Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2012, Article ID 704103, 9 pages
http://dx.doi.org/10.1155/2012/704103
Review Article

Examining Form and Function of Dendritic Spines

Heart and Stroke Foundation Centre for Stroke Recovery, Centre for Neural Dynamics, and, Department of Cellular and Molecular Medicine, University of Ottawa, 451 Smyth Road, Rm 3501N, Ottawa, ON, Canada K1H 8M5

Received 13 December 2011; Accepted 10 January 2012

Academic Editor: Volker Korz

Copyright © 2012 Kevin F. H. Lee et al. 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. S. R. Cajal, “Estructura de los centros nerviosos de las aves,” Revista Trimestral de Histología Normal y Patológica, vol. 1, pp. 1–10, 1888. View at Google Scholar
  2. R. Yuste, Dendritic Spines, The MIT Press, Cambridge, Mass, USA, 2010.
  3. S. F. Traynelis, L. P. Wollmuth, C. J. McBain et al., “Glutamate receptor ion channels: structure, regulation, and function,” Pharmacological Reviews, vol. 62, no. 3, pp. 405–496, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Matsuzaki, N. Honkura, G. C. R. Ellis-Davies, and H. Kasai, “Structural basis of long-term potentiation in single dendritic spines,” Nature, vol. 429, no. 6993, pp. 761–766, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. R. C. Malenka and M. F. Bear, “LTP and LTD: an embarrassment of riches,” Neuron, vol. 44, no. 1, pp. 5–21, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. J. T. R. Isaac, G. O. Hjelmstad, R. A. Nicoll, and R. C. Malenka, “Long-term potentiation at single fiber inputs to hippocampal CA1 pyramidal cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 16, pp. 8710–8715, 1996. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Allen and C. F. Stevens, “An evaluation of causes for unreliability of synaptic transmission,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 22, pp. 10380–10383, 1994. View at Publisher · View at Google Scholar · View at Scopus
  8. C. F. Stevens and Y. Wang, “Facilitation and depression at single central synapses,” Neuron, vol. 14, no. 4, pp. 795–802, 1995. View at Google Scholar · View at Scopus
  9. L. E. Dobrunz and C. F. Stevens, “Heterogeneity of release probability, facilitation, and depletion at central synapses,” Neuron, vol. 18, no. 6, pp. 995–1008, 1997. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron, vol. 50, no. 6, pp. 823–839, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. W. Denk, K. R. Delaney, A. Gelperin et al., “Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy,” Journal of Neuroscience Methods, vol. 54, no. 2, pp. 151–162, 1994. View at Publisher · View at Google Scholar · View at Scopus
  12. F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nature Methods, vol. 2, no. 12, pp. 932–940, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. R. Araya, J. Jiang, K. B. Eisenthal, and R. Yuste, “The spine neck filters membrane potentials,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 47, pp. 17961–17966, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Ashby and J. Isaac, “Maturation of a recurrent excitatory neocortical circuit by experience-dependent unsilencing of newly formed dendritic spines,” Neuron, vol. 70, no. 3, pp. 510–521, 2011. View at Publisher · View at Google Scholar
  15. J. C. Béïque, D. T. Lin, M. G. Kang, H. Aizawa, K. Takamiya, and R. L. Huganir, “Synapse-specific regulation of AMPA receptor function by PSD-95,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 51, pp. 19535–19540, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. J. C. Béïque, Y. Na, D. Kuhl, P. F. Worley, and R. L. Huganir, “Arc-dependent synapse-specific homeostatic plasticity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 2, pp. 816–821, 2011. View at Publisher · View at Google Scholar
  17. B. L. Bloodgood, A. J. Giessel, and B. L. Sabatini, “Biphasic synaptic Ca influx arising from compartmentalized electrical signals in dendritic spines,” PLoS Biology, vol. 7, no. 9, Article ID e1000190, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. G. Busetto, M. J. Higley, and B. L. Sabatini, “Developmental presence and disappearance of postsynaptically silent synapses on dendritic spines of rat layer 2/3 pyramidal neurons,” Journal of Physiology, vol. 586, no. 6, pp. 1519–1527, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. C. D. Harvey, R. Yasuda, H. Zhong, and K. Svoboda, “The spread of Ras activity triggered by activation of a single dendritic spine,” Science, vol. 321, no. 5885, pp. 136–140, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. C. D. Harvey and K. Svoboda, “Locally dynamic synaptic learning rules in pyramidal neuron dendrites,” Nature, vol. 450, no. 7173, pp. 1195–1200, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Losonczy and J. C. Magee, “Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons,” Neuron, vol. 50, no. 2, pp. 291–307, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Matsuzaki, G. C. R. Ellis-Davies, T. Nemoto, Y. Miyashita, M. Iino, and H. Kasai, “Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons,” Nature Neuroscience, vol. 4, no. 11, pp. 1086–1092, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. J. I. Tanaka, Y. Horiike, M. Matsuzaki, T. Miyazaki, G. C. R. Ellis-Davies, and H. Kasai, “Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines,” Science, vol. 319, no. 5870, pp. 1683–1687, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Matsuzaki and H. Kasai, “Two-photon uncaging microscopy,” Cold Spring Harbor Protocols, vol. 6, no. 5, 2011. View at Publisher · View at Google Scholar
  25. J. Noguchi, A. Nagaoka, S. Watanabe et al., “In vivo two-photon uncaging of glutamate revealing the structure-function relationships of dendritic spines in the neocortex of adult mice,” Journal of Physiology, vol. 589, no. 10, pp. 2447–2457, 2011. View at Publisher · View at Google Scholar
  26. G. A. Kerchner and R. A. Nicoll, “Silent synapses and the emergence of a postsynaptic mechanism for LTP,” Nature Reviews Neuroscience, vol. 9, no. 11, pp. 813–825, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. M. A. Smith, G. C. R. Ellis-Davies, and J. C. Magee, “Mechanism of the distance-dependent scaling of Schaffer collateral synapses in rat CA1 pyramidal neurons,” Journal of Physiology, vol. 548, no. 1, pp. 245–258, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. K. M. Harris, F. E. Jensen, and B. Tsao, “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, vol. 12, no. 7, pp. 2685–2705, 1992. View at Google Scholar · View at Scopus
  29. J. I. Arellano, R. Benavides-Piccione, J. Defelipe, and R. Yuste, “Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies,” Frontiers in Neuroscience, vol. 1, pp. 131–143, 2007. View at Google Scholar
  30. J. A. Connor, L. D. P. Miller, J. Petrozzino, and W. Muller, “Calcium signaling in dendritic spines of hippocampal neurons,” Journal of Neurobiology, vol. 25, no. 3, pp. 234–242, 1994. View at Google Scholar · View at Scopus
  31. J. Noguchi, M. Matsuzaki, G. C. R. Ellis-Davies, and H. Kasai, “Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites,” Neuron, vol. 46, no. 4, pp. 609–622, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. T. G. Oertner, B. L. Sabatini, E. A. Nimchinsky, and K. Svoboda, “Facilitation at single synapses probed with optical quantal analysis,” Nature Neuroscience, vol. 5, no. 7, pp. 657–664, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. W. Muller and J. A. Connor, “Ca2+ signalling in postsynaptic dendrites and spines of mammalian neurons in brain slice,” Journal of Physiology Paris, vol. 86, no. 1-3, pp. 57–66, 1992. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Yuste, A. Majewska, and K. Holthoff, “From form to function: calcium compartmentalization in dendritic spines,” Nature Neuroscience, vol. 3, no. 7, pp. 653–659, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Zito, V. Scheuss, G. Knott, T. Hill, and K. Svoboda, “Rapid functional maturation of nascent dendritic spines,” Neuron, vol. 61, no. 2, pp. 247–258, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. B. L. Bloodgood and B. L. Sabatini, “Neuronal activity regulates diffusion across the neck of dendritic spines,” Science, vol. 310, no. 5749, pp. 866–869, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Svoboda, D. W. Tank, and W. Denk, “Direct measurement of coupling between dendritic spines and shafts,” Science, vol. 272, no. 5262, pp. 716–719, 1996. View at Google Scholar · View at Scopus
  38. B. A. Smith, H. Roy, P. De Koninck, P. Grütter, and Y. De Koninck, “Dendritic spine viscoelasticity and soft-glassy nature: balancing dynamic remodeling with structural stability,” Biophysical Journal, vol. 92, no. 4, pp. 1419–1430, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Majewska, E. Brown, J. Ross, and R. Yuste, “Mechanisms of calcium decay kinetics in hippocampal spines: role of spine calcium pumps and calcium diffusion through the spine neck in biochemical compartmentalization,” Journal of Neuroscience, vol. 20, no. 5, pp. 1722–1734, 2000. View at Google Scholar · View at Scopus
  40. K. A. Kenyon, E. A. Bushong, A. S. Mauer, E. E. Strehler, R. J. Weinberg, and A. C. Burette, “Cellular and subcellular localization of the neuron-specific plasma membrane calcium ATPase PMCA1a in the rat brain,” Journal of Comparative Neurology, vol. 518, no. 16, pp. 3169–3183, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. R. L. Redondo and R. G. M. Morris, “Making memories last: the synaptic tagging and capture hypothesis,” Nature Reviews Neuroscience, vol. 12, no. 1, pp. 17–30, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Govindarajan, I. Israely, S. Y. Huang, and S. Tonegawa, “The dendritic branch is the preferred integrative unit for protein synthesis-dependent LTP,” Neuron, vol. 69, no. 1, pp. 132–146, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. W. C. Abraham and J. M. Williams, “LTP maintenance and its protein synthesis-dependence,” Neurobiology of Learning and Memory, vol. 89, no. 3, pp. 260–268, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. S. J. R. Lee, Y. Escobedo-Lozoya, E. M. Szatmari, and R. Yasuda, “Activation of CaMKII in single dendritic spines during long-term potentiation,” Nature, vol. 458, no. 7236, pp. 299–304, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Murakoshi, H. Wang, and R. Yasuda, “Local, persistent activation of Rho GTPases during plasticity of single dendritic spines,” Nature, vol. 472, no. 7341, pp. 100–106, 2011. View at Publisher · View at Google Scholar
  46. M. Heine, L. Groc, R. Frischknecht et al., “Surface mobility of postsynaptic AMPARs tunes synaptic transmission,” Science, vol. 320, no. 5873, pp. 201–205, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. A. J. Borgdorff and D. Choquet, “Regulation of AMPA receptor lateral movements,” Nature, vol. 417, no. 6889, pp. 649–653, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. 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
  49. M. C. Ashby, S. R. Maier, A. Nishimune, and J. M. Henley, “Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology,” Journal of Neuroscience, vol. 26, no. 26, pp. 7046–7055, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. D. Holcman and A. Triller, “Modeling synaptic dynamics driven by receptor lateral diffusion,” Biophysical Journal, vol. 91, no. 7, pp. 2405–2415, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. D. Choquet, “Fast AMPAR trafficking for a high-frequency synaptic transmission,” The European Journal of Neuroscience, vol. 32, no. 2, pp. 250–260, 2010. View at Google Scholar
  52. B. Rácz, T. A. Blanpied, M. D. Ehlers, and R. J. Weinberg, “Lateral organization of endocytic machinery in dendritic spines,” Nature Neuroscience, vol. 7, no. 9, pp. 917–918, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Lu, T. D. Helton, T. A. Blanpied et al., “Postsynaptic positioning of endocytic zones and AMPA receptor cycling by physical coupling of dynamin-3 to Homer,” Neuron, vol. 55, no. 6, pp. 874–889, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. N. Z. Gerges, D. S. Backos, C. N. Rupasinghe, M. R. Spaller, and J. A. Esteban, “Dual role of the exocyst in AMPA receptor targeting and insertion into the postsynaptic membrane,” EMBO Journal, vol. 25, no. 8, pp. 1623–1634, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. T. A. Blanpied, D. B. Scott, and M. D. Ehlers, “Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines,” Neuron, vol. 36, no. 3, pp. 435–449, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. E. M. Petrini, J. Lu, L. Cognet, B. Lounis, M. D. Ehlers, and D. Choquet, “Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation,” Neuron, vol. 63, no. 1, pp. 92–105, 2009. View at Google Scholar · View at Scopus
  57. M. Park, E. C. Penick, J. G. Edwards, J. A. Kauer, and M. D. Ehlers, “Recycling endosomes supply AMPA receptors for LTP,” Science, vol. 305, no. 5692, pp. 1972–1975, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. G. A. Yudowski, M. A. Puthenveedu, D. Leonoudakis et al., “Real-time imaging of discrete exocytic events mediating surface delivery of AMPA receptors,” Journal of Neuroscience, vol. 27, no. 41, pp. 11112–11121, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. D. T. Lin, Y. Makino, K. Sharma et al., “Regulation of AMPA receptor extrasynaptic insertion by 4.1N, phosphorylation and palmitoylation,” Nature Neuroscience, vol. 12, no. 7, pp. 879–887, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. C. Lüscher, H. Xia, E. C. Beattie et al., “Role of AMPA receptor cycling in synaptic transmission and plasticity,” Neuron, vol. 24, no. 3, pp. 649–658, 1999. View at Google Scholar · View at Scopus
  61. C. Koch and A. Zador, “The function of dendritic spines: devices subserving biochemical rather than electrical compartmentalization,” Journal of Neuroscience, vol. 13, no. 2, pp. 413–422, 1993. View at Google Scholar · View at Scopus
  62. D. Tsay and R. Yuste, “On the electrical function of dendritic spines,” Trends in Neurosciences, vol. 27, no. 2, pp. 77–83, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. Y. Kovalchuk, E. Hanse, K. W. Kafitz, and A. Konnerth, “Postsynaptic induction of BDNF-mediated long-term potentiation,” Science, vol. 295, no. 5560, pp. 1729–1734, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Grunditz, N. Holbro, L. Tian, Y. Zuo, and T. G. Oertner, “Spine neck plasticity controls postsynaptic calcium signals through electrical compartmentalization,” Journal of Neuroscience, vol. 28, no. 50, pp. 13457–13466, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. 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
  66. H. Jia, N. L. Rochefort, X. Chen, and A. Konnerth, “In vivo two-photon imaging of sensory-evoked dendritic calcium signals in cortical neurons,” Nature Protocols, vol. 6, no. 1, pp. 28–35, 2011. View at Publisher · View at Google Scholar
  67. X. Chen, U. Leischner, N. L. Rochefort, I. Nelken, and A. Konnerth, “Functional mapping of single spines in cortical neurons in vivo,” Nature, vol. 475, no. 7357, pp. 501–505, 2011. View at Publisher · View at Google Scholar
  68. Z. Varga, H. Jia, B. Sakmann, and A. Konnerth, “Dendritic coding of multiple sensory inputs in single cortical neurons in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 37, pp. 15420–15425, 2011. View at Publisher · View at Google Scholar
  69. Y. Fukazawa, Y. Saitoh, F. Ozawa, Y. Ohta, K. Mizuno, and K. Inokuchi, “Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo,” Neuron, vol. 38, no. 3, pp. 447–460, 2003. View at Publisher · View at Google Scholar · View at Scopus
  70. K. I. Okamoto, T. Nagai, A. Miyawaki, and Y. Hayashi, “Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity,” Nature Neuroscience, vol. 7, no. 10, pp. 1104–1112, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. H. Kasai, T. Hayama, M. Ishikawa, S. Watanabe, S. Yagishita, and J. Noguchi, “Learning rules and persistence of dendritic spines,” The European journal of neuroscience, vol. 32, no. 2, pp. 241–249, 2010. View at Google Scholar
  72. M. Patterson and R. Yasuda, “Signalling pathways underlying structural plasticity of dendritic spines,” British Journal of Pharmacology, vol. 163, no. 8, pp. 1626–1638, 2011. View at Publisher · View at Google Scholar
  73. A. Barria, D. Muller, V. Derkach, L. C. Griffith, and T. R. Soderling, “Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation,” Science, vol. 276, no. 5321, pp. 2042–2045, 1997. View at Publisher · View at Google Scholar · View at Scopus
  74. R. Malinow, H. Schulman, and R. W. Tsien, “Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP,” Science, vol. 245, no. 4920, pp. 862–866, 1989. View at Google Scholar · View at Scopus
  75. J. Lisman, H. Schulman, and H. Cline, “The molecular basis of CaMKII function in synaptic and behavioural memory,” Nature Reviews Neuroscience, vol. 3, no. 3, pp. 175–190, 2002. View at Publisher · View at Google Scholar · View at Scopus
  76. K. I. Okamoto, R. Narayanan, S. H. Lee, K. Murata, and Y. Hayashi, “The role of CaMKII as an F-actin-bundling protein crucial for maintenance of dendritic spine structure,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 15, pp. 6418–6423, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. L. A. Cingolani and Y. Goda, “Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy,” Nature Reviews Neuroscience, vol. 9, no. 5, pp. 344–356, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. M. L. Hayashi, S. Y. Choi, B. S. Shankaranarayana Rao et al., “Altered cortical synaptic morphology and impaired memory consolidation in forebrain- specific dominant-negative PAK transgenic mice,” Neuron, vol. 42, no. 5, pp. 773–787, 2004. View at Publisher · View at Google Scholar · View at Scopus
  79. T. Krucker, G. R. Siggins, and S. Halpain, “Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 12, pp. 6856–6861, 2000. View at Publisher · View at Google Scholar · View at Scopus
  80. L. Y. Chen, C. S. Rex, M. S. Casale, C. M. Gall, and G. Lynch, “Changes in synaptic morphology accompany actin signaling during LTP,” Journal of Neuroscience, vol. 27, no. 20, pp. 5363–5372, 2007. View at Publisher · View at Google Scholar · View at Scopus
  81. B. Ramachandran and J. U. Frey, “Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices in vitro,” Journal of Neuroscience, vol. 29, no. 39, pp. 12167–12173, 2009. View at Publisher · View at Google Scholar · View at Scopus
  82. C. D. Kopec, E. Real, H. W. Kessels, and R. Malinow, “GluR1 links structural and functional plasticity at excitatory synapses,” Journal of Neuroscience, vol. 27, no. 50, pp. 13706–13718, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Baude, Z. Nusser, E. Molnar, R. A. J. McIlhinney, and P. Somogyi, “High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus,” Neuroscience, vol. 69, no. 4, pp. 1031–1055, 1995. View at Publisher · View at Google Scholar · View at Scopus
  84. 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
  85. Y. Katz, V. Menon, D. A. Nicholson, Y. Geinisman, W. L. Kath, and N. Spruston, “Synapse distribution suggests a two-stage model of dendritic integration in CA1 pyramidal neurons,” Neuron, vol. 63, no. 2, pp. 171–177, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. Y. Takumi, A. Matsubara, E. Rinvik, and O. P. Ottersen, “The arrangement of glutamate receptors in excitatory synapses,” Annals of the New York Academy of Sciences, vol. 868, pp. 474–482, 1999. View at Publisher · View at Google Scholar · View at Scopus
  87. J. T. R. Isaac, M. C. Crair, R. A. Nicoll, and R. C. Malenka, “Silent synapses during development of thalamocortical inputs,” Neuron, vol. 18, no. 2, pp. 269–280, 1997. View at Publisher · View at Google Scholar · View at Scopus
  88. J. J. Zhu and R. Malinow, “Acute versus chronic NMDA receptor blockade and synaptic AMPA receptor delivery,” Nature Neuroscience, vol. 5, no. 6, pp. 513–514, 2002. View at Publisher · View at Google Scholar · View at Scopus
  89. Q. Zhou, K. J. Homma, and M. M. Poo, “Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses,” Neuron, vol. 44, no. 5, pp. 749–757, 2004. View at Publisher · View at Google Scholar · View at Scopus
  90. X. B. Wang, Y. Yang, and Q. Zhou, “Independent expression of synaptic and morphological plasticity associated with long-term depression,” Journal of Neuroscience, vol. 27, no. 45, pp. 12419–12429, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. A. D. Sdrulla and D. J. Linden, “Double dissociation between long-term depression and dendritic spine morphology in cerebellar Purkinje cells,” Nature Neuroscience, vol. 10, no. 5, pp. 546–548, 2007. View at Publisher · View at Google Scholar · View at Scopus
  92. G. Turrigiano, “Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement,” Annual Review of Neuroscience, vol. 34, pp. 89–103, 2011. View at Publisher · View at Google Scholar
  93. M. C. Lee, R. Yasuda, and M. D. Ehlers, “Metaplasticity at Single Glutamatergic Synapses,” Neuron, vol. 66, no. 6, pp. 859–870, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. T. A. Blanpied and M. D. Ehlers, “Membrane trafficking and cytoskeletal dynamics in neuronal function,” Molecular and Cellular Neuroscience, vol. 48, no. 4, pp. 267–268, 2011. View at Publisher · View at Google Scholar
  95. T. A. Blanpied, J. M. Kerr, and M. D. Ehlers, “Structural plasticity with preserved topology in the postsynaptic protein network,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 34, pp. 12587–12592, 2008. View at Publisher · View at Google Scholar · View at Scopus
  96. S. Fusi, P. J. Drew, and L. F. Abbott, “Cascade models of synaptically stored memories,” Neuron, vol. 45, no. 4, pp. 599–611, 2005. View at Publisher · View at Google Scholar · View at Scopus
  97. S. Fusi and L. F. Abbott, “Limits on the memory storage capacity of bounded synapses,” Nature Neuroscience, vol. 10, no. 4, pp. 485–493, 2007. View at Publisher · View at Google Scholar · View at Scopus