Advertisement

Neurochemical Journal

, Volume 7, Issue 1, pp 45–55 | Cite as

Central cholinergic systems in the mechanisms of hypoxic preconditioning: Diverse pathways of synaptic reorganization in vivo

  • E. I. ZakharovaEmail author
  • E. L. Germanova
  • R. A. Kopaladze
  • A. M. Dudchenko
Experimental Articles

Abstract

We studied the effects of single moderate hypobaric hypoxia (HBH, 10% O2, 60 min) on the central cholinergic systems. For this purpose, we determined the activity of the marker of cholinergic neurons choline acetyltransferase (ChAT) and the protein content in subfractions of synaptic membranes and synaptoplasm, which were isolated from the “light” and “heavy” synaptosomes of the pons varolii and medulla oblondata (“pontomedulla”), neocortex, and hippocampus. Experiments were performed with intact rats and rats with low and high resistance to hypoxia that first underwent severe hypobaric hypoxia (4% O2). We found that HBH influenced the synaptic pool of the pontomedulla in all groups of rats, the neocortex in groups of intact and highly resistant rats, and the hippocampus in neither group. HBH affected cytosolic and membrane-bound ChAT and proteins; the changes depended on the group of rats. We reviewed the role of cytosolic and membrane-bound ChAT in the regulation of exchange and secretion of acetylcholine in vitro. We show that in vivo acute adaptation (1) in the intact brain via transformation of cholinergic synaptic pool, which is associated with the formation and activation of contacts of the hypoxia-resistant morphological type; (2) occurs via inhibition of cholinergic activity in different populations of synapses and reduction of non-cholinergic, presumably GABAergic, populations in the brains of poorly and highly resistant rats. Our study demonstrates (1) numerous varieties of plastic possibilities of the brain and (2) one of natural mechanisms of hypoxic preconditioning of the intact brain, viz., the formation and activation of morphological hypoxia-resistant cholinergic synapses in the pontomedulla and neocortex.

Keywords

preconditioning moderate hypobaric hypoxia intact rats rats with low and high resistance to hypoxia pontomedulla neocortex hippocampus cholinergic systems subfractions of synaptic membranes and synapto-plasm membrane-bound and cytosolic choline acetyltransferase 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Strelkov, R.B., Chizhov, A.Ya., Il’ina, A.I., Kuznetsova, L.E., Pines, E.V., Raevskaya, S.A., Tyutikova, O.N., and Shchitkov, K.G., Vopr. Onkol., 1979, vol. 25, no. 6, pp. 3–6.PubMedGoogle Scholar
  2. 2.
    Strelkov, R.B., Vopr. Kurort. i Fizioter., 1997, no. 6, pp. 37–40.Google Scholar
  3. 3.
    Chizhov, A.Ya. and Potievskaya, V.I., Fiziol. Chel., 1997, vol. 23, no. 1, pp. 108–112.Google Scholar
  4. 4.
    Strelkov, R.B., Fiziol. Zh., 2003, vol. 49, no. 2, pp. 45–49.PubMedGoogle Scholar
  5. 5.
    Chizhov, A.Ya. and Bludov, A.A., in Problemy gipoksii: molekulyarnye, fiziologicheskie i meditsinskie aspekty (Problems of Hypoxia: Molecular, Physiological, and Medical Aspects), Luk’yanova, L.D. and Ushakov, I.B., Eds., Voronezh: Istoki, 2004, pp. 519–568.Google Scholar
  6. 6.
    Potievskaya, V.I. and Potievskii, B.G., Patogenez, 2008, no. 3, pp. 37–39.Google Scholar
  7. 7.
    Tarakanov, I.A. and Safanov, V.A., Patogenez, 2003, no. 2, pp. 11–24.Google Scholar
  8. 8.
    Safonov, V.A., Chelovek v vozdushnom okeane (Human in Air Ocean), Moscow: Natsional’noe obozrenie, 2006.Google Scholar
  9. 9.
    Butler, J.A., Anand, A., Crawford, M.R., Glanfille, A.R., McKensie, D.K., Paintal, A.S., Talor, J.L., and Gandevia, S.C., J. Physiol., 2001, vol. 534, no. 2, pp. 283–293.CrossRefGoogle Scholar
  10. 10.
    Iturriaga, R. and Alcayaga, J., Brain Res. Brain Res. Rev., 2004, vol. 47, pp. 46–53.PubMedCrossRefGoogle Scholar
  11. 11.
    He, L., Dinger, B., and Fidone, S., J. Appl. Physiol., 2005, vol. 8, no. 2, pp. 614–619.Google Scholar
  12. 12.
    Reynolds, D.J., Lowenstein, P.R., Moorman, J.M., Grahame-Smith, D.G., and Leslie, R.A., Neurochem. Int., 1994, vol. 25, no. 5, pp. 455–464.PubMedCrossRefGoogle Scholar
  13. 13.
    Ferguson, D.G., Haxhiu, M.A., To, A.J., Erokwu, B., and Dreshaj, I.A., Neurosci. Let., 2000, vol. 287, no. 2, pp. 141–145.CrossRefGoogle Scholar
  14. 14.
    Armstrong, D.M., Rotler, A., Hersh, L.B., and Pickel, V.M., J. Neurosci. Res, 1988, vol. 20, pp. 279–290.PubMedCrossRefGoogle Scholar
  15. 15.
    Lauterborn, J.C., Isackson, P.J., Montalvo, R., and Gall, C.M., Brain Res. Mol. Brain Res, 1993, vol. 17, nos. 1–2, pp. 59–69.PubMedCrossRefGoogle Scholar
  16. 16.
    Kc, P., Mayer, C.A., and Haxhiu, M.A., J. Appl. Physiol., 2004, vol. 97, no. 4, pp. 1508–1517.PubMedCrossRefGoogle Scholar
  17. 17.
    Kimura, T., Yu, J.G., Edvinsson, L., and Lee, T.J., Brain Res., 1997, vol. 773, nos. 1–2, pp. 117–124.PubMedCrossRefGoogle Scholar
  18. 18.
    Ichinose, M., Nihon Kokyuki Gakkai Zasshi, 1999, vol. 37, no. 1, pp. 3–9.PubMedGoogle Scholar
  19. 19.
    Si, M.L. and Lee, T.J., Circ. Res., 2002, vol. 91, no. 1, pp. 62–69.PubMedCrossRefGoogle Scholar
  20. 20.
    Loeschcke, H.H., J. Physiol., 1982, vol. 332, pp. 1–24.PubMedGoogle Scholar
  21. 21.
    Kubo, T., Hagiwara, Y., Sekiya, D., Chiba, S., and Fukumori, R., Brain Res. Bull., 2000, vol. 53, no. 3, pp. 275–282.PubMedCrossRefGoogle Scholar
  22. 22.
    Haxhiu, M.A., Kc, P., Moore, C.T., Acquah, S.S., Wilson, C.G., Zaidi, S.I., Massari, V.J., and Ferguson, D.G., J. Appl. Physiol., 2005, vol. 98, no. 6, pp. 1961–1982.PubMedCrossRefGoogle Scholar
  23. 23.
    Dehkordi, O., Kc, P., Balan, K.V., and Haxhiu, M.A., Auton. Neurosci., 2006, vol. 128, nos. 1–2, pp. 53–63.PubMedCrossRefGoogle Scholar
  24. 24.
    Moore, C., Wang, Y., and Ramage, A.G., Br. J. Pharmacol., 2008, vol. 153, no. 8, pp. 1728–1738.PubMedCrossRefGoogle Scholar
  25. 25.
    Kuo, J.S., Leung, Y.M., Lin, N.N., Lee, T.J., and Gong, C.L., Auton. Neurosci., 2010, vol. 152, nos. 1–2, pp. 49–54.PubMedCrossRefGoogle Scholar
  26. 26.
    Jordan, D. and Spyer, K.M., J. Physiol., 1981, vol. 320, pp. 103–111.PubMedGoogle Scholar
  27. 27.
    Shao, X.M. and Feldman, J.L., Cholinergic Neurotransmission in the PreBÖtzinger Complex Modulates Excitability of Inspiratory Neurons and Regulates Respiratory Rhythm, Neuroscience, 2005, vol. 130, issue 4, pp. 1069–1081.CrossRefGoogle Scholar
  28. 28.
    Luk’yanova, L.D., Germanova, E.L., Tsybina, T.A., Kopaladze, R.A., and Dudchenko, A.M., Patogenez, 2008, no. 3, pp. 32–36.Google Scholar
  29. 29.
    Zakharova, E.I., Svinov, M.M., Germanova, E.N., Fedorova, M.M., and Luk’yanova, L.D., in Problemy gipoksii: molekulyarnye, fiziologicheskie i meditsinskie aspekty (Problems of Hypoxia: Molecular, Physiological, and Medical Aspects), Luk’yanova, L.D. and Ushakov, I.B., Eds., Voronezh: Istoki, 2004, pp. 268–296.Google Scholar
  30. 30.
    Zakharova, E.I., Storojeva, Z.I., Germanova, E.L., Monakov, M.Y., Proshin, A.T., Dudchenko, A.M., and Lukyanova, L.D., Adaptation Biol. Med. (V 5: Health Potentials), Lukyanova, L., Takeda, N., and Singal, P.K., Eds., New Delhi: Narosa Publishing House Pvt. Ltd., 2008, pp. 122–141.Google Scholar
  31. 31.
    Zakharova, E.I., Dudchenko, A.M., Svinov, M.M., Fedorova, M.M., and Germanova, E.L., Neurochemical Journal, 2010, vol. 4, no. 4, pp. 290–303.CrossRefGoogle Scholar
  32. 32.
    Zakharova, E.I., Storozheva, Z.I., Dudchenko, A.M., and Kubatiev, A.A., Int. J. Alzheimers Dis., 2010, 954589.Google Scholar
  33. 33.
    Chernobaeva, G.N. and Luk’yanova, L.D., in Farmakologicheskaya korrektsiya gipoksicheskikh sostoyanii (Pharmacological Correction of Hypoxic States), Moscow, 1989, pp. 160–164.Google Scholar
  34. 34.
    Nakai, M., Tamaki, K., Ogata, J., Matsui, Y., and Maeda, M., Parasympathetic Cerebrovasodilator Center of the Facial Nerve, Circ. Res., 1993, vol. 72, no. 2, pp. 470–475.PubMedCrossRefGoogle Scholar
  35. 35.
    Fonnum, F., Biochem. J., 1969, vol. 115, pp. 465–472.PubMedGoogle Scholar
  36. 36.
    Zakharova, E.I., Dudchenko, A.M., Svinov, M.M., Ivanov, D.S., and Ignat’ev, I.V., Neirokhimiya, 2001, vol. 18, no. 2, pp. 119–131.Google Scholar
  37. 37.
    Lowry, O.H., Rosenbrough, N.J., Farr, A.L., and Randall, R., J. Biol. Chem., 1959, vol. 193, pp. 265–275.Google Scholar
  38. 38.
    Kobzar’, A.I., Prikladnaya matematicheskaya statistika. Dlya inzhenerov i nauchnykh rabotnikov (Applied Mathematical Statistics. For Engineers and Scientists), Moscow: Iz-vo “Fizmatlit”, 2006.Google Scholar
  39. 39.
    Mukhin, E.I., Zakharova, E.I., and Kikteva, E.A., Neurosci. Behav. Physiol., 2002. vol. 32, no. 4, pp. 379–387.PubMedCrossRefGoogle Scholar
  40. 40.
    Oda, Y., Pathol. Int., 1999, vol. 49, no. 11, pp. 921–937.PubMedCrossRefGoogle Scholar
  41. 41.
    Dobransky, T., Davis, W.L., Xiao, G.H., and Rylett, R.J., Biochem. J., 2000, vol. 349, pt 1, pp. 141–145.PubMedCrossRefGoogle Scholar
  42. 42.
    Dobransky, T., Davis, W.L., and Rylett, R.J., J. Biol. Chem., 2001, vol. 276, issue 25, pp. 22244–22250.CrossRefGoogle Scholar
  43. 43.
    Dobransky, T., Doherty-Kirby, A., Kim, A.R., Brewer, D., Lajoie, G., and Rylett, R.J., J. Biol. Chem., 2004, no. 50, pp. 52059–52068.Google Scholar
  44. 44.
    Dobransky, T. and Rylett, R.J., J. Neurochem., 2005, vol. 95, no. 2, pp. 305–313.PubMedCrossRefGoogle Scholar
  45. 45.
    Gill, S.K., Ishak, M., Dobransky, T., Haroutunian, V., Davis, K.L., and Rylett, R.J., Neurobiol. Aging, 2007, vol. 28, no. 7, pp. 1028–1040.PubMedCrossRefGoogle Scholar
  46. 46.
    Tooyama, I. and Kimura, H., J. Chem. Neuroanat., 2000, vol. 17, no. 4, pp. 217–226.PubMedCrossRefGoogle Scholar
  47. 47.
    Fonnum, F. and Malthe-Sorenssen, D., J. Neurochem., 1973, vol. 20, no. 5, pp. 1351–1359.PubMedCrossRefGoogle Scholar
  48. 48.
    Smith, C.P. and Carroll, P.T., Brain Res., 1980, vol. 185, no. 2, pp. 363–371.PubMedCrossRefGoogle Scholar
  49. 49.
    Benishin, C.G. and Carroll, P.T., J. Neurochem., 1983.Google Scholar
  50. 50.
    Fonnum, F., Biochem. J., 1967, vol. 103, no. 1, pp. 262–270.PubMedGoogle Scholar
  51. 51.
    Rylett, R.J., J. Neurochem., 1989, vol. 52, no. 3, pp. 869–875.PubMedCrossRefGoogle Scholar
  52. 52.
    Schmidt, B.M. and Rylett, R.J., Neuroscience, 1993a, vol. 54, no. 3, pp. 649–656.PubMedCrossRefGoogle Scholar
  53. 53.
    Smith, L.K. and Carroll, P.T., Brain Res., 1993, vol. 605, no. 1, pp. 155–163.PubMedCrossRefGoogle Scholar
  54. 54.
    Tuçek, S., Regulation of Acetylcholine Synthesis in the Brain, J. Neurochem., 1985, vol. 44, no. 1, pp. 11–24.PubMedCrossRefGoogle Scholar
  55. 55.
    Salem, N., Medilanski, J., Pellegrinelli, N., and Eder-Colli, L., Eur. J. Neurosci., 1994, vol. 6, no. 5, pp. 737–745.PubMedCrossRefGoogle Scholar
  56. 56.
    Carroll, P.T., Badamchian, M., Craig, P., and Lyness, W.H., Brain Res., 1986, vol. 383, nos. 1–2, pp. 83–99.PubMedCrossRefGoogle Scholar
  57. 57.
    Carroll, P.T., Brain Res., 1987, vol. 414, no. 2, pp. 401–404.PubMedCrossRefGoogle Scholar
  58. 58.
    Sha, D., Jin, H., Kopke, R.D., and Wu, J.Y., Neurochem. Res., 2004, vol. 29, no. 1, pp. 199–207.PubMedCrossRefGoogle Scholar
  59. 59.
    Carroll, P.T. and Benishin, C.G., Brain Res., 1984, vol. 291, no. 2, pp. 261–272.PubMedCrossRefGoogle Scholar
  60. 60.
    Carroll, P.T., Brain Res., 1997, vol. 753, no. 1, pp. 47–55.PubMedCrossRefGoogle Scholar
  61. 61.
    Alkondon, M., Pereira, E.F., Cortes, W.S., Maelicke, A., and Albuquerque, E.X., Eur. J. Neurosci, 1997, vol. 9, pp. 2734–2742.PubMedCrossRefGoogle Scholar
  62. 62.
    Si, M.L. and Lee, T.J., Circ. Res., 2002, vol. 91, no. 1, pp. 62–69.PubMedCrossRefGoogle Scholar
  63. 63.
    Eder-Colli, L., Briand, P.A., and Dunant, Y., Brain Res., 1992, vol. 573, no. 2, pp. 284–292.PubMedCrossRefGoogle Scholar
  64. 64.
    Whittaker, V.P., Michaelson, I.A., Jeanette, R., and Kirkland, A., Biochem. J., 1964, vol. 90, pp. 293–303.PubMedGoogle Scholar
  65. 65.
    Schmidt, B.M. and Rylett, R.J., J. Neurochem., 1993b, vol. 61, no. 5, pp. 1774–1781.PubMedCrossRefGoogle Scholar
  66. 66.
    Carroll, P.T., Brain Res., 1994, vol. 633, nos. 1–2, pp. 112–118.PubMedCrossRefGoogle Scholar
  67. 67.
    Birman, S., Israël, M., Lesbats, B., and Morel, N., J. Neurochem., 1986, vol. 47, no. 2, pp. 433–444.PubMedCrossRefGoogle Scholar
  68. 68.
    Falk-Vairant, J., Correges, P., Eder-Colli, L., Salem, N., Roulet, E., Bloc, A., Meunier, F., Lesbats, B., Loctin, F., Synguelakis, M., Israel, M., and Dunant, Y., Proc. Natl. Acad. Sci. USA, 1996, vol. 93, no. 11, pp. 5203–5207.PubMedCrossRefGoogle Scholar
  69. 69.
    Dunant, Y., Cordeiro, J.M., and Goncalves, P.P., Ann. N. Y. Acad. Sci., 2009, vol. 1152, pp. 100–112.PubMedCrossRefGoogle Scholar
  70. 70.
    Israel, M., Lesbats, B., Morel, N., and Manaranche, R., Le Gal La Salle G, FEBS Lett., 1988, vol. 233, no. 2, pp. 421–426.PubMedCrossRefGoogle Scholar
  71. 71.
    Dunant, Y. and Israel, M., Biochimie, 2000, vol. 82, no. 4, pp. 289–302.PubMedCrossRefGoogle Scholar
  72. 72.
    Bloc, A., Bugnard, E., Dunant, Y., Falk-Vairant, J., Israel, M., Loctin, F., and Roulet, E., Eur. J. Neurosci., 1999, vol. 11, no. 5, pp. 1523–1534.PubMedCrossRefGoogle Scholar
  73. 73.
    Dunant, Y., Loctin, F., Vallee, J.P., Parducz, A., Lesbats, B., and Israel, M., Pflugers Arc., vol. 432, no. 5, pp. 853–858.Google Scholar
  74. 74.
    Bancila, V., Nikonenko, I., Dunant, Y., and Bloc, A., J. Neurochem., 2004, vol. 90, no. 5, pp. 1243–1250.PubMedCrossRefGoogle Scholar
  75. 75.
    Medvedeva, Y.V., Lin, B., Shuttleworth, C.W., and Weiss, J.H., J. Neurosci., 2009, vol. 29, no. 4, pp. 1105–1114.PubMedCrossRefGoogle Scholar
  76. 76.
    Cordeiro, J.M., Goncalves, P.P., and Dunant, Y., J. Physiol., 2011, vol. 589.Google Scholar
  77. 77.
    Carroll, P.T., Brain Res., 1996, vol. 725, no. 1, pp. 3–10.PubMedGoogle Scholar
  78. 78.
    Rylett, R.J. and Schmidt, B.M., Prog. Brain Res., 1993, vol. 98, pp. 161–166.PubMedCrossRefGoogle Scholar
  79. 79.
    Parducz, A., Correges, P., Sors, P., and Dunant, Y., Eur. J. Neurosci., 1997, vol. 9, no. 4, pp. 732–738.PubMedCrossRefGoogle Scholar
  80. 80.
    Dobransky, T., Brewer, D., Lajoie, G., and Rylett, R.J., J. Biol. Chem., 2003, vol. 278, no. 8, pp. 5883–5893.PubMedCrossRefGoogle Scholar
  81. 81.
    Semchenko, V.V. and Stepanov, S.S., Tsitologiya, 1985, vol. 27, no. 11, pp. 1235–1239.Google Scholar
  82. 82.
    Semchenko, V.V. and Stepanov, S.S., Byul. Eksper. Biol., 1986, vol. 102, no. 7, pp. 100–102.Google Scholar
  83. 83.
    Semchenko, V.V. and Stepanov, S.S., Byul. Eksper. Biol., 1997, vol. 124, no. 7, pp. 4–12.Google Scholar
  84. 84.
    Bogolepov, N.N., Dovedova, E.L., Orlova, E.I., and Yakovleva, N.I., Arkh. Anat., 1985, vol. 89, no. 11, pp. 88–93.PubMedGoogle Scholar
  85. 85.
    Zakharova, E.I., Dudchenko, A.M., and Germanova, E.L., Biull. Eksp. Biol. Med., 2011, vol. 151, no. 2, pp. 179–182.CrossRefGoogle Scholar
  86. 86.
    Samoilov, M.O., Reaktsii neironov mozga na gipoksiyu, (Response of the Brain Neurons to Hypoxia), Leningrad: Nauka, 1985.Google Scholar
  87. 87.
    LaManna, J.C., Light, A.I., Peretsman, S.J., and Rosenthal, M., Brain Res., 1984, vol. 293, no. 2, pp. 313–318.PubMedCrossRefGoogle Scholar
  88. 88.
    Dudchenko, A.M., Goryacheva, T.V., Eliseev, A.L., Mikhal’skaya, I.O., Spasskaya, M.E., Glebov, R.N., and Luk’yanova, L.D., Byul. Eksper. Biol. i Med., 1993, vol. 116, no. 12, pp. 604–607.Google Scholar
  89. 89.
    Dudchenko, A.M., Chernobaeva, G.N., Belousova, V.V., Vlasova, I.G., and Luk’yanova, L.D., Byul. Eksper. Biol. i Med., 1993, vol. 115, no. 3, pp. 251–254.CrossRefGoogle Scholar
  90. 90.
    Haba, K., Ogawa, N., Mizukawa, K., and Mori, A., Brain Res., 1991, vol. 540, pp. 116–122.PubMedCrossRefGoogle Scholar
  91. 91.
    Ogawa, N., Haba, K., Asanuma, M., Mizukawa, K., and Mori, A., Neuroreceptor Mechanisms in Brain, Kito, S., et al., Eds., New York: Plenum Press, 1991, pp. 343–347.Google Scholar
  92. 92.
    Iwasaki, K., Kitamura, Y., Ohgami, Y., Mishima, K., and Fujiwara, M., Brain Res., 1996, vol. 709, no. 2, pp. 163–172.PubMedCrossRefGoogle Scholar
  93. 93.
    Semchenko, V.V., Stepanov, S.S., and Sergeeva, E.D., Byull. Eksper. Biol. i Med., 1995, vol. 119, no. 4, pp. 443–445.Google Scholar
  94. 94.
    Semchenko, V.V., Bogolepov, N.N., and Stepanov, S.S., in Sinaptoarkhitektonika kory bol’shogo mozga (Synaptic Architechtonics of the Brain Cortex), Omsk, 1995.Google Scholar
  95. 95.
    Malyshev, A.Yu., Luk’yanova, L.D., and Krapivin, S.V., Byul. Eksper. Biol., 1996, vol. 122, no. 9, pp. 264–267.Google Scholar
  96. 96.
    Engert, F. and Bonhoeffer, T., Nature, 1999, vol. 399, pp. 66–70.PubMedCrossRefGoogle Scholar
  97. 97.
    Hübener, M. and Bonhoeffer, T., Neuron, 2010, vol. 67, no. 3, pp. 363–371.PubMedCrossRefGoogle Scholar
  98. 98.
    Keck, T., Scheuss, V., Jacobsen, R.I., Wierenga, C.J., Eysel, U.T., Bonhoeffer, T., and Hubener, M., Neuron, 2011, vol. 71, no. 5, pp. 869–882.PubMedCrossRefGoogle Scholar
  99. 99.
    Woods, G.F., Oh, W.C., Boudewyn, L.C., Mikula, S.K., and Zito, K., J. Neurosci., 2011, vol. 31, no. 34, pp. 12129–12138.PubMedCrossRefGoogle Scholar
  100. 100.
    Kudryashova, I.V., Neirokhimiya, 2011, vol. 28, no. 4, pp. 261–273.Google Scholar
  101. 101.
    Gallo, G., J. Cell Sci., 2006, vol. 119,pt. 16, pp. 3413–3423.PubMedCrossRefGoogle Scholar
  102. 102.
    De Robertis, E., Pellegrino, De., and Araldi, A., Rodrigues De Lores Arnaiz G., Salganicoff L, J. Neurochem., 1962, vol. 9, pp. 23–35.CrossRefGoogle Scholar
  103. 103.
    Glebov, R.N. and Kryzhanovskii, G.N., Funktsional’naya biokhimiya sinapsov (Functional Biochemistry of Synapses), Moscow: Meditsina, 1978.Google Scholar
  104. 104.
    Pierrefiche, O., Schwarzacher, S.W., Bischoff, A.M., and Richter, D.W., J. Physiol., 1998, vol. 509, pt. 1, pp. 245–254.PubMedCrossRefGoogle Scholar
  105. 105.
    Shevtsova, N.A., Manzke, T., Molkov, Y.I., Bischoff, A., Smith, J.C., Rybak, I.A., and Richter, D.W., Eur. J. Neurosci., 2011, vol. 34, no. 8, pp. 1276–1291.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2013

Authors and Affiliations

  • E. I. Zakharova
    • 1
    • 2
    Email author
  • E. L. Germanova
    • 1
  • R. A. Kopaladze
    • 1
  • A. M. Dudchenko
    • 1
  1. 1.Institute of General Pathology and PathophysiologyRussian Academy of Medical SciencesMoscowRussia
  2. 2.MoscowRussia

Personalised recommendations