Skip to main content

Molecular Dynamics of the Excitatory Synapse

  • Chapter
  • First Online:

Part of the book series: Advances in Experimental Medicine and Biology ((volume 970))

Abstract

Molecular dynamics of synapses are one of the most important factors that control the remodeling of synaptic connection and efficacy of transmission. This chapter focuses on the dynamics of postsynaptic molecular machinery and describes the imaging technologies important for quantitative analyses of synapses, their application to the postsynaptic molecules, and the insights obtained from these analyses. New visualization techniques, such as super-resolution microscopy, will become an indispensable approach to reveal submicron changes of synaptic molecules. New methods of monitoring protein interactions will also be integrated with experimental paradigms of synaptic plasticity. Cell biological analyses, together with cutting-edge imaging technologies, have been applied to the studies of nascent synapse formation, synapse maintenance, and activity-dependent synapse remodeling. From these studies, a variety of new concepts emerged, such as local assembly of postsynaptic scaffolds, presence of “transport packets” of postsynaptic receptors, heterogeneity of actin movement within spines, and activity-free fluctuation of PSD/spine sizes. These new concepts are useful in understanding specific properties of postsynaptic functions and should be integrated in future to build a realistic model of the postsynaptic organization that can explain its remarkable stability and tunability.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Ando, R., Hama, H., Yamamoto-Hino, M., Mizuno, H., & Miyawaki, A. (2002). An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein. Proceedings of the National Academy of Sciences of the United States of America, 99, 12651–12656.

    Article  PubMed  CAS  Google Scholar 

  • Axelrod, D., Koppel, D. E., Schlessinger, J., Elson, E., & Webb, W. W. (1976). Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophysical Journal, 16, 1055–1069.

    Article  PubMed  CAS  Google Scholar 

  • Barrow, S. L., Constable, J. R., Clark, E., El-Sabeawy, F., McAllister, A. K., & Washbourne, P. (2009). Neuroligin1: A cell adhesion molecule that recruits PSD-95 and NMDA receptors by distinct mechanisms during synaptogenesis. Neural Development, 4, 17.

    Article  PubMed  CAS  Google Scholar 

  • Bates, M., Huang, B., Dempsey, G. T., & Zhuang, X. (2007). Multicolor super-resolution imaging with photo-switchable fluorescent probes. Science, 317, 1749–1753.

    Article  PubMed  CAS  Google Scholar 

  • Betzig, E., Patterson, G. H., Sougrat, R., Lindwasser, O. W., Olenych, S., Bonifacino, J. S., Davidson, M. W., Lippincott-Schwartz, J., & Hess, H. F. (2006). Imaging intracellular fluorescent proteins at nanometer resolution. Science, 313, 1642–1645.

    Article  PubMed  CAS  Google Scholar 

  • Bielas, S. L., Serneo, F. F., Chechlacz, M., Deerinck, T. J., Perkins, G. A., Allen, P. B., Ellisman, M. H., & Gleeson, J. G. (2007). Spinophilin facilitates dephosphorylation of doublecortin by PP1 to mediate microtubule bundling at the axonal wrist. Cell, 129, 579–591.

    Article  PubMed  CAS  Google Scholar 

  • Blanpied, T. A., Kerr, J. M., & Ehlers, M. D. (2008). Structural plasticity with preserved topology in the postsynaptic protein network. Proceedings of the National Academy of Sciences of the United States of America, 105, 12587–12592.

    Article  PubMed  CAS  Google Scholar 

  • Blanpied, T. A., Scott, D. B., & Ehlers, M. D. (2002). Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron, 36, 435–449.

    Article  PubMed  CAS  Google Scholar 

  • Brakeman, P. R., Lanahan, A. A., O’Brien, R., Roche, K., Barnes, C. A., Huganir, R. L., & Worley, P. F. (1997). Homer: A protein that selectively binds metabotropic glutamate receptors. Nature, 386, 284–288.

    Article  PubMed  CAS  Google Scholar 

  • Bresler, T., Ramati, Y., Zamorano, P. L., Zhai, R., Garner, C. C., & Ziv, N. E. (2001). The dynamics of SAP90/PSD-95 recruitment to new synaptic junctions. Molecular and Cellular Neuroscience, 18, 149–167.

    Article  PubMed  CAS  Google Scholar 

  • Bresler, T., Shapira, M., Boeckers, T., Dresbach, T., Futter, M., Garner, C. C., Rosenblum, K., Gundelfinger, E. D., & Ziv, N. E. (2004). Postsynaptic density assembly is fundamentally different from presynaptic active zone assembly. Journal of Neuroscience, 24, 1507–1520.

    Article  PubMed  CAS  Google Scholar 

  • Brose, N. (2009). Synaptogenic proteins and synaptic organizers: “Many hands make light work”. Neuron, 61, 650–652.

    Article  PubMed  CAS  Google Scholar 

  • Chen, X., Vinade, L., Leapman, R. D., Petersen, J. D., Nakagawa, T., Phillips, T. M., Sheng, M., & Reese, T. S. (2005). Mass of the postsynaptic density and enumeration of three key molecules. Proceedings of the National Academy of Sciences of the United States of America, 102, 11551–11556.

    Article  PubMed  CAS  Google Scholar 

  • Cheng, D., Hoogenraad, C. C., Rush, J., Ramm, E., Schlager, M. A., Duong, D. M., Xu, P., Wijayawardana, S. R., Hanfelt, J., Nakagawa, T., et al. (2006). Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Molecular & Cellular Proteomics, 5, 1158–1170.

    Article  CAS  Google Scholar 

  • Cho, K. O., Hunt, C. A., & Kennedy, M. B. (1992). The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron, 9, 929–942.

    Article  PubMed  CAS  Google Scholar 

  • D’Angelo, M. A., Raices, M., Panowski, S. H., & Hetzer, M. W. (2009). Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells. Cell, 136, 284–295.

    Article  PubMed  CAS  Google Scholar 

  • Dailey, M. E., & Smith, S. J. (1996). The dynamics of dendritic structure in developing hippocampal slices. Journal of Neuroscience, 16, 2983–2994.

    PubMed  CAS  Google Scholar 

  • Fischer, M., Kaech, S., Knutti, D., & Matus, A. (1998). Rapid actin-based plasticity in dendritic spines. Neuron, 20, 847–854.

    Article  PubMed  CAS  Google Scholar 

  • Frost, N. A., Shroff, H., Kong, H., Betzig, E., & Blanpied, T. A. (2010). Single-molecule discrimination of discrete perisynaptic and distributed sites of actin filament assembly within dendritic spines. Neuron, 67, 86–99.

    Article  PubMed  CAS  Google Scholar 

  • Fujiwara, T., Ritchie, K., Murakoshi, H., Jacobson, K., & Kusumi, A. (2002). Phospholipids undergo hop diffusion in compartmentalized cell membrane. The Journal of Cell Biology, 157, 1071–1081.

    Article  PubMed  CAS  Google Scholar 

  • Furutani, Y., Matsuno, H., Kawasaki, M., Sasaki, T., Mori, K., & Yoshihara, Y. (2007). Interaction between telencephalin and ERM family proteins mediates dendritic filopodia formation. Journal of Neuroscience, 27, 8866–8876.

    Article  PubMed  CAS  Google Scholar 

  • Gerrow, K., Romorini, S., Nabi, S. M., Colicos, M. A., Sala, C., & El-Husseini, A. (2006). A preformed complex of postsynaptic proteins is involved in excitatory synapse development. Neuron, 49, 547–562.

    Article  PubMed  CAS  Google Scholar 

  • Graf, E. R., Zhang, X., Jin, S. X., Linhoff, M. W., & Craig, A. M. (2004). Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell, 119, 1013–1026.

    Article  PubMed  CAS  Google Scholar 

  • Gray, N. W., Weimer, R. M., Bureau, I., & Svoboda, K. (2006). Rapid redistribution of synaptic PSD-95 in the neocortex in vivo. PLoS Biology, 4, e370.

    Article  PubMed  CAS  Google Scholar 

  • Groc, L., Heine, M., Cognet, L., Brickley, K., Stephenson, F. A., Lounis, B., & Choquet, D. (2004). Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nature Neuroscience, 7, 695–696.

    Article  PubMed  CAS  Google Scholar 

  • Groc, L., Lafourcade, M., Heine, M., Renner, M., Racine, V., Sibarita, J. B., Lounis, B., Choquet, D., & Cognet, L. (2007). Surface trafficking of neurotransmitter receptor: Comparison between single-molecule/quantum dot strategies. Journal of Neuroscience, 27, 12433–12437.

    Article  PubMed  CAS  Google Scholar 

  • Harris, K. M., Jensen, 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.

    PubMed  CAS  Google Scholar 

  • Hering, H., & Sheng, M. (2003). Activity-dependent redistribution and essential role of cortactin in dendritic spine morphogenesis. Journal of Neuroscience, 23, 11759–11769.

    PubMed  CAS  Google Scholar 

  • Hirokawa, N. (1989). The arrangement of actin filaments in the postsynaptic cytoplasm of the cerebellar cortex revealed by quick-freeze deep-etch electron microscopy. Neuroscience Research, 6, 269–275.

    Article  PubMed  CAS  Google Scholar 

  • Hoffman-Kim, D., Diefenbach, T. J., Eustace, B. K., & Jay, D. G. (2007). Chromophore-assisted laser inactivation. Methods in Cell Biology, 82, 335–354.

    Article  PubMed  CAS  Google Scholar 

  • Honkura, N., Matsuzaki, M., Noguchi, J., Ellis-Davies, G. C., & Kasai, H. (2008). The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron, 57, 719–729.

    Article  PubMed  CAS  Google Scholar 

  • Hotulainen, P., Llano, O., Smirnov, S., Tanhuanpaa, K., Faix, J., Rivera, C., & Lappalainen, P. (2009). Defining mechanisms of actin polymerization and depolymerization during dendritic spine morphogenesis. The Journal of Cell Biology, 185, 323–339.

    Article  PubMed  CAS  Google Scholar 

  • Huang, B., Wang, W., Bates, M., & Zhuang, X. (2008). Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science, 319, 810–813.

    Article  PubMed  CAS  Google Scholar 

  • Husi, H., Ward, M. A., Choudhary, J. S., Blackstock, W. P., & Grant, S. G. (2000). Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nature Neuroscience, 3, 661–669.

    Article  PubMed  CAS  Google Scholar 

  • Iki, J., Inoue, A., Bito, H., & Okabe, S. (2005). Bi-directional regulation of postsynaptic cortactin distribution by BDNF and NMDA receptor activity. European Journal of Neuroscience, 22, 2985–2994.

    Article  PubMed  Google Scholar 

  • Irie, M., Hata, Y., Takeuchi, M., Ichtchenko, K., Toyoda, A., Hirao, K., Takai, Y., Rosahl, T. W., & Sudhof, T. C. (1997). Binding of neuroligins to PSD-95. Science, 277, 1511–1515.

    Article  PubMed  CAS  Google Scholar 

  • Jaworski, J., Kapitein, L. C., Gouveia, S. M., Dortland, B. R., Wulf, P. S., Grigoriev, I., Camera, P., Spangler, S. A., Di Stefano, P., Demmers, J., et al. (2009). Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron, 61, 85–100.

    Article  PubMed  CAS  Google Scholar 

  • Jontes, J. D., Emond, M. R., & Smith, S. J. (2004). In vivo trafficking and targeting of N-cadherin to nascent presynaptic terminals. Journal of Neuroscience, 24, 9027–9034.

    Article  PubMed  CAS  Google Scholar 

  • Jordan, B. A., Fernholz, B. D., Boussac, M., Xu, C., Grigorean, G., Ziff, E. B., & Neubert, T. A. (2004). Identification and verification of novel rodent postsynaptic density proteins. Molecular & Cellular Proteomics, 3, 857–871.

    Article  CAS  Google Scholar 

  • Kopec, C. D., Li, B., Wei, W., Boehm, J., & Malinow, R. (2006). Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. Journal of Neuroscience, 26, 2000–2009.

    Article  PubMed  CAS  Google Scholar 

  • Kornau, H. C., Schenker, L. T., Kennedy, M. B., & Seeburg, P. H. (1995). Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science, 269, 1737–1740.

    Article  PubMed  CAS  Google Scholar 

  • Korobova, F., & Svitkina, T. (2010). Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Molecular Biology of the Cell, 21, 165–176.

    Article  PubMed  CAS  Google Scholar 

  • Kuriu, T., Inoue, A., Bito, H., Sobue, K., & Okabe, S. (2006). Differential control of postsynaptic density scaffolds via actin-dependent and -independent mechanisms. Journal of Neuroscience, 26, 7693–7706.

    Article  PubMed  CAS  Google Scholar 

  • Landis, D. M., & Reese, T. S. (1983). Cytoplasmic organization in cerebellar dendritic spines. The Journal of Cell Biology, 97, 1169–1178.

    Article  PubMed  CAS  Google Scholar 

  • Li, Z., Okamoto, K., Hayashi, Y., & Sheng, M. (2004). The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell, 119, 873–887.

    Article  PubMed  CAS  Google Scholar 

  • Majewska, A., Tashiro, A., & Yuste, R. (2000). Regulation of spine calcium dynamics by rapid spine motility. Journal of Neuroscience, 20, 8262–8268.

    PubMed  CAS  Google Scholar 

  • Matsuno, H., Okabe, S., Mishina, M., Yanagida, T., Mori, K., & Yoshihara, Y. (2006). Telencephalin slows spine maturation. Journal of Neuroscience, 26, 1776–1786.

    Article  PubMed  CAS  Google Scholar 

  • Matsuzaki, M., Honkura, N., Ellis-Davies, G. C., & Kasai, H. (2004). Structural basis of long-term potentiation in single dendritic spines. Nature, 429, 761–766.

    Article  PubMed  CAS  Google Scholar 

  • Matus, A. (2000). Actin-based plasticity in dendritic spines. Science, 290, 754–758.

    Article  PubMed  CAS  Google Scholar 

  • Mendez, P., De Roo, M., Poglia, L., Klauser, P., & Muller, D. (2010). N-cadherin mediates plasticity-induced long-term spine stabilization. The Journal of Cell Biology, 189, 589–600.

    Article  PubMed  CAS  Google Scholar 

  • Meyer, G., Varoqueaux, F., Neeb, A., Oschlies, M., & Brose, N. (2004). The complexity of PDZ domain-mediated interactions at glutamatergic synapses: A case study on neuroligin. Neuropharmacology, 47, 724–733.

    Article  PubMed  CAS  Google Scholar 

  • Minerbi, A., Kahana, R., Goldfeld, L., Kaufman, M., Marom, S., & Ziv, N. E. (2009). Long-term relationships between synaptic tenacity, synaptic remodeling, and network activity. PLoS Biology, 7, e1000136.

    Article  PubMed  CAS  Google Scholar 

  • Mitchison, T. J. (1989). Polewards microtubule flux in the mitotic spindle: Evidence from photoactivation of fluorescence. The Journal of Cell Biology, 109, 637–652.

    Article  PubMed  CAS  Google Scholar 

  • Nagerl, U. V., Eberhorn, N., Cambridge, S. B., & Bonhoeffer, T. (2004). Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron, 44, 759–767.

    Article  PubMed  Google Scholar 

  • Nam, C. I., & Chen, L. (2005). Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proceedings of the National Academy of Sciences of the United States of America, 102, 6137–6142.

    Article  PubMed  CAS  Google Scholar 

  • Newpher, T. M., & Ehlers, M. D. (2008). Glutamate receptor dynamics in dendritic microdomains. Neuron, 58, 472–497.

    Article  PubMed  CAS  Google Scholar 

  • Nusser, Z. (1999). A new approach to estimate the number, density and variability of receptors at central synapses. European Journal of Neuroscience, 11, 745–752.

    Article  PubMed  CAS  Google Scholar 

  • Nusser, Z., Lujan, R., Laube, G., Roberts, J. D., Molnar, E., & Somogyi, P. (1998). Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron, 21, 545–559.

    Article  PubMed  CAS  Google Scholar 

  • Okabe, S. (2007). Molecular anatomy of the postsynaptic density. Molecular and Cellular Neuroscience, 34, 503–518.

    Article  PubMed  CAS  Google Scholar 

  • Okabe, S., & Hirokawa, N. (1989). Incorporation and turnover of biotin-labeled actin microinjected into fibroblastic cells: An immunoelectron microscopic study. The Journal of Cell Biology, 109, 1581–1595.

    Article  PubMed  CAS  Google Scholar 

  • Okabe, S., & Hirokawa, N. (1992). Differential behavior of photoactivated microtubules in growing axons of mouse and frog neurons. The Journal of Cell Biology, 117, 105–120.

    Article  PubMed  CAS  Google Scholar 

  • Okabe, S., & Hirokawa, N. (1993). Do photobleached fluorescent microtubules move?: Re-evaluation of fluorescence laser photobleaching both in vitro and in growing Xenopus axon. The Journal of Cell Biology, 120, 1177–1186.

    Article  PubMed  CAS  Google Scholar 

  • Okabe, S., Miwa, A., & Okado, H. (2001a). Spine formation and correlated assembly of presynaptic and postsynaptic molecules. Journal of Neuroscience, 21, 6105–6114.

    PubMed  CAS  Google Scholar 

  • Okabe, S., Urushido, T., Konno, D., Okado, H., & Sobue, K. (2001b). Rapid redistribution of the postsynaptic density protein PSD-Zip45 (Homer 1c) and its differential regulation by NMDA receptors and calcium channels. Journal of Neuroscience, 21, 9561–9571.

    PubMed  CAS  Google Scholar 

  • Palade, G. E., & Palay, S. L. (1954). Electron microscopic observations of interneuronal and neuromuscular synapses. Anatomical Record, 118, 335–336.

    Google Scholar 

  • Park, M., Salgado, J. M., Ostroff, L., Helton, T. D., Robinson, C. G., Harris, K. M., & Ehlers, M. D. (2006). Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron, 52, 817–830.

    Article  PubMed  CAS  Google Scholar 

  • Patterson, G. H., & Lippincott-Schwartz, J. (2002). A photoactivatable GFP for selective photolabeling of proteins and cells. Science, 297, 1873–1877.

    Article  PubMed  CAS  Google Scholar 

  • Petralia, R. S., Wang, Y. X., & Wenthold, R. J. (1994a). The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. Journal of Neuroscience, 14, 6102–6120.

    PubMed  CAS  Google Scholar 

  • Petralia, R. S., Yokotani, N., & Wenthold, R. J. (1994b). Light and electron microscope distributions of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. Journal of Neuroscience, 14, 667–696.

    PubMed  CAS  Google Scholar 

  • Petrini, E. M., Lu, J., Cognet, L., Lounis, B., Ehlers, M. D., & Choquet, D. (2009). Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron, 63, 92–105.

    Article  PubMed  CAS  Google Scholar 

  • Portera-Cailliau, C., Pan, D. T., & Yuste, R. (2003). Activity-regulated dynamic behavior of early dendritic protrusions: Evidence for different types of dendritic filopodia. Journal of Neuroscience, 23, 7129–7142.

    PubMed  CAS  Google Scholar 

  • Racz, B., Blanpied, T. A., Ehlers, M. D., & Weinberg, R. J. (2004). Lateral organization of endocytic machinery in dendritic spines. Nature Neuroscience, 7, 917–918.

    Article  PubMed  CAS  Google Scholar 

  • Rajfur, Z., Roy, P., Otey, C., Romer, L., & Jacobson, K. (2002). Dissecting the link between stress fibres and focal adhesions by CALI with EGFP fusion proteins. Nature Cell Biology, 4, 286–293.

    Article  PubMed  CAS  Google Scholar 

  • Reits, E. A., & Neefjes, J. J. (2001). From fixed to FRAP: Measuring protein mobility and activity in living cells. Nature Cell Biology, 3, E145–E147.

    Article  PubMed  CAS  Google Scholar 

  • Rust, M. J., Bates, M., & Zhuang, X. (2006). Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nature Methods, 3, 793–795.

    Article  PubMed  CAS  Google Scholar 

  • Saglietti, L., Dequidt, C., Kamieniarz, K., Rousset, M. C., Valnegri, P., Thoumine, O., Beretta, F., Fagni, L., Choquet, D., Sala, C., et al. (2007). Extracellular interactions between GluR2 and N-cadherin in spine regulation. Neuron, 54, 461–477.

    Article  PubMed  CAS  Google Scholar 

  • Schapitz, I. U., Behrend, B., Pechmann, Y., Lappe-Siefke, C., Kneussel, S. J., Wallace, K. E., Stempel, A. V., Buck, F., Grant, S. G., Schweizer, M., et al. (2010). Neuroligin 1 is dynamically exchanged at postsynaptic sites. Journal of Neuroscience, 30, 12733–12744.

    Article  PubMed  CAS  Google Scholar 

  • Scheiffele, P., Fan, J., Choih, J., Fetter, R., & Serafini, T. (2000). Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell, 101, 657–669.

    Article  PubMed  CAS  Google Scholar 

  • Schneider, M., Barozzi, S., Testa, I., Faretta, M., & Diaspro, A. (2005). Two-photon activation and excitation properties of PA-GFP in the 720–920-nm region. Biophysical Journal, 89, 1346–1352.

    Article  PubMed  CAS  Google Scholar 

  • Sharma, K., Fong, D. K., & Craig, A. M. (2006). Postsynaptic protein mobility in dendritic spines: Long-term regulation by synaptic NMDA receptor activation. Molecular and Cellular Neuroscience, 31, 702–712.

    Article  PubMed  CAS  Google Scholar 

  • Shepherd, J. D., & Huganir, R. L. (2007). The cell biology of synaptic plasticity: AMPA receptor trafficking. Annual Review of Cell and Developmental Biology, 23, 613–643.

    Article  PubMed  CAS  Google Scholar 

  • Shroff, H., Galbraith, C. G., Galbraith, J. A., White, H., Gillette, J., Olenych, S., Davidson, M. W., & Betzig, E. (2007). Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes. Proceedings of the National Academy of Sciences of the United States of America, 104, 20308–20313.

    Article  PubMed  CAS  Google Scholar 

  • Sinnecker, D., Voigt, P., Hellwig, N., & Schaefer, M. (2005). Reversible photobleaching of enhanced green fluorescent proteins. Biochemistry, 44, 7085–7094.

    Article  PubMed  CAS  Google Scholar 

  • Spacek, J. (1985). Three-dimensional analysis of dendritic spines. II. Spine apparatus and other cytoplasmic components. Anatomy and Embryology, 171, 235–243.

    Article  PubMed  CAS  Google Scholar 

  • Spacek, J., & Harris, K. M. (1998). Three-dimensional organization of cell adhesion junctions at synapses and dendritic spines in area CA1 of the rat hippocampus. The Journal of Comparative Neurology, 393, 58–68.

    Article  PubMed  CAS  Google Scholar 

  • Stan, A., Pielarski, K. N., Brigadski, T., Wittenmayer, N., Fedorchenko, O., Gohla, A., Lessmann, V., Dresbach, T., & Gottmann, K. (2010). Essential cooperation of N-cadherin and neuroligin-1 in the transsynaptic control of vesicle accumulation. Proceedings of the National Academy of Sciences of the United States of America, 107, 11116–11121.

    Article  PubMed  CAS  Google Scholar 

  • Star, E. N., Kwiatkowski, D. J., & Murthy, V. N. (2002). Rapid turnover of actin in dendritic spines and its regulation by activity. Nature Neuroscience, 5, 239–246.

    Article  PubMed  CAS  Google Scholar 

  • Sugiyama, Y., Kawabata, I., Sobue, K., & Okabe, S. (2005). Determination of absolute protein numbers in single synapses by a GFP-based calibration technique. Nature Methods, 2, 677–684.

    Article  PubMed  CAS  Google Scholar 

  • Svitkina, T. M., Bulanova, E. A., Chaga, O. Y., Vignjevic, D. M., Kojima, S., Vasiliev, J. M., & Borisy, G. G. (2003). Mechanism of filopodia initiation by reorganization of a dendritic network. The Journal of Cell Biology, 160, 409–421.

    Article  PubMed  CAS  Google Scholar 

  • Svoboda, K., Tank, D. W., & Denk, W. (1996). Direct measurement of coupling between dendritic spines and shafts. Science, 272, 716–719.

    Article  PubMed  CAS  Google Scholar 

  • Tanaka, J., Matsuzaki, M., Tarusawa, E., Momiyama, A., Molnar, E., Kasai, H., & Shigemoto, R. (2005). Number and density of AMPA receptors in single synapses in immature cerebellum. Journal of Neuroscience, 25, 799–807.

    Article  PubMed  CAS  Google Scholar 

  • Tatavarty, V., Kim, E. J., Rodionov, V., & Yu, J. (2009). Investigating sub-spine actin dynamics in rat hippocampal neurons with super-resolution optical imaging. PloS One, 4, e7724.

    Article  PubMed  CAS  Google Scholar 

  • Thyagarajan, A., & Ting, A. Y. (2010). Imaging activity-dependent regulation of neurexin-neuroligin interactions using trans-synaptic enzymatic biotinylation. Cell, 143, 456–469.

    Article  PubMed  CAS  Google Scholar 

  • Togashi, H., Abe, K., Mizoguchi, A., Takaoka, K., Chisaka, O., & Takeichi, M. (2002). Cadherin regulates dendritic spine morphogenesis. Neuron, 35, 77–89.

    Article  PubMed  CAS  Google Scholar 

  • Tomita, S., Adesnik, H., Sekiguchi, M., Zhang, W., Wada, K., Howe, J. R., Nicoll, R. A., & Bredt, D. S. (2005). Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature, 435, 1052–1058.

    Article  PubMed  CAS  Google Scholar 

  • Triller, A., & Choquet, D. (2008). New concepts in synaptic biology derived from single-molecule imaging. Neuron, 59, 359–374.

    Article  PubMed  CAS  Google Scholar 

  • Tu, J. C., Xiao, B., Naisbitt, S., Yuan, J. P., Petralia, R. S., Brakeman, P., Doan, A., Aakalu, V. K., Lanahan, A. A., Sheng, M., & Worley, P. F. (1999). Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron, 23, 583–592.

    Article  PubMed  CAS  Google Scholar 

  • Valtschanoff, J. G., & Weinberg, R. J. (2001). Laminar organization of the NMDA receptor complex within the postsynaptic density. Journal of Neuroscience, 21, 1211–1217.

    PubMed  CAS  Google Scholar 

  • Wang, Z., Edwards, J. G., Riley, N., Provance, D. W., Jr., Karcher, R., Li, X. D., Davison, I. G., Ikebe, M., Mercer, J. A., Kauer, J. A., & Ehlers, M. D. (2008). Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell, 135, 535–548.

    Article  PubMed  CAS  Google Scholar 

  • Washbourne, P., Bennett, J. E., & McAllister, A. K. (2002). Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nature Neuroscience, 5, 751–759.

    PubMed  CAS  Google Scholar 

  • Yasumatsu, N., Matsuzaki, M., Miyazaki, T., Noguchi, J., & Kasai, H. (2008). Principles of long-term dynamics of dendritic spines. Journal of Neuroscience, 28, 13592–13608.

    Article  PubMed  CAS  Google Scholar 

  • Yoshihara, Y., Oka, S., Nemoto, Y., Watanabe, Y., Nagata, S., Kagamiyama, H., & Mori, K. (1994). An ICAM-related neuronal glycoprotein, telencephalin, with brain segment-specific expression. Neuron, 12, 541–553.

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura, Y., Yamauchi, Y., Shinkawa, T., Taoka, M., Donai, H., Takahashi, N., Isobe, T., & Yamauchi, T. (2004). Molecular constituents of the postsynaptic density fraction revealed by proteomic analysis using multidimensional liquid chromatography-tandem mass spectrometry. Journal of Neurochemistry, 88, 759–768.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, Q., Homma, K. J., & Poo, M. M. (2004). Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron, 44, 749–757.

    Article  PubMed  CAS  Google Scholar 

  • Zuo, Y., Lin, A., Chang, P., & Gan, W. B. (2005). Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron, 46, 181–189.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shigeo Okabe .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag/WIen

About this chapter

Cite this chapter

Okabe, S. (2012). Molecular Dynamics of the Excitatory Synapse. In: Kreutz, M., Sala, C. (eds) Synaptic Plasticity. Advances in Experimental Medicine and Biology, vol 970. Springer, Vienna. https://doi.org/10.1007/978-3-7091-0932-8_6

Download citation

Publish with us

Policies and ethics