Size and receptor density of glutamatergic synapses: A viewpoint from left-right asymmetry of CA3-CA1 connections

Frontiers in Neuroanatomy

Volumn 3, Issue JUL, 2009, Pages

  Shinohara, Yoshiaki ^a   Hirase, Hajime ^a,b  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b SAITAMA UNIVERSITY   (Japan)

Author keywords

AMPAR; Glutamate; MGlur5; NMDAR; PSD; Spines

Indexed keywords

EID: 84886580278     PISSN: 16625129     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.05.010.2009     Document Type: Article

References (60)

1. Adesnik, H., and Nicoll, R. A. (2007). Conservation of glutamate receptor 2-containing AMPA receptors during long-term potentiation. J. Neurosci. 27, 4598-4602.
2. Bagal, A. A., Kao, J. P., Tang, C. M., and Thompson, S. M. (2005). Long-term potentiation of exogenous glutamate responses at single dendritic spines. Proc. Natl. Acad. Sci. USA 102, 14434-14439.
3. Clem, R. L., and Barth, A. (2006). Pathwayspecifi c traffi cking of native AMPARs by in vivo experience. Neuron 49, 663-670.
4. Clements, J. D., and Westbrook, G. L. (1991). Activation kinetics reveal the number of glutamate and glycine binding sites on the N-methyl-D-aspartate receptor. Neuron 7, 605-613.
5. Derkach, V. A., Oh, M. C., Guire, E. S., and Soderling, T. R. (2007). Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat. Rev. Neurosci. 8, 101-113.
6. Engert, F., and Bonhoeffer, T. (1999). Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70.
7. Enoki, R., Hu, Y. L., Hamilton, D., and Fine, A. (2009). Expression of longterm plasticity at individual synapses in hippocampus is graded, bidirectional, and mainly presynaptic: optical quantal analysis. Neuron 62, 242-253.
8. Furukawa, H., Singh, S. K., Mancusso, R., and Gouaux, E. (2005). Subunit arrangement and function in NMDA receptors. Nature 438, 185-192.
9. Grutzendler, J., Kasthuri, N., and Gan, W. B. (2002). Long-term dendritic spine stability in the adult cortex. Nature 420, 812-816.
10. Harris, K. M., and Stevens, J. K. (1989). Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9, 2982-2997.
11. Hayashi, Y., Shi, S. H., Esteban, J. A., Piccini, A., Poncer, J. C., and Malinow, R. (2000). Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262-2267.
12. Hell, S. W., Dyba, M., and Jakobs, S. (2004). Concepts for nanoscale resolution in fl uorescence microscopy. Curr. Opin. Neurobiol. 14, 599-609.
13. Holtmaat, A. J., Trachtenberg, J. T., Wilbrecht, L., Shepherd, G. M., Zhang, X., Knott, G. W., and Svoboda, K. (2005). Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45, 279-291.
14. Kasai, H., Matsuzaki, M., Noguchi, J., Yasumatsu, N., and Nakahara, H. (2003). Structure-stability-function relationships of dendritic spines. Trends Neurosci. 26, 360-368.
15. Kawakami, R., Shinohara, Y., Kato, Y., Sugiyama, H., Shigemoto, R., and Ito, I. (2003). Asymmetrical allocation of NMDA receptor epsilon2 subunits in hippocampal circuitry. Science 300, 990-994.
16. Konur, S., Rabinowitz, D., Fenstermaker, V. L., and Yuste, R. (2003). Systematic regulation of spine sizes and densities in pyramidal neurons. J. Neurobiol. 56, 95-112.
17. Kopec, C. D., Real, E., Kessels, H. W., and Malinow, R. (2007). GluR1 links structural and functional plasticity at excitatory synapses. J. Neurosci. 27, 13706-13718.
18. Kuriu, T., Inoue, A., Bito, H., Sobue, K., and Okabe, S. (2006). Differential control of postsynaptic density scaffolds via actin-dependent and - independent mechanisms. J. Neurosci. 26, 7693-7706.
19. Liu, L., Wong, T. P., Pozza, M. F., Lingenhoehl, K., Wang, Y., Sheng, M., Auberson, Y. P., and Wang, Y. T. (2004). Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304, 1021-1024.
20. Lu, Y. M., Jia, Z., Janus, C., Henderson, J. T., Gerlai, R., Wojtowicz, J. M., and Roder, J. C. (1997). Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J. Neurosci. 17, 5196-5205.
21. Lujan, R., Nusser, Z., Roberts, J. D., Shigemoto, R., and Somogyi, P. (1996). Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur. J. Neurosci. 8, 1488-1500.
22. Maccaferri, G., Toth, K., and McBain, C. J. (1998). Target-specifi c expression of presynaptic mossy fiber plasticity. Science 279, 1368-1370.
23. Malenka, R. C., and Bear, M. F. (2004). LTP and LTD: an embarrassment of riches. Neuron 44, 5-21.
24. Malinow, R., and Malenka, R. C. (2002). AMPA receptor traffi cking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103-126.
25. Masugi-Tokita, M., and Shigemoto, R. (2007). High-resolution quantitative visualization of glutamate and GABA receptors at central synapses. Curr. Opin. Neurobiol. 17, 387-393.
26. Matsuo, N., Reijmers, L., and Mayford, M. (2008). Spine-type-specifi c recruitment of newly synthesized AMPA receptors with learning. Science 319, 1104-1107.
27. Matsuzaki, M. (2007). Factors critical for the plasticity of dendritic spines and memory storage. Neurosci. Res. 57, 1-9.
28. Matsuzaki, M., Honkura, N., Ellis- Davies, G. C., and Kasai, H. (2004). Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761-766.
29. McCann, C. M., Tapia, J. C., Kim, H., Coggan, J. S., and Lichtman, J. W. (2008). Rapid and modifiable neurotransmitter receptor dynamics at a neuronal synapse in vivo. Nat. Neurosci. 11, 807-815.
30. Micheva, K. D., and Smith, S. J. (2007). Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 55, 25-36.
31. Miwa, H., Fukaya, M., Watabe, A. M., Watanabe, M., and Manabe, T. (2008). Functional contributions of synaptically localized NR2B subunits of the NMDA receptor to synaptic transmission and long-term potentiation in the adult mouse CNS. J. Physiol. 586, 2539-2550.
32. Nakanishi, S. (1992). Molecular diversity of glutamate receptors and implications for brain function. Science 258, 597-603.
33. Nase, G., Weishaupt, J., Stern, P., Singer, W., and Monyer, H. (1999). Genetic and epigenetic regulation of NMDA receptor expression in the rat visual cortex. Eur. J. Neurosci. 11, 4320-4326.
34. Okamoto, K., and Hayashi, Y. (2006). Visualization of F-actin and G-actin equilibrium using fl uorescence resonance energy transfer (FRET) in cultured cells and neurons in slices. Nat. Protoc. 1, 911-919.
35. Okamoto, K., Nagai, T., Miyawaki, A., and Hayashi, Y. (2004). Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat. Neurosci. 7, 1104-1112.
36. Park, M., Penick, E. C., Edwards, J. G., Kauer, J. A., and Ehlers, M. D. (2004). Recycling endosomes supply AMPA receptors for LTP. Science 305, 1972-1975.
37. Plant, K., Pelkey, K. A., Bortolotto, Z. A., Morita, D., Terashima, A., McBain, C. J., Collingridge, G. L., and Isaac, J. T. (2006). Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 9, 602-604.
38. Racca, C., Stephenson, F. A., Streit, P., Roberts, J. D., and Somogyi, P. (2000). NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J. Neurosci. 20, 2512-2522.
39. Rodrigues, S. M., Bauer, E. P., Farb, C. R., Schafe, G. E., and LeDoux, J. E. (2002). The group I metabotropic glutamate receptor mGluR5 is required for fear memory formation and long-term potentiation in the lateral amygdala. J. Neurosci. 22, 5219-5229.
40. Rosenmund, C., Stern-Bach, Y., and Stevens, C. F. (1998). The tetrameric structure of a glutamate receptor channel. Science 280, 1596-1599.
41. Rumpel, S., LeDoux, J., Zador, A., and Malinow, R. (2005). Postsynaptic receptor trafficking underlying a form of associative learning. Science 308, 83-88.
42. Sans, N., Petralia, R. S., Wang, Y. X., Blahos, J. II, Hell, J. W., and Wenthold, R. J. (2000). A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J. Neurosci. 20, 1260-1271.
43. Scimemi, A., Fine, A., Kullmann, D. M., and Rusakov, D. A. (2004). NR2Bcontaining receptors mediate cross talk among hippocampal synapses. J. Neurosci. 24, 4767-4777.
44. Scott, R., and Rusakov, D. A. (2006). Main determinants of presynaptic Ca2+ dynamics at individual mossy fiber-CA3 pyramidal cell synapses. J. Neurosci. 26, 7071-7081.
45. Shi, S., Hayashi, Y., Esteban, J. A., and Malinow, R. (2001). Subunit- specifi c rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105, 331-343.
46. Shi, S. H., Hayashi, Y., Petralia, R. S., Zaman, S. H., Wenthold, R. J., Svoboda, K., and Malinow, R. (1999). Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 1811-1816.
47. Shinohara, Y., Hirase, H., Watanabe, M., Itakura, M., Takahashi, M., and Shigemoto, R. (2008). Left-right asymmetry of the hippocampal synapses with differential subunit allocation of glutamate receptors. Proc. Natl. Acad. Sci. USA 105, 19498-19503.
48. Sobczyk, A., Scheuss, V., and Svoboda, K. (2005). NMDA receptor subunitdependent [Ca2+] signaling in individual hippocampal dendritic spines. J. Neurosci. 25, 6037-6046.
49. Somogyi, P., Tamas, G., Lujan, R., and Buhl, E. H. (1998). Salient features of synaptic organisation in the cerebral cortex. Brain Res. Brain Res. Rev. 26, 113-135.
50. Stocca, G., and Vicini, S. (1998). Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. J. Physiol. 507(Pt 1), 13-24.
51. Takahashi, T., Svoboda, K., and Malinow, R. (2003). Experience strengthening transmission by driving AMPA receptors into synapses. Science 299, 1585-1588.
52. Takumi, Y., Ramirez-Leon, V., Laake, P., Rinvik, E., and Ottersen, O. P. (1999). Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat. Neurosci. 2, 618-624.
53. Tovar, K. R., and Westbrook, G. L. (1999). The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J. Neurosci. 19, 4180-4188.
54. Trachtenberg, J. T., Chen, B. E., Knott, G. W., Feng, G., Sanes, J. R., Welker, E., and Svoboda, K. (2002). Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420, 788-794.
55. Ward, B., McGuinness, L., Akerman, C. J., Fine, A., Bliss, T. V., and Emptage, N. J. (2006). State-dependent mechanisms of LTP expression revealed by optical quantal analysis. Neuron 52, 649-661.
56. Weisskopf, M. G., and Nicoll, R. A. (1995). Presynaptic changes during mossy fi bre LTP revealed by NMDA receptormediated synaptic responses. Nature 376, 256-259.
57. Wenthold, R. J., Petralia, R. S., Blahos, J. II, and Niedzielski, A. S. (1996). Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J. Neurosci. 16, 1982-1989.
58. Wu, Y., Kawakami, R., Shinohara, Y., Fukaya, M., Sakimura, K., Mishina, M., Watanabe, M., Ito, I., and Shigemoto, R. (2005). Target-cell-specifi c left-right asymmetry of NMDA receptor content in Schaffer collateral synapses in epsilon1/NR2A knock-out mice. J. Neurosci. 25, 9213-9226.
59. Xiang, Z., Greenwood, A. C., Kairiss, E. W., and Brown, T. H. (1994). Quantal mechanism of long-term potentiation in hippocampal mossy-fi ber synapses. J. Neurophysiol. 71, 2552-2556.
60. Yashiro, K., and Philpot, B. D. (2008). Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology 55, 1081-1094.