fokker-Planck equation: Methods of solution and applications (2nd edn.). Berlin: Springer.
77. Rosenmund, C., Feltz, A., & Westbrook, G. L. (1995). Calcium-dependent inactivation of synaptic NMDA receptors in hippocampal neurons. Journal of Neurophysiology, 73, 427-430.
78. Rubin, J., Lee, D. D., & Sompolinsky, H. (2001). Equilibrium properties of temporally asymmetric Hebbian plasticity. Physical Review Letters, 86, 364-367.
79. Rubin, J. E., Gerkin, R. C., Bi, G. Q., & Chow, C. C. (2005). Calcium time course as a signal for spike-timing-dependent plasticity. Journal of Neurophysiology, 93, 2600-2613.
80. Rumsey, C. C., & Abbott, L. F. (2006). Synaptic democracy in active dendrites. Journal of Neurophysiology, 96, 2307-2318.
81. 2+ signaling in dendritic spines. Current Opinion in Neurobiology, 11, 349-356.
82. 2+ ions in dendritic spines. Neuron, 33, 439-452.
83. Sah, P., & Bekkers, J. M. (1996). Apical dendritic location of slow afterhyperpolarization current in hippocampal pyramidal neurons: Implications for the integration of long-term potentiation. Journal of Neuroscience, 16, 4537-4542.
84. Sakimura, K., Kutsuwada, T., Ito, I., Manabe, T., Takayama, C., Kushiya, E., et al. (1995). Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor ε1 subunit. Nature, 373, 151-155.
85. Sans, N. A., Montcouquiol, M. E., & Raymond, J. (2000). Postnatal developmental changes in AMPA and NMDA receptors in the rat vestibular nuclei. Developmental Brain Research, 123, 41-52.
86. Schiller, J., Helmchen, F., & Sakmann, B. (1995). Spatial profile of dendritic calcium transients evoked by action potentials in rat neocortical pyramidal neurons. Journal of Physiology (London), 487, 583-600.
87. 2+ influx and reversal potentials in recombinant N-methyl-D-aspartate receptor channels. Biophysical Journal, 70, 2165-2174.
88. Schneggenburger, R., Zhou, Z., Konnerth, A., & Neher, E. (1993). Fractional contribution of calcium to the cation current through glutamate receptor channels. Neuron, 11, 133-143.
89. Sheng, M., Cummings, J., Roldan, L. A., Jan, Y. N., & Jan, L. Y. (1994). Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature, 368, 144-147.
90. Shi, J., Aamodt, S. M., & Constantine-Paton, M. (1997). Temporal correlations between functional and molecular changes in NMDA receptors and GABA neurotransmission in the superior colliculus. Journal of Neuroscience, 17, 6264-6276.
91. Shouval, H. Z., Bear, M. F., & Cooper, L. N. (2002). A unified model of NMDA receptor-dependent bidirectional synaptic plasticity. Proceedings of the National Academy of Sciences of the United States of America, 99, 10831-10836.
92. Shouval, H. Z., & Kalantzis, G. (2005). Stochastic properties of synaptic transmission affect the shape of spike time-dependent plasticity curves. Journal of Neurophysiology, 93, 1069-1073.
93. Simons, D. J. (1978). Response properties of vibrissa units in rat SI somatosensory neocortex. Journal of Neurophysiology, 41, 798-820.
94. Simons, D. J., & Carvell, G. E. (1989). Thalamocortical response transformation in the rat vibrissa/barrel system. Journal of Neurophysiology, 61, 311-330.
95. Song, S., & Abbott, L. F. (2001). Cortical development and remapping through spike timing-dependent plasticity. Neuron, 32, 339-350.
96. Song, S., Miller, K. D., & Abbott, L. F. (2000). Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nature Neuroscience, 3, 919-926.
97. Steigerwald, F., Schulz, T. W., Schenker, L. T., Kennedy, M. B., Seeburg, P. H., & Köhr, G. (2000). C-terminal truncation of NR2A subunits impairs synaptic but not extrasynaptic localization of NMDA receptors. Journal of Neuroscience, 20, 4573-4581.
98. Stephenson, F. A. (2001). Subunit characterization of NMDA receptors. Current Drug Targets, 2, 233-239.
99. Stern, E. A., Maravall, M., & Svoboda, K. (2001). Rapid development and plasticity of layer 2/3 maps in rat barrel cortex in vivo. Neuron, 31, 305-315.
100. Svoboda, K., Denk, W., Kleinfeld, D., & Tank, D. W. (1997). In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature, 385, 161-165.
101. Tang, Y. P., Shimizu, E., Dube, G. R., Rampon, C., Kerchner, G. A., Zhuo, M., et al. (1999). Genetic enhancement of learning and memory in mice. Nature, 401, 63-69.
102. Tateno, T., Harsch, A., & Robinson, H. P. C. (2004). Threshold firing frequency-current relationships of neurons in rat somatosensory cortex: Type 1 and type 2 dynamics. Journal of Neurophysiology, 92, 2283-2294.
103. Tegner, J., & Kepecs, A. (2002). Why neuronal dynamics should control synaptic learning rules. In T. G. Dietterich, S. Becker, & Z. Ghahramani (Eds.), Advances in Neural Information Processing Systems 14. Cambridge: MIT Press.
104. Togashi, K., Kitajima, T., Aihara, T., Hong, K., Poo, M., & Nishiyama, M. (2003). Gating of activity-dependent long-term depression by GABAergic activity in the hippocampus. Society for Neuroscience, 123.4 (Abstract).
105. Troyer, T. W., & Miller, K. D. (1997). Physiological gain leads to high ISI variability in a simple model of a cortical regular spiking cell. Neural Computation, 9, 971-983.
106. Umemiya, M., Chen, N., Raymond, L. A., & Murphy, T. H. (2001). A calcium-dependent feedback mechanism participates in shaping single NMDA miniature EPSCs. Journal of Neuroscience, 21, 1-9.
107. Van Rossum, M. C. W., Bi, G. Q., & Turrigiano, G. G. (2000). Stable Hebbian learning from spike timing-dependent plasticity. Journal of Neuroscience, 20, 8812-8821.
108. Vicini, S., Wang, J. F., Li, J. H., Zhu, W. J., Wang, Y. H., Luo, J. H., et al. (1998). Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. Journal of Neurophysiology, 79, 555-566.
109. Wang, H. X., Gerkin, R. C., Nauen, D. W., & Bi, G. Q. (2005). Coactivation and timing-dependent integration of synaptic potentiation and depression. Nature Neuroscience, 8, 187-193.
110. Xia, Z., & Storm, D. R. (2005). The role of calmodulin as a signal integrator for synaptic plasticity. Nature Reviews. Neuroscience, 6, 267-276.
111. 2+]i elevation. Journal of Neurophysiology, 81, 781-787.
112. Zador, A., Koch, C., & Brown, T. H. (1990). Biophysical model of a Hebbian synapse. Proceedings of the National Academy of Sciences of the United States of America, 87, 6718-6722.
113. 2+/ calmodulin-dependent protein kinase-phosphatase system. Biophysical Journal, 79, 2211-2221.
114. Zhang, L. I., Tao, H. W., Holt, C. E., Harris, W. A., & Poo, M. M. (1998). A critical window for cooperation and competition among developing retinotectal synapses. Nature, 395, 37-44.