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The plasticity of inhibitory synapses as a factor of long-term modifications

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Abstract

We review the current data on the functions of GABAergic inhibition in the mechanisms of long-term plasticity that underlie learning and memory. We present the main principles of the organization of the inhibitory inputs and molecular composition of synapses. So-called “ionic plasticity” is a specific feature of the inhibitory synapses. The range of ionic plasticity that is associated with the depolarizing effect of GABA is of particular interest. In adult animals, this effect is observed after high-frequency stimulation of synaptic inputs. The main attention was focused on the reaction of disinhibition in the hippocampus that is induced by high-frequency stimulation of the afferent inputs that are used for LTP induction. We argue that the disinhibition effect is crucially important for more effective consolidation of long-term modifications, including structural plasticity.

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References

  1. Capogna, M. and Pearce, R.A., Trend. Neurosci., 2011, vol. 34, pp. 101–112.

    CAS  PubMed  Google Scholar 

  2. Willadt, S., Nenniger, M., and Vogt, K.E., PLoS One, 2013, vol. 8, p. 11.

    Google Scholar 

  3. Kremkow, J., Aertsen, A., and Kumar, A., J. Neurosci., 2010, vol. 30, pp. 15760–15768.

    CAS  PubMed  Google Scholar 

  4. Klausberger, T. and Somogyi, P., Science, 2008, vol. 321, pp. 53–57.

    PubMed Central  CAS  PubMed  Google Scholar 

  5. Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., and Wu, C., Nat. Rev. Neurosci., 2004, vol. 5, pp. 793–807.

    CAS  PubMed  Google Scholar 

  6. Kole, M.H.P. and Stuart, G.J., Neuron, 2012, vol. 73, pp. 235–247.

    CAS  PubMed  Google Scholar 

  7. Gidon, A. and Segev, I., Neuron, 2012, vol. 75, pp. 330–341.

    CAS  PubMed  Google Scholar 

  8. Chen, J.L., Villa, K.L., Cha, J.W., So, P.T., Kubota, Y., and Nedivi, E., Neuron, 2012, vol. 74, pp. 361–373.

    PubMed Central  CAS  PubMed  Google Scholar 

  9. Müller, C., Beck, H., Coulter, D., and Remy, S., Neuron, 2012, vol. 75, pp. 851–864.

    PubMed  Google Scholar 

  10. Lovett-Barron, M., Turi, G.F., Kaifosh, P., Lee, P.H., Bolze, F., Sun, X.-H., Nicoud, J.F., Zemelman, B.V., Sternson, S.M., and Losonczy, A., Nat. Neurosci., 2012, vol. 15, pp. 423–430.

    CAS  PubMed  Google Scholar 

  11. Jiang, X., Wang, G., Lee, A.J., Stornetta, R.L., and Zhu, J.J., Nat. Neurosci., 2013, vol. 16, pp. 210–220.

    PubMed Central  CAS  PubMed  Google Scholar 

  12. Klausberger, T., Eur. J. Neurosci., 2009, vol. 30, no. 6, pp. 947–957.

    PubMed  Google Scholar 

  13. Ormond, J. and Woodin, M.A., PLoS One, 2009, vol. 4, p. e7224.

    Google Scholar 

  14. Boyken, J., Grønborg, M., Riedel, D., Urlaub, H., Jahn, R., and Chua, J.J.E., Neuron, 2013, vol. 78, pp. 285–297.

    CAS  PubMed  Google Scholar 

  15. Buddhala, C., Hsu, C.C., and Wu, J.Y., Neurochem. Int., 2009, vol. 55, pp. 9–12.

    CAS  PubMed  Google Scholar 

  16. Rose, T., Schoenenberger, P., Jezek, K., and Oertner, T.G., Neuron, 2013, vol. 77, pp. 1109–1121.

    CAS  PubMed  Google Scholar 

  17. Raingo, J., Khvotchev, M., Liu, P., Darios, F., Li, Y.C., Ramirez, D.M., Adachi, M., Lemieux, P., Toth, K., Davletov, B., and Kavalali, E.T., Nat. Neurosci., 2012, vol. 15, no. 5, pp. 738–745.

    PubMed Central  CAS  PubMed  Google Scholar 

  18. Maximov, A. and Sudhof, T.C., Neuron, 2005, vol. 48, pp. 547–554.

    CAS  PubMed  Google Scholar 

  19. Scimemi, A., Semyanov, A., Sperk, G., Kullmann, D.M., and Walker, M.C., J. Neurosci., 2005, vol. 25, pp. 10016–10024.

    CAS  PubMed  Google Scholar 

  20. Lee, S., Yoon, B.E., Berglund, K., Oh, S.J., Park, H., Shin, H.S., Augustine, G.J., and Lee, C.J., Science, 2010, vol. 330, no. 6005, pp. 790–796.

    CAS  PubMed  Google Scholar 

  21. Angulo, M.C., Le Meur, K., Kozlov, A.S., Charpak, S., and Audinat, E., Prog. Neurobiol., 2008, vol. 86, pp. 297–303.

    CAS  PubMed  Google Scholar 

  22. Kersante, F., Rowley, S.C., Pavlov, I., Gutierrez-Mecinas, M., Semyanov, A., Reul, J.M., Walker,M.C., and Linthorst, A.C., J. Physiol., 2013, vol. 591, no. 10, pp. 2429–2441.

    PubMed Central  CAS  PubMed  Google Scholar 

  23. Wu, Y., Wang, W., Diez-Sampedro, A., and Richerson, G.B., Neuron, 2007, vol. 56, pp. 851–865.

    PubMed Central  CAS  PubMed  Google Scholar 

  24. Moss, F.J., Imoukhuede, P.I., Scott, K., Hu, J., Jankowsky, J.L., Quick, M.W., and Lester, H.A., J. Gen. Physiol., 2009, vol. 134, no. 6, pp. 489–521.

    PubMed Central  CAS  PubMed  Google Scholar 

  25. Soragna, A., Bossi, E., Giovannardi, S., Pisani, R., and Peres, A., Cell. Mol. Life Sci., 2005, vol. 62, pp. 2877–2885.

    CAS  PubMed  Google Scholar 

  26. Engel, D., Schmitz, D., Gloveli, T., Frahm, C., Heinemann, U., and Draguhn, A., J. Physiol., 1998, vol. 512, no. 3, pp. 643–649.

    PubMed Central  CAS  PubMed  Google Scholar 

  27. Overstreet, L.S. and Westbrook, G.L., J. Neurosci., 2003, vol. 23, pp. 2618–2626.

    CAS  PubMed  Google Scholar 

  28. Glykys, J. and Mody, I., J. Physiol., 2007, vol. 582, pp. 1163–1178.

    PubMed Central  CAS  PubMed  Google Scholar 

  29. Beenhakker, M.P. and Huguenard, J.R., J. Neurosci., 2010, vol. 30, pp. 15262–15276.

    PubMed Central  CAS  PubMed  Google Scholar 

  30. Heja, L., Nyitrai, G., Kekesi, O., Dobolyi, A., Szabo, P., Fiath, R., Ulbert, I., Pál-Szenthe, B., Palkovits, M., and Kardos, J., BMC Biol., 2012, vol. 10, p. 26.

    PubMed Central  CAS  PubMed  Google Scholar 

  31. Vithlani, M., Terunuma, M., and Moss, S.J., Physiol. Rev., 2011, vol. 91, pp. 1009–1022.

    PubMed Central  CAS  PubMed  Google Scholar 

  32. Fang, C., Deng, L., Keller, C.A., Fukata, M., Fukata, Y., Chen, G., and Luscher, B., J. Neurosci., 2006, vol. 26, no. 49, pp. 12758–12768.

    PubMed Central  CAS  PubMed  Google Scholar 

  33. Tyagarajan, S.K. and Fritschy, J.M., Nat. Rev. Neurosci., 2014, vol. 15, pp. 141–156.

    CAS  PubMed  Google Scholar 

  34. Fritschy, J. and Panzanelli, P., Eur. J. Neurosci., 2014, vol. 39, pp. 1845–1865.

    PubMed  Google Scholar 

  35. Kuzirian, M.S., Moore, A.R., Staudenmaier, E.K., Friedel, R.H., and Paradis, S., J. Neurosci., 2013, vol. 33, pp. 8961–8973.

    PubMed Central  CAS  PubMed  Google Scholar 

  36. Blaesse, P., Airaksinen, M.S., Rivera, C., and Kaila, K., Neuron, 2009, vol. 61, pp. 820–838.

    CAS  PubMed  Google Scholar 

  37. Rinke, I., Artmann, J., and Stein, V., J. Neurosci., 2010, vol. 30, pp. 4776–4786.

    CAS  PubMed  Google Scholar 

  38. Bogdanov, Y., Michels, G., Armstrong-Gold, C., Haydon, P., Lindstrom, J., Pangalos, M., and Moss, S., EMBO J., 2006, vol. 25, pp. 4381–4389.

    PubMed Central  CAS  PubMed  Google Scholar 

  39. Vogels, T.P., Sprekeler, H., Zenke, F., Clopath, C., and Gerstner, W., Science, 2011, vol. 334, pp. 1569–1573.

    CAS  PubMed  Google Scholar 

  40. Hartman, K.N., Pal, S.K., Burrone, J., and Murthy, V.N., Nat. Neurosci., 2006, vol. 9, pp. 642–649.

    CAS  PubMed  Google Scholar 

  41. Kullmann, D.M., Moreau, A.W., Bakiri, Y., and Nicholson, E., Neuron, 2012, vol. 75, pp. 951–962.

    CAS  PubMed  Google Scholar 

  42. Castillo, P.E., Chiu, C.Q., and Carroll, R.C., Curr. Opin. Neurobiol., 2011, vol. 21, pp. 328–338.

    PubMed Central  CAS  PubMed  Google Scholar 

  43. Rannals, M.D. and Kapur, J., J. Neurosci., 2011, vol. 31, pp. 17701–17712.

    PubMed Central  CAS  PubMed  Google Scholar 

  44. Luscher, B., Fuchs, T., and Kilpatrick, C.L., Neuron, 2011, vol. 70, pp. 385–409.

    PubMed Central  CAS  PubMed  Google Scholar 

  45. Abramian, A.M., Comenencia-Ortiz, E., Vithlani, M., Tretter, E.V., Sieghart, W., Davies, P.A., and Moss, S.J., J. Biol. Chem., 2010, vol. 285, no. 53, pp. 41795–41805.

    PubMed Central  CAS  PubMed  Google Scholar 

  46. Petrini, E.M., Ravasenga, T., Hausrat, T.J., Iurilli, G., Olcese, U., Racine, V., Sibarita, J.B., Jacob, T.C., Moss, S.J., Benfenati, F., Medini, P., Kneussel, M., and Barberis, A., Nat. Commun., 2014, vol. 5, p. 3921.

    PubMed Central  CAS  PubMed  Google Scholar 

  47. Saliba, R.S., Kretschmannova, K., and Moss, S.J., EMBO J., 2012, vol. 31, pp. 2937–2951.

    PubMed Central  CAS  PubMed  Google Scholar 

  48. Bright, D.P. and Smart, T.G., Eur. J. Neurosci, 2013, vol. 38, pp. 3408–3423.

    PubMed Central  PubMed  Google Scholar 

  49. Kittler, J.T. and Moss, S.J., Curr. Opin. Neurobiol., 2003, vol. 13, pp. 341–347.

    CAS  PubMed  Google Scholar 

  50. Muir, J., Arancibia-Carcamo, I.L., MacAskill, A.F., Smith, K.R., Griffin, L.D., and Kittler, J.T., Proc. Natl. Acad. Sci. USA, 2010, vol. 107, no. 38, pp. 16679–16684.

    PubMed Central  CAS  PubMed  Google Scholar 

  51. Bannai, H., Levi, S., Schweizer, C., Inoue, T., Launey, T., Racine, V., Sibarita, J.B., Mikoshiba, K., and Triller, A., Neuron, 2009, vol. 62, pp. 670–682.

    CAS  PubMed  Google Scholar 

  52. Marsden, K.C., Beattie, J.B., Friedenthal, J., and Carroll, R.C., J. Neurosci., 2007, vol. 27, no. 52, pp. 14326–14337.

    CAS  PubMed  Google Scholar 

  53. Arancibia-Cárcamo, L., Yuen, E.Y., Muir, J., Lumb, M.J., Michels, G., Saliba, R.S., Smart, T.G., Yan, Zh., Kittler, J.T., and Moss, S.J., Proc. Natl. Acad. Sci. USA, 2009, vol. 106, no. 41, pp. 17552–17557.

    PubMed Central  PubMed  Google Scholar 

  54. Kittler, J.T., Chen, G., Kukhtina, V., Vahedi-Faridi, A., Gu, Z., Tretter, V., Smith, K.R., McAinsh, K., Arancibia-Carcamo, I.L., Saenger, W., Haucke, V., Yan, Z., and Moss, S.J., Proc. Natl. Acad. Sci. USA, 2008, vol. 105, no. 9, pp. 3616–3621.

    PubMed Central  CAS  PubMed  Google Scholar 

  55. Vlachos, A., Reddy-Alla, S., Papadopoulos, T., Deller, T., and Betz, H., Cereb. Cortex, 2013, vol. 23, pp. 2700–2711.

    PubMed  Google Scholar 

  56. Lushnikova, I., Skibo, G., Muller, D., and Nikonenko, I., Neuropharmacology, 2011, vol. 60, pp. 757–764.

    CAS  PubMed  Google Scholar 

  57. Specht, C.G., Izeddin, I., Rodriguez, P.C., El Beheiry, M., Rostaing, P., Darzacq, X., Dahan, M., and Triller, A., Neuron, 2013, vol. 79, no. 2, pp. 308–321.

    CAS  PubMed  Google Scholar 

  58. Hanus, C., Ehrensperger, M.-V., and Triller, A., J. Neurosci., 2006, vol. 26, pp. 4586–4595.

    CAS  PubMed  Google Scholar 

  59. Tyagarajan, S.K., Ghosh, H., Yevenes, G.E., Nikonenko, I., Ebeling, C., Schwerdel, C., Sidler, C., Zeilhofer, H.U., Gerrits, B., Muller, D., and Fritschy, J.M., Proc. Natl. Acad. Sci. USA, 2011, vol. 108, pp. 379–384.

    PubMed Central  CAS  PubMed  Google Scholar 

  60. Tyagarajan, S.K., Ghosh, H., Yévenes, G.E., Imanishi, S.Y., Zeilhofer, H.U., Gerrits, B., and Fritschy, J.M., J. Biol. Chem., 2013, vol. 288, pp. 9634–9647.

    PubMed Central  CAS  PubMed  Google Scholar 

  61. Bausen, M., Weltzien, F., Betz, H., and O’Sullivan, G.A., Mol. Cell. Neurosci., 2010, vol. 44, pp. 201–209.

    CAS  PubMed  Google Scholar 

  62. Dejanovic, B., Semtner, M., Ebert, S., Lamkemeyer, T., Neuser, F., Lüscher, B., Meier, J.C., and Schwarz, G., PLoS Biol., 2014, vol. 12, no. 7.

    Google Scholar 

  63. Dejanovic, B. and Schwarz, G., J. Neurosci., 2014, vol. 34, pp. 7763–7768.

    CAS  PubMed  Google Scholar 

  64. Peng, Y.-R., Zeng, S.-Y., Song, H.-L., Li, M.-Y., Yamada, M.K., and Yu, X., J. Neurosci., 2010, vol. 30, pp. 16220–16231.

    CAS  PubMed  Google Scholar 

  65. Sihra, T.S. and Rodriguez-Moreno, A., Adv. Exp. Med. Biol., 2011, vol. 717, pp. 1–10.

    CAS  PubMed  Google Scholar 

  66. Chen, A., Nguyen, C., Copenhagen, D., Badurek, S., Minichiello, L., Ranscht, B., and Reichardt, L., J. Neurosci., 2011, vol. 31, pp. 2769–2780.

    PubMed Central  CAS  PubMed  Google Scholar 

  67. Gottmann, K., Lessmann, V., and Mittmann, T., Exp. Brain Res., 2009, vol. 199, pp. 203–234.

    CAS  PubMed  Google Scholar 

  68. Hablitz, J.J., Mathew, S.S., and Pozzo-Miller, L., Neuroscientist, 2009, vol. 15, no. 3, pp. 218–224.

    PubMed Central  CAS  PubMed  Google Scholar 

  69. Pitler, T.A. and Alger, B.E., J. Physiol., 1992, vol. 450, pp. 127–142.

    PubMed Central  CAS  PubMed  Google Scholar 

  70. Cui, Y., Costa, R.M., Murphy, G.G., Elgersma, Y., Zhu, Y., Gutmann, D.H., Parada, L.F., Mody, I., and Silva, A.J., Cell, 2008, vol. 135, no. 3, pp. 549–560.

    PubMed Central  CAS  PubMed  Google Scholar 

  71. Cunha, R.A. and Ribeiro, J.A., Neuropharmacology, 2000, vol. 39, pp. 1156–1167.

    CAS  PubMed  Google Scholar 

  72. Tarasenko, A., Krupko, O., and Himmelreich, N., Biochim. Biophys. Acta, 2014, vol. 1840, pp. 1923–1932.

    CAS  PubMed  Google Scholar 

  73. McBain, C.J. and Kauer, J.A., Curr. Opin. Neurobiol., 2009, vol. 19, pp. 254–262.

    PubMed Central  CAS  PubMed  Google Scholar 

  74. Kim, J. and Alger, B.E., Nat. Neurosci., 2010, vol. 13, pp. 592–600.

    PubMed Central  CAS  PubMed  Google Scholar 

  75. Fu, Y. and Huang, Z.J., Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 22699–22704.

    PubMed Central  CAS  PubMed  Google Scholar 

  76. Futai, K., Doty, C.D., Baek, B., Ryu, J., and Sheng, M., J. Neurosci., 2013, vol. 33, pp. 3612–3623.

    CAS  PubMed  Google Scholar 

  77. Woo, J., Kwon, S.-K., Nam, J., Choi, S., Takahashi, H., Krueger, D., Park, J., Lee, Y., Bae, J.Y., Lee, D., Ko, J., Kim, H., Kim, M.H., Bae, Y.C., Chang, S., Craig, A.M., and Kim, E., J. Cell Biol., 2013, vol. 201, no. 6, pp. 929–944.

    PubMed Central  CAS  PubMed  Google Scholar 

  78. Sarto-Jackson, I., Milenkovic, I., Smalla, K.-H., Gundelfinger, E.D., Kaehne, T., Herrera-Molina, R., Thomas, S., Kiebler, M.A., and Sieghart, W., J. Biol. Chem., 2012, vol. 287, no. 17, pp. 14201–14214.

    PubMed Central  CAS  PubMed  Google Scholar 

  79. Fazzari, P., Paternain, A.V., Valiente, M., Pla, R., Luján, R., Lloyd, K., Lerma, J., Marín, O., and Rico, B., Nature, 2010, vol. 464, no. 7293, pp. 1376–1380.

    CAS  PubMed  Google Scholar 

  80. Brennaman, L.H., Zhang, X., Guan, H., Triplett, J.W., Brown, A., Demyanenko, G.P., Manis, P.B., Landmesser, L., and Maness, P.F., Cereb. Cortex, 2013, vol. 23, no. 1, pp. 162–177.

    PubMed Central  PubMed  Google Scholar 

  81. Lee, K., Kim, Y., Lee, S.-J., Qiang, Y., Lee, D., Lee, H.W., Kim, H., Je, H.S., Südhof, T.C., and Ko, J., Proc. Natl. Acad. Sci. USA, 2013, vol. 110, pp. 336–341.

    PubMed Central  CAS  PubMed  Google Scholar 

  82. Raissi, A.J., Staudenmaier, E.K., David, S., Hu, L., and Paradis, S., Mol. Cell. Neurosci., 2013, vol. 57C, pp. 23–32.

    CAS  PubMed  Google Scholar 

  83. Huang, Z.J., J. Physiol., 2009, vol. 587, no. 9, pp. 1881–1888.

    PubMed Central  CAS  PubMed  Google Scholar 

  84. Lau, C.G. and Murthy, V.N., J. Neurosci., 2012, vol. 32, no. 25, pp. 8521–8531.

    PubMed Central  CAS  PubMed  Google Scholar 

  85. Gierdalski, M., Jablonska, B., Siucinska, E., Lech, M., Skibinska, A., and Kossut, M., Cereb. Cortex, 2001, vol. 11, pp. 806–815.

    CAS  PubMed  Google Scholar 

  86. Kinney, J.W., Davis, C.N., Tabarean, I., Conti, B., Bartfai, T., and Behrens, M.M., J. Neurosci., 2006, vol. 26, pp. 1604–1615.

    CAS  PubMed  Google Scholar 

  87. Henneberger, C., Kirischuk, S., and Grantyn, R., Neuroscience, 2005, vol. 135, pp. 749–763.

    CAS  PubMed  Google Scholar 

  88. Deken, S.L., Wang, D., and Quick, M.W., J. Neurosci., 2003, vol. 23, pp. 1563–1568.

    CAS  PubMed  Google Scholar 

  89. Mathews, G.C. and Diamond, J.S., J. Neurosci., 2003, vol. 23, pp. 2040–2048.

    CAS  PubMed  Google Scholar 

  90. Cristóvão-Ferreira, S., Vaz, S.H., Ribeiro, J.A., and Sebastião, A.M., J. Neurochem., 2009, vol. 109, pp. 336–347.

    PubMed  Google Scholar 

  91. Beckman, M.L., Bernstein, E.M., and Quick, M.W., J. Neurosci., 1999, vol. 19.

  92. Law, R.M., Stafford, A., and Quick, M.W., J. Biol. Chem., 2000, vol. 275, pp. 23986–23991.

    CAS  PubMed  Google Scholar 

  93. Whitworth, T.L. and Quick, M.W., J. Biol. Chem., 2001, vol. 276, pp. 42932–42937.

    CAS  PubMed  Google Scholar 

  94. Imoukhuede, P.I., Moss, F.J., Michael, D.J., Chow, R.H., and Lester, H.A., Biophys. J., 2009, vol. 96, pp. 2949–2960.

    PubMed Central  CAS  PubMed  Google Scholar 

  95. Wang, D. and Quick, M.W., J. Biol. Chem., 2005, vol. 280, pp. 18703–18709.

    CAS  PubMed  Google Scholar 

  96. Hartmann, K., Bruehl, C., Golovko, T., and Draguhn, A., PLoS One, 2008, vol. 3.

  97. Rivera, C., Voipio, J., and Kaila, K., J Physiol., 2005, vol. 562, no. 1, pp. 27–36.

    PubMed Central  CAS  PubMed  Google Scholar 

  98. Woodin, M.A., Ganguly, K., and Poo, M., Neuron, 2003, vol. 39, pp. 807–820.

    CAS  PubMed  Google Scholar 

  99. Lamsa, K.P. and Taira, T., J. Neurophysiol., 2003, vol. 90, no. 3, pp. 1983–1995.

    CAS  PubMed  Google Scholar 

  100. Doyon, N., Prescott, S.A., Castonguay, A., Godin, A.G., Kröger, H., and De Koninck, Y., PLoS Comput. Biol., 2011, vol. 7.

  101. Farrant, M. and Kaila, K., Prog. Brain Res., 2007, vol. 160, pp. 59–87.

    CAS  PubMed  Google Scholar 

  102. Jedlicka, P., Deller, T., and Gutkin, B., Hippocampus, 2011, vol. 898, pp. 885–898.

    Google Scholar 

  103. Smirnov, S., Paalasmaa, P., Uusisaari, M., Voipio, J., and Kaila, K., J. Neurosci., 1999, vol. 19, pp. 9252–9260.

    CAS  PubMed  Google Scholar 

  104. Fiumelli, H., Cancedda, L., and Poo, M.-M., Neuron, 2005, vol. 48, pp. 773–786.

    CAS  PubMed  Google Scholar 

  105. Saraga, F., Balena, T., Wolansky, T., Dickson, C.T., and Woodin, M.A., Neuroscience, 2008, vol. 155, pp. 64–75.

    CAS  PubMed  Google Scholar 

  106. Wright, R., Raimondo, J.V., and Akerman, C.J., Neural. Plasticity, 2011, vol. 2011, p. 728395.

    PubMed Central  CAS  PubMed  Google Scholar 

  107. Chiang, P.-H., Wu, P.-Y., Kuo, T.-W., Liu, Y.-C., Chan, C.-F., Chien, T.-C., Cheng, J.K., Huang, Y.Y., Chiu, C.D., and Lien, C.C., J. Neurosci., 2012, vol. 32, no. 1, pp. 62–67.

    CAS  PubMed  Google Scholar 

  108. Viitanen, T., Ruusuvuori, E., Kaila, K., and Voipio, J., J. Physiol., 2010, vol. 588, pp. 1527–1540.

    PubMed Central  CAS  PubMed  Google Scholar 

  109. Kaila, K., Lamsa, K., Smirnov, S., Taira, T., and Voipio, J., J. Neurosci., 1997, vol. 17, no. 20, pp. 7662–7672.

    CAS  PubMed  Google Scholar 

  110. Kuriu, T., Yanagawa, Y., and Konishi, S., Mol. Cell. Neurosci., 2012, vol. 49, pp. 184–195.

    CAS  PubMed  Google Scholar 

  111. Dobie, F.A. and Craig, A.M., J. Neurosci., 2011, vol. 31, pp. 10481–10493.

    CAS  PubMed  Google Scholar 

  112. Pribiag, H., Peng, H., Shah, W.A., Stellwagen, D., and Carbonetto, S., Proc. Natl. Acad. Sci. USA, 2014, vol. 111, pp. 6810–6815.

    PubMed Central  CAS  PubMed  Google Scholar 

  113. Bourne, J.N. and Harris, K.M., Hippocampus, 2011, vol. 21, pp. 354–373.

    PubMed Central  CAS  PubMed  Google Scholar 

  114. Bloodgood, B.L., Sharma, N., Browne, H.A., Trepman, A.Z., and Greenberg, M.E., Nature, 2013, vol. 503, pp. 121–125.

    PubMed Central  CAS  PubMed  Google Scholar 

  115. Kohara, K., Yasuda, H., Huang, Y., Adachi, N., Sohya, K., and Tsumoto, T., J. Neurosci., 2007, vol. 27, pp. 7234–7244.

    CAS  PubMed  Google Scholar 

  116. Jovanovic, J.N., Thomas, P., Kittler, J.T., Smart, T.G., and Moss, S.J., J. Neurosci., 2004, vol. 24, pp. 522–530.

    CAS  PubMed  Google Scholar 

  117. Wang, L. and Maffei, A., J. Neurosci., 2014, vol. 34, pp. 1083–1093.

    PubMed Central  CAS  PubMed  Google Scholar 

  118. Storozhuk, M.V., Ivanova, S.Y., Pivneva, T.A., Melnick, I.V., Skibo, G.G., Belan, P.V., and Kostyuk, P.G., Neurosci. Let., 2002, vol. 323, no. 1, pp. 5–8.

    CAS  Google Scholar 

  119. Ivenshitz, M. and Segal, M., J. Neurosci., 2006, vol. 26, pp. 1199–1210.

    CAS  PubMed  Google Scholar 

  120. McMahon, L.L. and Kauer, J.A., Neuron, 1997, vol. 18, pp. 295–305.

    CAS  PubMed  Google Scholar 

  121. Kullmann, D.M. and Lamsa, K.P., Nat. Rev. Neurosci., 2007, vol. 8, pp. 687–699.

    CAS  PubMed  Google Scholar 

  122. Wang, J., Liu, S., Haditsch, U., Tu, W., Cochrane, K., Ahmadian, G., Tran, L., Paw, J., Wang, Y., Mansuy, I.M., Salter, M., and Lu, Y.M., J. Neurosci., 2003, vol. 23, pp. 826–836.

    CAS  PubMed  Google Scholar 

  123. Marsden, K.C., Shemesh, A., Bayer, K.U., and Carroll, R.C., Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 20559–20564.

    PubMed Central  CAS  PubMed  Google Scholar 

  124. Tanaka, T., Saito, H., and Matsuki, N., J. Neurosci., 1997, vol. 17, no. 9, pp. 2959–2966.

    CAS  PubMed  Google Scholar 

  125. Niwa, F., Bannai, H., Arizono, M., Fukatsu, K., Triller, A., and Mikoshiba, K., PLoS ONE, 2012, vol. 7.

  126. Chamma, I., Heubl, M., Chevy, Q., Renner, M., Moutkine, I., Eugene, E., Poncer, J., and Levi, S., J. Neurosci., 2013, vol. 33, pp. 15488–15503.

    CAS  PubMed  Google Scholar 

  127. Puskarjov, M., Ahmad, F., Kaila, K., and Blaesse, P., J. Neurosci., 2012, vol. 32, pp. 11356–11364.

    CAS  PubMed  Google Scholar 

  128. Lee, H., Deeb, T., Walker, J., Davies, P., and Moss, S., Nat. Neurosci., 2011, vol. 14, pp. 736–743.

    PubMed Central  CAS  PubMed  Google Scholar 

  129. Wang, W., Gong, N., and Xu, T.L., Biochem. Biophys. Res. Commun., 2006, vol. 343, pp. 1209–1215.

    CAS  PubMed  Google Scholar 

  130. Vithlani, M., Hines, R., Zhong, P., Terunuma, M., Hines, D., Revilla-Sanchez, R., Jurd, R., Haydon, P., Rios, M., Brandon, N., Yan, Z., and Moss, S., J. Neurosci., 2013, vol. 33, pp. 15567–15577.

    PubMed Central  CAS  PubMed  Google Scholar 

  131. Pilter, T.A. and Alger, B.E., Neuron, 1994, vol. 13, pp. 1447–1455.

    Google Scholar 

  132. McBain, C.J., Prog. Brain. Res., 2008, vol. 169, pp. 225–240.

    PubMed Central  CAS  PubMed  Google Scholar 

  133. Pelkey, K.A., Lavezzari, G., Racca, C., Roche, K.W., and McBain, C.J., Neuron, 2005, vol. 46, pp. 89–102.

    CAS  PubMed  Google Scholar 

  134. Pelkey, K.A., Topolnik, L., Yuan, X.Q., Lacaille, J.C., and McBain, C.J., Neuron, 2008, vol. 60, pp. 980–987.

    PubMed Central  CAS  PubMed  Google Scholar 

  135. Wierenga, C.J., Becker, N., and Bonhoeffer, T., Nat. Neurosci., 2008, vol. 11, pp. 1044–1052.

    CAS  PubMed  Google Scholar 

  136. Chen, J.L., Lin, W.C., Cha, J.W., So, P.T., Kubota, Y., and Nedivi, E., Nat. Neurosci., 2011, vol. 14, pp. 587–594.

    PubMed Central  CAS  PubMed  Google Scholar 

  137. Froemke, R.C., Merzenich, M.M., and Schreiner, C.E., Nature, 2007, vol. 450, pp. 425–429.

    CAS  PubMed  Google Scholar 

  138. Kleschevnikov, A.M., Belichenko, P.V., Villar, A.J., Epstein, C.J., Malenka, R.C., and Mobley, W.C., J. Neurosci., 2004, vol. 24, pp. 8153–8160.

    CAS  PubMed  Google Scholar 

  139. Shen, H., Sabaliauskas, N., Sherpa, A., Fenton, A.A., Stelzer, A., Aoki, C., and Smith, S.S., Science, 2010, vol. 327, no. 5972, pp. 1515–1518.

    PubMed Central  CAS  PubMed  Google Scholar 

  140. Matsuyama, S., Taniguchi, T., Kadoyama, K., and Matsumoto, A., Neuroreport, 2008, vol. 19, pp. 1809–1813.

    CAS  PubMed  Google Scholar 

  141. Arima-Yoshida, F., Watabe, A.M., and Manabe, T., Eur. J. Neurosci., 2011, vol. 33, pp. 1637–1646.

    PubMed  Google Scholar 

  142. Balena, T. and Woodin, M.A., Eur. J. Neurosci., 2008, vol. 27, pp. 2402–2412.

    PubMed  Google Scholar 

  143. Wakita, M., Kotani, N., Kogure, K., and Akaike, N., J. Pharmacol. Exp. Ther., 2013, vol. 348, pp. 246–259.

    PubMed  Google Scholar 

  144. Farmer, L.M., Le, B.N., and Nelson, D.J., J. Physiol., 2013, vol. 591, pp. 1001–1015.

    PubMed Central  CAS  PubMed  Google Scholar 

  145. Xu, J.Y. and Sastry, B.R., Exp. Neurol., 2007, vol. 204, pp. 836–839.

    PubMed Central  CAS  PubMed  Google Scholar 

  146. Kanemoto, Y., Matsuzaki, M., Morita, S., Hayama, T., Noguchi, J., Senda, N., Momotake, A., Arai, T., and Kasai, H., PLoS ONE, 2011, vol. 6, no. 7, p. 22652.

    Google Scholar 

  147. Paille, V., Fino, E., Du, K., Morera-Herreras, T., Perez, S., Kotaleski, J.H., and Venance, L., J. Neurosci., 2013, vol. 33, no. 22, pp. 9353–9363.

    CAS  PubMed  Google Scholar 

  148. Hayama, T., Noguchi, J., Watanabe, S., Takahashi, N., Hayashi-Takagi, A., Ellis-Davies, G.C., Matsuzaki, M., and Kasai, H., Nat. Neurosci., 2013, vol. 16, no. 10, pp. 1409–1416.

    PubMed Central  CAS  PubMed  Google Scholar 

  149. Thompson, S.M. and Gahwiler, B.H., J. Neurophysiol., 1989, vol. 61, no. 3, pp. 512–523.

    CAS  PubMed  Google Scholar 

  150. Ben-Ari, Y., Gaiarsa, J.L., Tyzio, R., and Khazipov, R., Physiol. Rev., 2007, vol. 87, pp. 1215–1284.

    CAS  PubMed  Google Scholar 

  151. Kuczewski, N., Fuchs, C., Ferrand, N., Jovanovic, J.N., Gaiarsa, J.L., and Porcher, C., J. Neurochem., 2011, vol. 118, pp. 533–545.

    CAS  PubMed  Google Scholar 

  152. Marty, S., Berninger, B., Carroll, P., and Thoenen, H., Neuron, 1996, vol. 16, pp. 565–570.

    CAS  PubMed  Google Scholar 

  153. Bony, G., Szczurkowska, J., Tamagno, I., Shelly, M., Contestabile, A., and Cancedda, L., Nat. Commun., 2013, vol. 4, p. 1800.

    PubMed  Google Scholar 

  154. Cancedda, L., Fiumelli, H., Chen, K., and Poo, M.M., J. Neurosci., 2007, vol. 27, pp. 5224–5235.

    CAS  PubMed  Google Scholar 

  155. Lee, H., Lee, D., Park, C.H., Ho, W.K., and Lee, S.H., Eur. J. Neurosci, 2012, vol. 36, pp. 2743–2752.

    PubMed  Google Scholar 

  156. He, S., Ma, J., Liu, N., and Yu, X., J. Neurosci., 2010, vol. 30, pp. 7910–7916.

    CAS  PubMed  Google Scholar 

  157. Giachino, C., Barz, M., Tchorz, J.S., Tome, M., Gassmann, M., Bischofberger, J., Bettler, B., and Taylor, V., Development, 2014, vol. 141, no. 1, pp. 83–90.

    CAS  PubMed  Google Scholar 

  158. Chancey, J.H., Adlaf, E.W., Sapp, M.C., Pugh, P.C., Wadiche, J.I., and Overstreet-Wadiche, L.S., J. Neurosci., 2013, vol. 33, pp. 6614–6622.

    PubMed Central  CAS  PubMed  Google Scholar 

  159. Berg, D.A., Belnoue, L., Song, H., and Simon, A., Development, 2013, vol. 140, pp. 2548–2561.

    PubMed Central  CAS  PubMed  Google Scholar 

  160. Duveau, V., Laustela, S., Barth, L., Gianolini, F., Vogt, K.E., Keist, R., Chandra, D., Homanics, G.E., Rudolph, U., and Fritschy, J.M., Eur. J. Neurosci., 2011, vol. 34, no. 3, pp. 362–373.

    PubMed Central  PubMed  Google Scholar 

  161. Marin-Burgin, A., Mongiat, L.A., Pardi, M.B., and Schinder, A.F., Science, 2012, vol. 335, pp. 1238–1242.

    PubMed Central  CAS  PubMed  Google Scholar 

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Original Russian Text © I.V. Kudryashova, 2015, published in Neirokhimiya, 2015, Vol. 32, No. 3, pp. 181–191.

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Kudryashova, I.V. The plasticity of inhibitory synapses as a factor of long-term modifications. Neurochem. J. 9, 159–168 (2015). https://doi.org/10.1134/S1819712415030058

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