Advertisement

Neurochemical Journal

, Volume 5, Issue 4, pp 229–239 | Cite as

Structural and functional modifications of presynaptic afferents: Do they correlate with learning mechanisms?

  • I. V. Kudryashova
Review Articles
  • 46 Downloads

Abstract

We review the modern data on the involvement of structural modifications of presynaptic afferents during the acquisition of individual experiences. During the ontogeny or regeneration of nervous tissue, this mechanism is responsible for adjusting the architecture of neuronal ensembles to the demands of adaptive behavior. The molecular basis of the formation and elimination of additional axonal branches is the modification of the actin cytoskeleton. These modifications involve cell adhesion molecules, as well as extracellular and intracellular signal and regulatory proteins, most of which play an important role in long-term plasticity. The possible involvement of structural modifications of presynaptic afferents in long-term memory consolidation is discussed.

Key words

long-term plasticity modification of presynaptic afference synaptogenesis synapse elimination cytoskeleton regulatory proteins cell adhesion molecules 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Butz, M., Wörgötter, F., and van Ooyen, A., Brain Res. Rev., 2009, vol. 60, no. 2, pp. 287–305.CrossRefGoogle Scholar
  2. 2.
    Craig, A.M., Graf, E.R., and Linhoff, M.W., Trends Neurosci., 2006, vol. 29, no. 1, pp. 8–20.PubMedCrossRefGoogle Scholar
  3. 3.
    Waites, C.L., Craig, A.M., and Garner, C.C., Annu. Rev. Neurosci., 2005, vol. 28, pp. 251–274.PubMedCrossRefGoogle Scholar
  4. 4.
    Holtmaat, A. and Svoboda, K., Nat. Rev. Neurosci., 2009, vol. 10, no. 9, pp. 647–658.PubMedCrossRefGoogle Scholar
  5. 5.
    Gallagher, H.C., Murphy, K.J., Foley, A.G., and Regan, C.M., J. Neurochem., 2001, vol. 77, no. 2, pp. 425–434.PubMedCrossRefGoogle Scholar
  6. 6.
    Lushnikova, I., Skibo, G., Muller, D., and Nikonenko, I., Hippocampus, 2009, vol. 19, no. 8, pp. 753–762.PubMedCrossRefGoogle Scholar
  7. 7.
    Santello, M. and Volterra, A., Neuroscience, 2009, vol. 158, no. 1, pp. 253–259.PubMedCrossRefGoogle Scholar
  8. 8.
    Halassa, M.M. and Haydon, P.G., Annu. Rev. Physiol., 2010, vol. 72, pp. 335–355.PubMedCrossRefGoogle Scholar
  9. 9.
    Theodosis, D.T., Piet, R., Poulain, D.A., and Oliet, S.H., Neurochem. Int., 2004, vol. 45, no. 4, pp. 491–501.PubMedCrossRefGoogle Scholar
  10. 10.
    Geraldo, S. and Gordon-Weeks, P.R., J. Cell Sci., 2009, vol. 122, no. 20, pp. 3595–3604.PubMedCrossRefGoogle Scholar
  11. 11.
    Kalil, K. and Dent, E.W., Curr. Opin. Neurobiol., 2005, vol. 15, no. 5, pp. 521–526.PubMedCrossRefGoogle Scholar
  12. 12.
    Kornack, D.R. and Giger, R.J., Curr. Opin. Neurobiol., 2005, vol. 15, no. 1, pp. 58–66.PubMedCrossRefGoogle Scholar
  13. 13.
    Gogolla, N., Galimberti, I., and Caroni, P., Curr. Opin. Neurobiol., 2007, vol. 17, no. 5, pp. 516–524.PubMedCrossRefGoogle Scholar
  14. 14.
    Stettler, D.D., Yamahachi, H., Li, W., Denk, W., and Gilbert, C.D., Neuron, 2006, vol. 49, no. 6, pp. 877–887.PubMedCrossRefGoogle Scholar
  15. 15.
    Leu, B., Koch, E., and Schmidt, J.T., Dev. Neurobiol., 2010, vol. 70, no. 13, pp. 897–911.PubMedGoogle Scholar
  16. 16.
    Tallafuss, A., Constable, J.R., and Washbourne, P., Eur. J. Neurosci., 2010, vol. 32, no. 2, pp. 198–206.PubMedCrossRefGoogle Scholar
  17. 17.
    Yamahachi, H., Marik, S.A., McManus, J.N., Denk, W., and Gilbert, C.D., Neuron, 2009, vol. 64, no. 5, pp. 719–729.PubMedCrossRefGoogle Scholar
  18. 18.
    García-Junco-Clemente, P., Cantero, G., Gómez-Sánchez, L., Linares-Clemente, P., Martínez-López, J.A., Luján, R., and Fernández-Chacón, R., J. Neurosci., 2010, vol. 30, no. 21, pp. 7377–7391.PubMedCrossRefGoogle Scholar
  19. 19.
    Yi, J.J. and Ehlers, M.D., Pharmacol. Rev., 2007, vol. 59, no. 1, pp. 14–39.PubMedCrossRefGoogle Scholar
  20. 20.
    Hegde, A.N., Learn. Mem., 2010, vol. 17, no. 7, pp. 314–327.PubMedCrossRefGoogle Scholar
  21. 21.
    DiAntonio, A. and Hicke, L., Annu. Rev. Neurosci., 2004, vol. 27, pp. 223–246.PubMedCrossRefGoogle Scholar
  22. 22.
    Bingol, B. and Schuman, E.M., Curr. Opin. Neurobiol., 2005, vol. 15, no. 5, pp. 536–541.PubMedCrossRefGoogle Scholar
  23. 23.
    Patrick, G.N., Curr. Opin. Neurobiol., 2006, vol. 16, no. 1, pp. 90–94.PubMedCrossRefGoogle Scholar
  24. 24.
    Ding, M. and Shen, K., BioEssays, 2008, vol. 30, nos. 11–12, pp. 1075–1083.PubMedCrossRefGoogle Scholar
  25. 25.
    Cline, H., Curr. Biol., 2003, vol. 13, no. 13, pp. R514–R516.PubMedCrossRefGoogle Scholar
  26. 26.
    Ehlers, M.D., Nat. Neurosci., 2003, vol. 6, no. 3, pp. 231–242.PubMedCrossRefGoogle Scholar
  27. 27.
    Johnston, J.A. and Madura, K., Prog. Neurobiol., 2004, vol. 73, no. 4, pp. 227–257.PubMedCrossRefGoogle Scholar
  28. 28.
    Tai, H.C. and Schuman, E.M., Nat. Rev. Neurosci., 2008, vol. 9, no. 11, pp. 826–838.PubMedCrossRefGoogle Scholar
  29. 29.
    Stahl, S., Reinders, Y., Asan, E., Mothes, W., Conzelmann, E., Sickmann, A., and Felbor, U., Biochim. Biophys. Acta, 2007, vol. 1774, no. 10, pp. 1237–1246.PubMedGoogle Scholar
  30. 30.
    Haas, K.F. and Broadie, K., Biochim. Biophys. Acta, 2008, vol. 1779, no. 8, pp. 495–506.PubMedGoogle Scholar
  31. 31.
    Kudryashova, I.V., Neirokhimiya, 2009, vol. 26, no. 3, pp. 191–201.Google Scholar
  32. 32.
    Karpova, A., Mikhaylova, M., Thomas, U., Knöpfel, T., and Behnisch, T., J. Neurosci., 2006, vol. 26, no. 18, pp. 4949–4955.PubMedCrossRefGoogle Scholar
  33. 33.
    Tsuriel, S., Geva, R., Zamorano, P., Dresbach, T., Boeckers, T., Gundelfinger, E.D., Garner, C.C., and Ziv, N.E., PLoS Biol., 2006, vol. 4, no. 9, p. e271.PubMedCrossRefGoogle Scholar
  34. 34.
    Rinetti, G.V. and Schweizer, F.E., J. Neurosci., 2010, vol. 30, no. 9, pp. 3157–3166.PubMedCrossRefGoogle Scholar
  35. 35.
    Zhao, Y., Hegde, A.N., and Martin, K.C., Curr. Biol., 2003, vol. 13, no. 11, pp. 887–898.PubMedCrossRefGoogle Scholar
  36. 36.
    Speese, S.D., Trotta, N., Rodesch, C.K., Aravamudan, B., and Broadie, K., Curr. Biol., 2003, vol. 13, no. 11, pp. 899–910.PubMedCrossRefGoogle Scholar
  37. 37.
    Morfini, G., Pigino, G., Opalach, K., Serulle, Y., Moreira, J.E., Sugimori, M., Llinás, R.R., and Brady, S.T., Proc. Natl. Acad. Sci. USA, 2007, vol. 104, no. 7, pp. 2442–2447.PubMedCrossRefGoogle Scholar
  38. 38.
    Suh, E.C., Jung, Y.J., Kim, Y.A., Park, E.M., and Lee, K.E., Neurotoxicology, 2008, vol. 29, no. 4, pp. 691–699.PubMedCrossRefGoogle Scholar
  39. 39.
    Serulle, Y., Morfini, G., Pigino, G., Moreira, J.E., Sugimori, M., Brady, S.T., and Llinás, R.R., Proc. Natl. Acad. Sci. USA, 2007, vol. 104, no. 7, pp. 2437–2441.PubMedCrossRefGoogle Scholar
  40. 40.
    Zuliani, C., Kleber, S., Klussmann, S., Wenger, T., Kenzelmann, M., Schreglmann, N., Martinez, A., del Rio, J.A., Soriano, E., Vodrazka, P., Kuner, R., Groene, H.J., Herr, I., Krammer, P.H., and Martin-Villalba, A., Cell Death Differ., 2006, vol. 13, no. 1, pp. 31–40.PubMedCrossRefGoogle Scholar
  41. 41.
    Gulyaeva, N.V., Kudryashov, I.E., and Kudryashova, I.V., J. Neurosci. Res., 2003, vol. 73, pp. 853–864.PubMedCrossRefGoogle Scholar
  42. 42.
    Stepanichev, M.Y., Kudryashova, I.V., Yakovlev, A.A., Onufriev, M.V., Khaspekov, L.G., Lyzhin, A.A., Lazareva, N.A., and Gulyaeva, N.V., Neuroscience, 2005, vol. 136, pp. 579–591.PubMedCrossRefGoogle Scholar
  43. 43.
    Stepanichev, M.Yu., Kudryashova, I.V., Yakovlev, A.A., Vorontsova, O.N., Lazareva, N.A., and Gulyaeva, N.V., Zhurn. Vyssh. Nervn. Deyat., 2006, vol. 56, no. 2, pp. 247–256.Google Scholar
  44. 44.
    Kudryashova, I.V., Stepanichev, M.Yu., and Gulyaeva, N.V., Zhurn. Vyssh. Nervn. Deyat., 2007, vol. 57, no. 6, pp. 702–710.Google Scholar
  45. 45.
    Kudryashova, I.V., Onufriev, M.V., Kudryashov, I.E., and Gulyaeva, N.V., Neirokhimiya, 2008, vol. 25, no. 4, pp. 304–308.Google Scholar
  46. 46.
    Kudryashova, I.V., Onufriev, M.V., Kudryashov, I.E., and Gulyaeva, N.V., Neirokhimiya, 2009, vol. 26, no. 4, pp. 290–296.Google Scholar
  47. 47.
    Gilman, C.P. and Mattson, M.P., Neuromol. Med., 2002, vol. 2, no. 2, pp. 197–214.CrossRefGoogle Scholar
  48. 48.
    Léveillé, F., Papadia, S., Fricker, M., Bell, K.F., Soriano, F.X., Martel, M.A., Puddifoot, C., Habel, M., Wyllie, D.J., Ikonomidou, C., Tolkovsky, A.M., and Hardingham, G.E., J. Neurosci., 2010, vol. 30, no. 7, pp. 2623–2635.PubMedCrossRefGoogle Scholar
  49. 49.
    Zakharov, V.V. and Mosevitsky, M.I., J. Neurochem., 2007, vol. 101, no. 6, pp. 1539–1551.PubMedCrossRefGoogle Scholar
  50. 50.
    Gulyaeva, N.V., Zhurn. Vyssh. Nervn. Deyat., 2004, vol. 54, no. 4, pp. 437–447.Google Scholar
  51. 51.
    Wu, H.Y. and Lynch, D.R., Mol. Neurobiol., 2006, vol. 33, no. 3, pp. 215–236.PubMedCrossRefGoogle Scholar
  52. 52.
    Zadran, S., Bi, X., and Baudry, M., Mol. Neurobiol., 2010, vol. 42, no. 2, pp. 143–150.PubMedCrossRefGoogle Scholar
  53. 53.
    Zhao, C., Teng, E.M., Summers, R.G., Jr., Ming, G.L., and Gage, F.H., J. Neurosci., 2006, vol. 26, pp. 3–11.PubMedCrossRefGoogle Scholar
  54. 54.
    Ide, Y., Fujiyama, F., Okamoto-Furuta, K., Tamamaki, N., Kaneko, T., and Hisatsune, T., Eur. J. Neurosci., 2008, vol. 28, pp. 2381–2392.PubMedCrossRefGoogle Scholar
  55. 55.
    Winner, B., Melrose, H.L., Zhao, C., Hinkle, K.M., Yue, M., Kent, C., Braithwaite, A.T., Ogholikhan, S., Aigner, R., Winkler, J., Farrer, M.J., and Gage, F.H., Neurobiol. Dis., 2011, vol. 41, pp. 706–716.PubMedCrossRefGoogle Scholar
  56. 56.
    Saegusa, T., Mine, S., Iwasa, H., Murai, H., Seki, T., Yamaura, A., and Yuasa, S., Neurosci. Res., 2004, vol. 48, no. 2, pp. 185–194.PubMedCrossRefGoogle Scholar
  57. 57.
    Carlen, M., Cassidy, R.M., Brismar, H., Smith, G.A., Enquist, L.W., and Frisen, J., Curr. Biol., 2002, vol. 12, pp. 606–608.PubMedCrossRefGoogle Scholar
  58. 58.
    Abrous, D.N. and Koehl, M., Le Moal, M., Physiol. Rev., 2005, vol. 85, pp. 523–569.PubMedCrossRefGoogle Scholar
  59. 59.
    Bonfanti, L., Prog. Neurobiol., 2006, vol. 80, no. 3, pp. 129–164.PubMedCrossRefGoogle Scholar
  60. 60.
    Eadie, B.D., Redila, V.A., and Christie, B.R., J. Comp. Neurol., 2005, vol. 486, pp. 39–47.PubMedCrossRefGoogle Scholar
  61. 61.
    Redila, V.A. and Christie, B.R., Neuroscience, 2006, vol. 137, pp. 1299–1307.PubMedCrossRefGoogle Scholar
  62. 62.
    Ambrogini, P., Cuppini, R., Lattanzi, D., Ciuffoli, S., Frontini, A., and Fanelli, M., Hippocampus, 2010, vol. 20, pp. 799–810.PubMedGoogle Scholar
  63. 63.
    Tronel, S., Fabre, A., Charrier, V., Oliet, S.H., Gage, F.H., and Abrous, D.N., Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 7963–7968.PubMedCrossRefGoogle Scholar
  64. 64.
    Seymour, C.M., Foley, A.G., Murphy, K.J., and Regan, C.M., Neuroscience, 2008, vol. 157, no. 4, pp. 813–820.PubMedCrossRefGoogle Scholar
  65. 65.
    Dityatev, A. and Schachner, M., Nat. Rev. Neurosci., 2003, vol. 4, no. 6, pp. 456–468.PubMedCrossRefGoogle Scholar
  66. 66.
    Gallo, G. and Letourneau, P.C., J. Neurobiol., 2004, vol. 58, no. 1, pp. 92–102.PubMedCrossRefGoogle Scholar
  67. 67.
    Torreano, P.J., Waterman-Storer, C.M., and Cohan, C.S., Cell Motil. Cytoskeleton, 2005, vol. 60, no. 3, pp. 166–179.PubMedCrossRefGoogle Scholar
  68. 68.
    Gallo, G., J. Cell Sci., 2006, vol. 119, no. 16, pp. 3413–3423.PubMedCrossRefGoogle Scholar
  69. 69.
    Brown, J.A. and Bridgman, P.C., Dev. Neurobiol., 2009, vol. 69, no. 10, pp. 633–646.PubMedCrossRefGoogle Scholar
  70. 70.
    Grabham, P.W., Reznik, B., and Goldberg, D.J., J. Cell Sci., 2003, vol. 116, no. 18, pp. 3739–3748.PubMedCrossRefGoogle Scholar
  71. 71.
    Zhou, F.Q. and Cohan, C.S., J. Neurobiol., 2004, vol. 58, no. 1, pp. 84–91.PubMedCrossRefGoogle Scholar
  72. 72.
    Endo, M., Ohashi, K., and Mizuno, K., J. Biol. Chem., 2007, vol. 282, no. 18, pp. 13692–13702.PubMedCrossRefGoogle Scholar
  73. 73.
    Rajnicek, A.M., Foubister, L.E., and McCaig, C.D., J. Cell Sci., 2006, vol. 119, no. 9, pp. 1736–1745.PubMedCrossRefGoogle Scholar
  74. 74.
    Johnson-Venkatesh, E.M. and Umemori, H., Eur. J. Neurosci., 2010, vol. 32, no. 2, pp. 181–190.PubMedCrossRefGoogle Scholar
  75. 75.
    Cassens, C., Kleene, R., Xiao, M.F., Friedrich, C., Dityateva, G., Schafer-Nielsen, C., and Schachner, M., J. Biol. Chem., 2010, vol. 285, no. 37, pp. 28959–28967.PubMedCrossRefGoogle Scholar
  76. 76.
    Kleene, R., Cassens, C., Bähring, R., Theis, T., Xiao, M.F., Dityatev, A., Schafer-Nielsen, C., Döring, F., Wisch-meyer, E., and Schachner, M., J. Biol. Chem., 2010, vol. 285, no. 37, pp. 28968–28979.PubMedCrossRefGoogle Scholar
  77. 77.
    Dityatev, A., Bukalo, O., and Schachner, M., Neuron Glia Biol., 2008, vol. 4, no. 3, pp. 197–209.PubMedCrossRefGoogle Scholar
  78. 78.
    Wu, K.Y., Hengst, U., Cox, L.J., Macosko, E.Z., Jeromin, A., Urquhart, E.R., and Jaffrey, S.R., Nature, 2005, vol. 436, no. 7053, pp. 1020–1024.PubMedCrossRefGoogle Scholar
  79. 79.
    Denny, J.B., Curr. Neuropharmacol., 2006, vol. 4, no. 4, pp. 293–304.PubMedCrossRefGoogle Scholar
  80. 80.
    Ditlevsen, D.K., Povlsen, G.K., Berezin, V., and Bock, E., J. Neurosci. Res., 2008, vol. 86, no. 4, pp. 727–743.PubMedCrossRefGoogle Scholar
  81. 81.
    Dunican, D.J. and Doherty, P., Mol. Cell. Biol. Res. Commun., 2000, vol. 3, no. 5, pp. 255–263.PubMedCrossRefGoogle Scholar
  82. 82.
    Leshchyns’ka, I., Sytnyk, V., Morrow, J.S., and Schachner, M., J. Cell Biol., 2003, vol. 161, no. 3, pp. 625–639.PubMedCrossRefGoogle Scholar
  83. 83.
    Bodrikov, V., Leshchyns’ka, I., Sytnyk, V., Overvoorde, J., Hertog, J., and Schachner, M., J. Cell Biol., 2005, vol. 168, no. 1, pp. 127–139.PubMedCrossRefGoogle Scholar
  84. 84.
    Krucker, T., Siggins, G.R., and Halpain, S., Proc. Natl. Acad. Sci. USA, 2000, vol. 97, no. 12, pp. 6856–6861.PubMedCrossRefGoogle Scholar
  85. 85.
    Chang, S. and De Camilli, P., Nat. Neurosci., 2001, vol. 4, no. 8, pp. 787–793.PubMedCrossRefGoogle Scholar
  86. 86.
    Hansen, S.M., Berezin, V., and Bock, E., Cell Mol. Life Sci., 2008, vol. 65, no. 23, pp. 3809–3821.PubMedCrossRefGoogle Scholar
  87. 87.
    Lee, A.C. and Suter, D.M., Dev. Neurobiol., 2008, vol. 68, no. 12, pp. 1363–1377.PubMedCrossRefGoogle Scholar
  88. 88.
    Bukalo, O., Fentrop, N., Lee, A.Y., Salmen, B., Law, J.W., Wotjak, C.T., Schweizer, M., Dityatev, A., and Schachner, M., J. Neurosci., 2004, vol. 24, no. 7, pp. 1565–1577.PubMedCrossRefGoogle Scholar
  89. 89.
    Büttner, B. and Horstkorte, R., Adv. Exp. Med. Biol., 2010, vol. 663, pp. 55–66.PubMedCrossRefGoogle Scholar
  90. 90.
    Ditlevsen, D.K., Køhler, L.B., Berezin, V., and Bock, E., J. Neurosci. Res., 2007, vol. 85, no. 4, pp. 703–711.PubMedCrossRefGoogle Scholar
  91. 91.
    Francavilla, C., Loeffler, S., Piccini, D., Kren, A., Christofori, G., and Cavallaro, U., J. Cell Sci., 2007, vol. 120, no. 24, pp. 4388–4394.PubMedCrossRefGoogle Scholar
  92. 92.
    Ponimaskin, E., Dityateva, G., Ruonala, M.O., Fukata, M., Fukata, Y., Kobe, F., Wouters, F.S., Delling, M., Bredt, D.S., Schachner, M., and Dityatev, A., J. Neurosci., 2008, vol. 28, no. 36, pp. 8897–8907.PubMedCrossRefGoogle Scholar
  93. 93.
    Gascon, E., Vutskits, L., and Kiss, J.Z., Brain Res. Rev., 2007, vol. 56, no. 1, pp. 101–118.PubMedCrossRefGoogle Scholar
  94. 94.
    Kochlamazashvili, G., Senkov, O., Grebenyuk, S., Robinson, C., Xiao, M.F., Stummeyer, K., GerardySchahn, R., Engel, A.K., Feig, L., Semyanov, A., Suppiramaniam, V., Schachner, M., and Dityatev, A., J. Neurosci., 2010, vol. 30, no. 11, pp. 4171–4183.PubMedCrossRefGoogle Scholar
  95. 95.
    Lopez-Fernandez, M.A., Montaron, M.F., Varea, E., Rougon, G., Venero, C., Abrous, D.N., and Sandi, C., J. Neurosci., 2007, vol. 27, no. 17, pp. 4552–4561.PubMedCrossRefGoogle Scholar
  96. 96.
    Mac-kowiak, M., Chocyk, A., Dudys, D., and Wedzony, K., Neurosci., 2009, vol. 158, no. 4, pp. 1708–1716.CrossRefGoogle Scholar
  97. 97.
    Mazzetti, S., Ortino, B., Inverardi, F., Frassoni, C., and Amadeo, A., Brain Res. Bull., 2007, vol. 71, no. 6, pp. 578–586.PubMedCrossRefGoogle Scholar
  98. 98.
    Markram, K., Gerardy-Schahn, R., and Sandi, C., Neurosci., 2007, vol. 144, no. 3, pp. 788–796.CrossRefGoogle Scholar
  99. 99.
    Conboy, L., Foley, A.G., O’Boyle, N.M., Lawlor, M., Gallagher, H.C., Murphy, K.J., and Regan, C.M., Biochem. Pharmacol., 2009, vol. 77, no. 7, pp. 1254–1265.PubMedCrossRefGoogle Scholar
  100. 100.
    Senkov, O., Sun, M., Weinhold, B., Gerardy-Schahn, R., Schachner, M., and Dityatev, A., J. Neurosci., 2006, vol. 26, no. 42, pp. 10888–10898.PubMedCrossRefGoogle Scholar
  101. 101.
    Mac-kowiak, M., Chocyk, A., Markowicz-Kula, K., and Wedzony, K., Brain Res., 2007, vol. 1148, pp. 43–52.CrossRefGoogle Scholar
  102. 102.
    Bisaz, R., Conboy, L., and Sandi, C., Neurobiol. Learn. Mem., 2009, vol. 91, no. 4, pp. 333–342.PubMedCrossRefGoogle Scholar
  103. 103.
    Bodrikov, V., Sytnyk, V., Leshchyns’ka, I., Hertog, J., and Schachner, M., J. Cell Biol., 2008, vol. 182, no. 6, pp. 1185–1200.PubMedCrossRefGoogle Scholar
  104. 104.
    Kudryashova, I.V., Neirokhimiya, 2007, vol. 24, no. 4, pp. 290–296.Google Scholar
  105. 105.
    Korshunova, I. and Mosevitsky, M., Adv. Exp. Med. Biol., 2010, vol. 663, pp. 169–182.PubMedCrossRefGoogle Scholar
  106. 106.
    Namgung, U., Matsuyama, S., and Routtenberg, A., Proc. Natl. Acad. Sci. USA, 1997, vol. 94, no. 21, pp. 11675–11680.PubMedCrossRefGoogle Scholar
  107. 107.
    Ramakers, G.M., McNamara, R.K., Lenox, R.H., and De Graan, P.N., J. Neurochem., 1999, vol. 73, no. 5, pp. 2175–2183.PubMedGoogle Scholar
  108. 108.
    Hulo, S., Alberi, S., Laux, T., Muller, D., and Caroni, P., Eur. J. Neurosci., 2002, vol. 15, no. 12, pp. 1976–1982.PubMedCrossRefGoogle Scholar
  109. 109.
    Paratcha, G., Furman, M., Bevilaqua, L., Cammarota, M., Vianna, M., de Stein, M.L., Izquierdo, I., and Medina, J.H., Brain Res., 2000, vol. 855, no. 2, pp. 199–205.PubMedCrossRefGoogle Scholar
  110. 110.
    Holahan, M. and Routtenberg, A., Hippocampus, 2008, vol. 18, no. 11, pp. 1099–1102.PubMedCrossRefGoogle Scholar
  111. 111.
    Ou, L.C., Yeh, S.H., and Gean, P.W., Neurobiol. Learn. Mem., 2010, vol. 93, no. 3, pp. 372–382.PubMedCrossRefGoogle Scholar
  112. 112.
    Holahan, M.R., Honegger, K.S., Tabatadze, N., and Routtenberg, A., Learn. Mem., 2007, vol. 14, no. 6, pp. 407–415.PubMedCrossRefGoogle Scholar
  113. 113.
    Venero, C., Tilling, T., Hermans-Borgmeyer, I., Herrero, A.I., Schachner, M., and Sandi, C., J. Neurosci. Res., 2004, vol. 75, no. 2, pp. 172–181.PubMedCrossRefGoogle Scholar
  114. 114.
    Sanchez-Heras, E., Howell, F.V., Williams, G., and Doherty, P., J. Biol. Chem., 2006, vol. 281, no. 46, pp. 35208–35216.PubMedCrossRefGoogle Scholar
  115. 115.
    Huntley, G.W., Gil, O., and Bozdagi, O., Neuroscientist, 2002, vol. 8, no. 3, pp. 221–233.PubMedGoogle Scholar
  116. 116.
    Bozdagi, O., Wang, X.B., Nikitczuk, J.S., Anderson, T.R., Bloss, E.B., Radice, G.L., Zhou, Q., Benson, D.L., and Huntley, G.W., J. Neurosci., 2010, vol. 30, no. 30, pp. 9984–9989.PubMedCrossRefGoogle Scholar
  117. 117.
    Edsbagge, J., Zhu, S., Xiao, M.Y., Wigström, H., Mohammed, A.H., and Semb, H., Mol. Cell Neurosci., 2004, vol. 25, no. 3, pp. 524–535.PubMedCrossRefGoogle Scholar
  118. 118.
    Huang, Z., Shimazu, K., Woo, N.H., Zang, K., Müller, U., Lu, B., and Reichardt, L.F., J. Neurosci., 2006, vol. 26, no. 43, pp. 11208–11219.PubMedCrossRefGoogle Scholar
  119. 119.
    Chan, C.S., Levenson, J.M., Mukhopadhyay, P.S., Zong, L., Bradley, A., Sweatt, J.D., and Davis, R.L., Learn. Mem., 2007, vol. 14, no. 9, pp. 606–615.PubMedCrossRefGoogle Scholar
  120. 120.
    Kramár, E.A., Lin, B., Rex, C.S., Gall, C.M., and Lynch, G., Proc. Natl. Acad. Sci. USA, 2006, vol. 103, no. 14, pp. 5579–5584.PubMedCrossRefGoogle Scholar
  121. 121.
    Dahlhaus, R., Hines, R.M., Eadie, B.D., Kannangara, T.S., Hines, D.J., Brown, C.E., Christie, B.R., and El-Husseini, A., Hippocampus, 2010, vol. 20, no. 2, pp. 305–322.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  1. 1.Institute of Higher Nervous Activity and NeurophysiologyRussian Academy of SciencesMoscowRussia

Personalised recommendations