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The Scientific World Journal
Volume 2012, Article ID 267120, 11 pages
http://dx.doi.org/10.1100/2012/267120
Review Article

Distribution of Extrasynaptic NMDA Receptors on Neurons

Advanced Imaging Core, NIDCD/NIH, 50 South Drive (50/4142), Bethesda, MD 20892-8027, USA

Received 12 December 2011; Accepted 2 January 2012

Academic Editors: E. Kumamoto, B. Martinac, B. Poulain, and T. E. Salt

Copyright © 2012 Ronald S. Petralia. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. W. Gereau IV and G. T. Swanson, The Glutamate Receptors, Humana Press, Totowa, NJ, USA, 2008.
  2. J. Kehoe, S. Buldakova, F. Acher, J. Dent, P. Bregestovski, and J. Bradley, “Aplysia cys-loop glutamate-gated chloride channels reveal convergent evolution of ligand specificity,” Journal of Molecular Evolution, vol. 69, no. 2, pp. 125–141, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. H. Janovjak, G. Sandoz, and E. Y. Isacoff, “A modern ionotropic glutamate receptor with a K+ selectivity signature sequence,” Nature Communications, vol. 2, no. 1, article 231, 2011. View at Publisher · View at Google Scholar
  4. T. J. Ryan and S. G. N. Grant, “The origin and evolution of synapses,” Nature Reviews Neuroscience, vol. 10, no. 10, pp. 701–712, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Alié and M. Manuël, “The backbone of the post-synaptic density originated in a unicellular ancestor of choanoflagellates and metazoans,” BMC Evolutionary Biology, vol. 10, no. 1, article 34, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Srivastava, O. Simakov, J. Chapman et al., “The Amphimedon queenslandica genome and the evolution of animal complexity,” Nature, vol. 466, no. 7307, pp. 720–726, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. C.-Y. Zheng, G. K. Seabold, M. Horak, and R. S. Petralia, “MAGUKs, synaptic development, and synaptic plasticity,” Neuroscientist, vol. 17, no. 5, pp. 493–512, 2011. View at Publisher · View at Google Scholar
  8. R. S. Petralia, Y. X. Wang, F. Hua et al., “Organization of NMDA receptors at extrasynaptic locations,” Neuroscience, vol. 167, no. 1, pp. 68–87, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. C. M. Gladding and L. A. Raymond, “Mechanisms underlying NMDA receptor synaptic/extrasynaptic distribution and function,” Molecular and Cellular Neuroscience, vol. 48, no. 4, pp. 308–320, 2011. View at Publisher · View at Google Scholar
  10. M. A. Henson, A. C. Roberts, I. Pérez-Otaño, and B. D. Philpot, “Influence of the NR3A subunit on NMDA receptor functions,” Progress in Neurobiology, vol. 91, no. 1, pp. 23–37, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Zhao, Y. Peng, Z. Xu et al., “Synaptic metaplasticity through NMDA receptor lateral diffusion,” Journal of Neuroscience, vol. 28, no. 12, pp. 3060–3070, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. L. Groc, L. Bard, and D. Choquet, “Surface trafficking of N-methyl-d-aspartate receptors: physiological and pathological perspectives,” Neuroscience, vol. 158, no. 1, pp. 4–18, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. L. Bard and L. Groc, “Glutamate receptor dynamics and protein interaction: lessons from the NMDA receptor,” Molecular and Cellular Neuroscience, vol. 48, no. 4, pp. 298–307, 2011. View at Publisher · View at Google Scholar
  14. P. Y. Wang, R. S. Petralia, Y.-X. Wang, R. J. Wenthold, and S. D. Brenowitz, “Functional NMDA receptors at axonal growth cones of young hippocampal neurons,” Journal of Neuroscience, vol. 31, no. 25, pp. 9289–9297, 2011. View at Publisher · View at Google Scholar
  15. R. S. Petralia, Y. X. Wang, and R. J. Wenthold, “Internalization at glutamatergic synapses during development,” European Journal of Neuroscience, vol. 18, no. 12, pp. 3207–3217, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Washbourne, X. B. Liu, E. G. Jones, and A. K. McAllister, “Cycling of NMDA receptors during trafficking in neurons before synapse formation,” Journal of Neuroscience, vol. 24, no. 38, pp. 8253–8264, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. H. Suh, A. Terashima, R. S. Petralia et al., “A neuronal role for SNAP-23 in postsynaptic glutamate receptor trafficking,” Nature Neuroscience, vol. 13, no. 3, pp. 338–343, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Washbourne, J. E. Bennett, and A. K. McAllister, “Rapid recruitment of NMDA receptor transport packets to nascent synapses,” Nature Neuroscience, vol. 5, no. 8, pp. 751–759, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. V. Sytnyk, I. Leshchyns'Ka, A. G. Nikonenko, and M. Schachner, “NCAM promotes assembly and activity-dependent remodeling of the postsynaptic signaling complex,” Journal of Cell Biology, vol. 174, no. 7, pp. 1071–1085, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. R. S. Petralia, N. Sans, Y. X. Wang, and R. J. Wenthold, “Ontogeny of postsynaptic density proteins at glutamatergic synapses,” Molecular and Cellular Neuroscience, vol. 29, no. 3, pp. 436–452, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. R. S. Petralia, “Trafficking and targeting of NMDA receptors,” in Biology of the NMDA Receptor, A. M. van Dongen, Ed., pp. 149–200, CRC/Taylor and Francis, Boca Raton, Fla, USA, 2009. View at Google Scholar
  22. J. C. Platel, K. A. Dave, V. Gordon, B. Lacar, M. E. Rubio, and A. Bordey, “NMDA receptors activated by subventricular zone astrocytic glutamate are critical for neuroblast survival prior to entering a synaptic network,” Neuron, vol. 65, no. 6, pp. 859–872, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. W. C. Sin, K. Haas, E. S. Ruthazer, and H. T. Cline, “Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases,” Nature, vol. 419, no. 6906, pp. 475–480, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Georgiev, H. Taniura, Y. Kambe, T. Takarada, and Y. Yoneda, “A critical importance of polyamine site in NMDA receptors for neurite outgrowth and fasciculation at early stages of P19 neuronal differentiation,” Experimental Cell Research, vol. 314, no. 14, pp. 2603–2617, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. M. D. Ehlers, E. T. Fung, R. J. O'Brien, and R. L. Huganir, “Splice variant-specific interaction of the NMDA receptor subunit NR1 with neuronal intermediate filaments,” Journal of Neuroscience, vol. 18, no. 2, pp. 720–730, 1998. View at Google Scholar · View at Scopus
  26. M. Herkert, S. Rottger, and C. M. Becker, “The NMDA receptor subunit NR2B of neonatal rat brain: complex formation and enrichment in axonal growth cones,” European Journal of Neuroscience, vol. 10, no. 5, pp. 1553–1562, 1998. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Nishiyama, M. J. Von Schimmelmann, K. Togashi, W. M. Findley, and K. Hong, “Membrane potential shifts caused by diffusible guidance signals direct growth-cone turning,” Nature Neuroscience, vol. 11, no. 7, pp. 762–771, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Schmitz, J. Luccarelli, M. Kim, M. Wang, and D. Sulzer, “Glutamate controls growth rate and branching of dopaminergic axons,” Journal of Neuroscience, vol. 29, no. 38, pp. 11973–11981, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. P. M. Kim, H. Aizawa, P. S. Kim et al., “Serine racemase: activation by glutamate neurotransmission via glutamate receptor interacting protein and mediation of neuronal migration,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 6, pp. 2105–2110, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Komuro and P. Rakic, “Modulation of neuronal migration by NMDA receptors,” Science, vol. 259, no. 5104, pp. 95–97, 1993. View at Google Scholar · View at Scopus
  31. E. Michard, P. T. Lima, F. Borges et al., “Glutamate receptor-like genes form Ca2+ channels in pollen ubes and are regulated by pistil D-serine,” Science, vol. 332, no. 6028, pp. 434–437, 2011. View at Publisher · View at Google Scholar
  32. P. Paudice, A. Gemignani, and M. Raiteri, “Evidence for functional native NMDA receptors activated by glycine or D-serine alone in the absence of glutamatergic coagonist,” European Journal of Neuroscience, vol. 10, no. 9, pp. 2934–2944, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. J. C. Piña-Crespo, M. Talantova, I. Micu et al., “Excitatory glycine responses of CNS myelin mediated by NR1/NR3 “NMDA" receptor subunits,” Journal of Neuroscience, vol. 30, no. 34, pp. 11501–11505, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. W. Lu and K. W. Roche, “Posttranslational regulation of AMPA receptor trafficking and function,” Current Opinion in Neurobiology. In press. View at Publisher · View at Google Scholar
  35. H. D. MacGillavry, J. M. Kerr, and T. A. Blanpied, “Lateral organization of the postsynaptic density,” Molecular and Cellular Neuroscience, vol. 48, no. 4, pp. 321–331, 2011. View at Publisher · View at Google Scholar
  36. R. S. Petralia, Y. X. Wang, and R. J. Wenthold, “NMDA receptors and PSD-95 are found in attachment plaques in cerebellar granular layer glomeruli,” European Journal of Neuroscience, vol. 15, no. 3, pp. 583–587, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. C. Rosenmund, A. Feltz, and G. L. Westbrook, “Synaptic NMDA receptor channels have a low open probability,” Journal of Neuroscience, vol. 15, no. 4, pp. 2788–2795, 1995. View at Google Scholar · View at Scopus
  38. K. R. Tovar and G. L. Westbrook, “The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro,” Journal of Neuroscience, vol. 19, no. 10, pp. 4180–4188, 1999. View at Google Scholar · View at Scopus
  39. K. R. Tovar and G. L. Westbrook, “Mobile NMDA receptors at hippocampal synapses,” Neuron, vol. 34, no. 2, pp. 255–264, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Ivanov, C. Pellegrino, S. Rama et al., “Opposing role of synaptic and extrasynaptic NMDA receptors in regulation of the extracellular signal-regulated kinases (ERK) activity in cultured rat hippocampal neurons,” Journal of Physiology, vol. 572, no. 3, pp. 789–798, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Z. Harris and D. L. Pettit, “Extrasynaptic and synaptic NMDA receptors form stable and uniform pools in rat hippocampal slices,” Journal of Physiology, vol. 584, no. 2, pp. 509–519, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. C. M. Low and K. S. L. Wee, “New insights into the not-so-new NR3 subunits of N-methyl-D-aspartate receptor: localization, structure, and function,” Molecular Pharmacology, vol. 78, no. 1, pp. 1–11, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Prybylowski, G. Rumbaugh, B. B. Wolfe, and S. Vicini, “Increased exon 5 expression alters extrasynaptic NMDA receptors in cerebellar neurons,” Journal of Neurochemistry, vol. 75, no. 3, pp. 1140–1146, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. N. A. Lozovaya, S. E. Grebenyuk, T. S. Tsintsadze, B. Feng, D. T. Monaghan, and O. A. Krishtal, “Extrasynaptic NR2B and NR2D subunits of NMDA receptors shape 'superslow' afterburst EPSC in rat hippocampus,” Journal of Physiology, vol. 558, no. 2, pp. 451–463, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. G. Rumbaugh and S. Vicini, “Distinct synaptic and extrasynaptic NMDA receptors in developing cerebellar granule neurons,” Journal of Neuroscience, vol. 19, no. 24, pp. 10603–10610, 1999. View at Google Scholar · View at Scopus
  46. A. M. Binshtok, I. A. Fleidervish, R. Sprengel, and M. J. Gutnick, “NMDA receptors in layer 4 spiny stellate cells of the mouse barrel cortex contain the NR2C subunit,” Journal of Neuroscience, vol. 26, no. 2, pp. 708–715, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. N. Sans, R. S. Petralia, Y. X. Wang, J. Blahos, J. W. Hell, and R. J. Wenthold, “A developmental change in NMDA receptor-associated proteins at hippocampal synapses,” Journal of Neuroscience, vol. 20, no. 3, pp. 1260–1271, 2000. View at Google Scholar · View at Scopus
  48. A. Erisir and J. L. Harris, “Decline of the critical period of visual plasticity is concurrent with the reduction of NR2B subunit of the synaptic NMDA receptor in layer 4,” Journal of Neuroscience, vol. 23, no. 12, pp. 5208–5218, 2003. View at Google Scholar · View at Scopus
  49. X. B. Liu, K. D. Murray, and E. G. Jones, “Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development,” Journal of Neuroscience, vol. 24, no. 40, pp. 8885–8895, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. L. Groc, M. Heine, L. Cognet et al., “Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors,” Nature Neuroscience, vol. 7, no. 7, pp. 695–696, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. L. Groc, M. Heine, S. L. Cousins et al., “NMDA receptor surface mobility depends on NR2A-2B subunits,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 49, pp. 18769–18774, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. Y. N. Dong, H. Y. Wu, F. C. Hsu, D. A. Coulter, and D. R. Lynch, “Developmental and cell-selective variations in N-methyl-D-aspartate receptor degradation by calpain,” Journal of Neurochemistry, vol. 99, no. 1, pp. 206–217, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. I. Pérez-Otaño, R. Luján, S. J. Tavalin et al., “Endocytosis and synaptic removal of NR3A-containing NMDA receptors by PACSIN1/syndapin1,” Nature Neuroscience, vol. 9, no. 5, pp. 611–621, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. J.-H. Tao-Cheng et al., “Evidence from electron micrographs for NMDA receptor trafficking in hippocampal cultures,” Society for Neuroscience, Abstract no. 865.07, 2011. View at Google Scholar
  55. C. Aoki, C. Venkatesan, C. G. Go, J. A. Mong, and T. M. Dawson, “Cellular and subcellular localization of NMDA-R1 subunit immunoreactivity in the visual cortex of adult and neonatal rats,” Journal of Neuroscience, vol. 14, no. 9, pp. 5202–5222, 1994. View at Google Scholar · View at Scopus
  56. Y. Takumi, V. Ramírez-León, P. Laake, E. Rinvik, and O. P. Ottersen, “Different modes of expression of AMPA and NMDA receptors in hippocampal synapses,” Nature Neuroscience, vol. 2, no. 7, pp. 618–624, 1999. View at Publisher · View at Google Scholar · View at Scopus
  57. J. G. Valtschanoff, A. Burette, R. J. Wenthold, and R. J. Weinberg, “Expression of NR2 receptor subunit in rat somatic sensory cortex: synaptic distribution and colocalization with NR1 and PSD-95,” Journal of Comparative Neurology, vol. 410, no. 4, pp. 599–611, 1999. View at Publisher · View at Google Scholar · View at Scopus
  58. V. N. Kharazia and R. J. Weinberg, “Immunogold localization of AMPA and NMDA receptors in somatic sensory cortex of albino rat,” Journal of Comparative Neurology, vol. 412, no. 2, pp. 292–302, 1999. View at Publisher · View at Google Scholar · View at Scopus
  59. D. A. Rusakov and D. M. Kullmann, “Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation,” Journal of Neuroscience, vol. 18, no. 9, pp. 3158–3170, 1998. View at Google Scholar · View at Scopus
  60. L. Alonso-Nanclares, A. Minelli, M. Melone, R. H. Edwards, J. Defelipe, and F. Conti, “Perisomatic glutamatergic axon terminals: a novel feature of cortical synaptology revealed by vesicular glutamate transporter 1 immunostaining,” Neuroscience, vol. 123, no. 2, pp. 547–556, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Merchán-Pérez, J. R. Rodriguez, C. E. Ribak, and J. DeFelipe, “Proximity of excitatory and inhibitory axon terminals adjacent to pyramidal cell bodies provides a putative basis for nonsynaptic interactions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 24, pp. 9878–9883, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Alamilla and D. C. Gillespie, “Glutamatergic inputs and glutamate-releasing immature inhibitory inputs activate a shared postsynaptic receptor population in lateral superior olive,” Neuroscience, vol. 196, pp. 285–296, 2011. View at Publisher · View at Google Scholar
  63. C. G. Thomas, H. Tian, and J. S. Diamond, “The relative roles of diffusion and uptake in clearing synaptically released glutamate change during early postnatal development,” Journal of Neuroscience, vol. 31, no. 12, pp. 4743–4754, 2011. View at Publisher · View at Google Scholar
  64. M. A. Xu-Friedman and W. G. Regehr, “Ultrastructural contributions to desensitization at cerebellar mossy fiber to granule cell synapses,” Journal of Neuroscience, vol. 23, no. 6, pp. 2182–2192, 2003. View at Google Scholar · View at Scopus
  65. G. Szapiro and B. Barbour, “Parasynaptic signalling by fast neurotransmitters: the cerebellar cortex,” Neuroscience, vol. 162, no. 3, pp. 644–655, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. P. Rossi, E. Sola, V. Taglietti et al., “NMDA receptor 2 (NR2) C-terminal control of NR open probability regulates synaptic transmission and plasticity at a cerebellar synapse,” Journal of Neuroscience, vol. 22, no. 22, pp. 9687–9697, 2002. View at Google Scholar · View at Scopus
  67. K. Matsui, C. E. Jahr, and M. E. Rubio, “High-concentration rapid transients of glutamate mediate neural-glial communication via ectopic release,” Journal of Neuroscience, vol. 25, no. 33, pp. 7538–7547, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. K. Matsui and C. E. Jahr, “Exocytosis unbound,” Current Opinion in Neurobiology, vol. 16, no. 3, pp. 305–311, 2006. View at Publisher · View at Google Scholar · View at Scopus
  69. N. B. Hamilton and D. Attwell, “Do astrocytes really exocytose neurotransmitters?” Nature Reviews Neuroscience, vol. 11, no. 4, pp. 227–238, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. T. Fellin, O. Pascual, S. Gobbo, T. Pozzan, P. G. Haydon, and G. Carmignoto, “Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors,” Neuron, vol. 43, no. 5, pp. 729–743, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. L. H. Bergersen and V. Gundersen, “Morphological evidence for vesicular glutamate release from astrocytes,” Neuroscience, vol. 158, no. 1, pp. 260–265, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. P. Jourdain, L. H. Bergersen, K. Bhaukaurally et al., “Glutamate exocytosis from astrocytes controls synaptic strength,” Nature Neuroscience, vol. 10, no. 3, pp. 331–339, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. M. Kukley, E. Capetillo-Zarate, and D. Dietrich, “Vesicular glutamate release from axons in white matter,” Nature Neuroscience, vol. 10, no. 3, pp. 311–320, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. J. L. Ziskin, A. Nishiyama, M. Rubio, M. Fukaya, and D. E. Bergles, “Vesicular release of glutamate from unmyelinated axons in white matter,” Nature Neuroscience, vol. 10, no. 3, pp. 321–330, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. A. M. De Jesus Domingues, K. M. Neugebauer, and R. Fern, “Identification of four functional NR3B isoforms in developing white matter reveals unexpected diversity among glutamate receptors,” Journal of Neurochemistry, vol. 117, no. 3, pp. 449–460, 2011. View at Publisher · View at Google Scholar
  76. X. Chen, C. Winters, R. Azzam et al., “Organization of the core structure of the postsynaptic density,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 11, pp. 4453–4458, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. L. Groc, M. Lafourcade, M. Heine et al., “Surface trafficking of neurotransmitter receptor: comparison between single-molecule/quantum dot strategies,” Journal of Neuroscience, vol. 27, no. 46, pp. 12433–12437, 2007. View at Publisher · View at Google Scholar · View at Scopus
  78. Z. Yi, R. S. Petralia, Z. Fu et al., “The role of the PDZ protein GIPC in regulating NMDA receptor trafficking,” Journal of Neuroscience, vol. 27, no. 43, pp. 11663–11675, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. D. Li, C. G. Specht, C. L. Waites et al., “SAP97 directs NMDA receptor spine targeting and synaptic plasticity,” Journal of Physiology, vol. 589, no. 18, pp. 4491–4510, 2011. View at Publisher · View at Google Scholar
  80. D. W. Allison, V. I. Gelfand, I. Spector, and A. M. Craig, “Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors,” Journal of Neuroscience, vol. 18, no. 7, pp. 2423–2436, 1998. View at Google Scholar · View at Scopus
  81. N. Sans, K. Prybylowski, R. S. Petralia et al., “NMDA receptor trafficking through an interaction between PDZ proteins and the exocyst complex,” Nature Cell Biology, vol. 5, no. 6, pp. 520–530, 2003. View at Publisher · View at Google Scholar · View at Scopus
  82. N. Sans, P. Y. Wang, Q. Du et al., “mPins modulates PSD-95 and SAP102 trafficking and influences NMDA receptor surface expression,” Nature Cell Biology, vol. 7, no. 12, pp. 1079–1090, 2005. View at Publisher · View at Google Scholar · View at Scopus
  83. G. E. Hardingham and H. Bading, “Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders,” Nature Reviews Neuroscience, vol. 11, no. 10, pp. 682–696, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. A. Scimemi, A. Fine, D. M. Kullmann, and D. A. Rusakov, “NR2B-containing receptors mediate cross talk among hippocampal synapses,” Journal of Neuroscience, vol. 24, no. 20, pp. 4767–4777, 2004. View at Publisher · View at Google Scholar · View at Scopus
  85. J. R. Chalifoux and A. G. Carter, “Glutamate spillover promotes the generation of NMDA spikes,” Journal of Neuroscience, vol. 31, no. 45, pp. 16435–16446, 2011. View at Publisher · View at Google Scholar
  86. S. Chen and J. S. Diamond, “Synaptically released glutamate activates extrasynaptic NMDA receptors on cells in the ganglion cell layer of rat retina,” Journal of Neuroscience, vol. 22, no. 6, pp. 2165–2173, 2002. View at Google Scholar · View at Scopus
  87. J. Zhang and J. S. Diamond, “Subunit- and pathway-specific localization of NMD a receptors and scaffolding proteins at ganglion cell synapses in rat retina,” Journal of Neuroscience, vol. 29, no. 13, pp. 4274–4286, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. A. Momiyama, “Distinct synaptic and extrasynaptic NMDA receptors identified in dorsal horn neurones of the adult rat spinal cord,” Journal of Physiology, vol. 523, no. 3, pp. 621–628, 2000. View at Google Scholar · View at Scopus
  89. J. E. Mellem, P. J. Brockie, Y. Zheng, D. M. Madsen, and A. V. Maricq, “Decoding of polymodal sensory stimuli by postsynaptic glutamate receptors in C. elegans,” Neuron, vol. 36, no. 5, pp. 933–944, 2002. View at Publisher · View at Google Scholar · View at Scopus
  90. C. Y. Tai, S. A. Kim, and E. M. Schuman, “Cadherins and synaptic plasticity,” Current Opinion in Cell Biology, vol. 20, no. 5, pp. 567–575, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. H. Togashi, J. Miyoshi, T. Honda, T. Sakisaka, Y. Takai, and M. Takeichi, “Interneurite affinity is regulated by heterophilic nectin interactions in concert with the cadherin machinery,” Journal of Cell Biology, vol. 174, no. 1, pp. 141–151, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. D. Gall, F. Prestori, E. Sola et al., “Intracellular calcium regulation by burst discharge determines bidirectional long-term synaptic plasticity at the cerebellum input stage,” Journal of Neuroscience, vol. 25, no. 19, pp. 4813–4822, 2005. View at Publisher · View at Google Scholar · View at Scopus
  93. C. E. Andreescu, F. Prestori, F. Brandalise et al., “NR2A subunit of the N-methyl d-aspartate receptors are required for potentiation at the mossy fiber to granule cell synapse and vestibulo-cerebellar motor learning,” Neuroscience, vol. 176, pp. 274–283, 2011. View at Publisher · View at Google Scholar
  94. P. Singh et al., “NMDA receptor mechanosensitivity is governed by the C-terminus of the NR2B subunit,” The Journal of Biological Chemistry, vol. 287, no. 6, pp. 4348–4359, 2011. View at Google Scholar