Today: Dec 3, 2024
RU / EN
Last update: Oct 30, 2024
Forms and Mechanisms of Homeostatic Synaptic Plasticity

Forms and Mechanisms of Homeostatic Synaptic Plasticity

Balashova A.N., Dityatev A.E., Mukhina I.V.
Key words: synaptic plasticity; scaling; homeostasis; synapse.
2013, volume 5, issue 2, page 98.

Full text

pdf
0
2032

Long-term changes of neuronal network activity level result in the activity of excitatory and inhibitory synapses counteracting the change of the mean frequency of spike generation and contributing to network homeostasis maintenance. The review describes the manifestations of homeostatic synaptic plasticity in vivo and in vitro. The best investigated form of homeostatic synaptic plasticity, or “synaptic scaling” is the change of synapse intensity between excitatory neurons, multiple of initial synapse intensity and inversely proportional to the change of the frequency of spikes in postsynaptic neurons. However, the intensity of inhibitory synapses on excitatory neurons, as well as the intensity of excitatory synapses on inhibitory neurons, change directly proportionally to the change of spike frequency. There has been considered the central postsynaptic mechanism participating in the occurrence and further regulation of homeostatic plasticity of excitatory synapses — the alteration of the pool of α-amino-3-hydroxy-5-methyl-4-isoxasolpropionic acid receptors (AMPA-receptors). There have been characterized presynaptic molecular mechanisms and considered the role of concentration changes of intracellular calcium, molecules of cytoadherence, and the secretion of signal molecules in postsynaptic regulation of homeostatic plasticity.

  1. Turrigiano G.G., Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 2004; 5: 97–107.
  2. Bienenstock E.L., Cooper L.N., Munro P.W. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 1982; 2: 32–48.
  3. Bear M.F., Cooper L.N., Ebner F.F. A physiological basis for a theory of synapse modification. Science 1987; 237: 42–48.
  4. Miller K.D., Mackay D.J.C. The role of constraints in Hebbian learning. Neural Comput 1994: 6: 100–126.
  5. Turrigiano G.G. The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 2008; 135: 422–435.
  6. Ibata K., Sun Q., Turrigiano G.G. Rapid synaptic scaling induced by changes in postsynaptic firing. Neuron 2008; 57: 819–826.
  7. Turrigiano G.G., Leslie K.R., Desai N.S., Rutherford L.C., Nelson S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 1998; 391: 892–896.
  8. Burrone J., Murthy V.N. Synaptic gain control and homeostasis. Curr Opin Neurobiol 2003; 13: 560–567.
  9. Chang M.C., Park J.M., Pelkey K.A., Grabenstatter H.L., Xu D., Linden D.J., Sutula T.P., McBain C.J., Worley P.F. Narp regulates homeostatic scaling of excitatory synapses on parvalbumin-expressing interneurons. Nat Neurosci 2010; 13: 1090–1097.
  10. Lissin D.V., Gomperts S.N., Carroll R.C., Christine C.W., Kalman D., Kitamura M., Hardy S., Nicoll R.A., Malenka R.C., Von Zastrow M. Activity differentially regulates the surface expression of synaptic AMPA and NMDA glutamate receptors. Proc Natl Acad Sci USA 1998; 95: 7097–7102.
  11. Rutherford L.C., Nelson S.B., Turrigiano G.G. BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses. Neuron 1998; 21: 521–530.
  12. Burrone J., O’Byrne M., Murthy V.N. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature 2002; 420: 414–418.
  13. Gao M., Sossa K., Song L., Errington L., Cummings L., Hwang H., Kuhl D., Worley P., Lee H.K. A specific requirement of Arc/Arg3.1 for visual experience-induced homeostatic synaptic plasticity in mouse primary visual cortex. J Neurosci 2010; 30: 7174–7178.
  14. Kim J., Alger B.E. Reduction in endocannabinoid tone is a homeostatic mechanism for specific inhibitory synapses. Nat Neurosci 2010; 13: 592–600.
  15. Maffei A., Nelson S.B., Turrigiano G.G. Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat Neurosci 2004; 7: 1353–1359.
  16. Pratt K.G., Aizenman C.D. Homeostatic regulation of intrinsic excitability and synaptic transmission in a developing visual circuit. J Neurosci 2007; 27: 8274–8277.
  17. Quinlan E.M., Olstein D.H., Bear M.F. Bidirectional, experience-dependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proc Natl Acad Sci USA 1999; 96: 12876–12880.
  18. Quinlan E.M., Philpot B.D., Huganir R.L., Bear M.F. Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat Neurosci 1999; 2: 352–357.
  19. Maghsoodi B., Poon M.M., Nam C.I., Aoto J., Ting P., Chen L. Retinoic acid regulates RARalpha-mediated control of translation in dendritic RNA granules during homeostatic synaptic plasticity. Proc Natl Acad Sci USA 2008; 105: 16015–16020.
  20. Tetzlaff C., Kolodziejski C., Timme M., Wörgötter F. Synaptic scaling in combination with many generic plasticity mechanisms stabilizes circuit connectivity. Front in computneurosci 2011; 5: 47.
  21. Tetzlaff C., Kolodziejski C., Timme M., Wörgötter F. Analysis of synaptic scaling in combination with Hebbian plasticity in several simple networks. Front in computneurosci 2012; 6: 36.
  22. Watt A.J., Desai N.S. Homeostatic plasticity and STDP: keeping a neuron’s cool in a fluctuating world. Front in Syn Neurosci 2010; 2: 5.
  23. Keck C., Savin C., Lücke J. Feedforward Inhibition and Synaptic Scaling — Two Sides of the Same Coin? PLoS Comput Biol 2012; 8(3): e1002432.
  24. Wierenga C.J., Ibata K., Turrigiano G.G. Postsynaptic expression of homeostatic plasticity at neocortical synapses. J Neurosci 2005; 25: 2895–2905.
  25. Ranson A., Cheetham C.E.J., Fox K., Sengpiel F. Homeostatic plasticity mechanisms are required for juvenile, but not adult, ocular dominance plasticity. PNAS 2012; 109(4): 1311–1316.
  26. Echegoyen J., Neu A., Graber K.D., Soltesz I. Homeostatic plasticity studied using in vivo hippocampal activity-blockade: synaptic scaling, intrinsic plasticity and age-dependence. PLoS One 2007; 2: e700.
  27. Wilbrecht L., Holtmaat A., Wright N., Fox K., Svoboda K. Structural plasticity underlies experience-dependent functional plasticity of cortical circuits. J Neurosci 2010 Apr 7; 30(14): 4927–4932.
  28. Vlachos A., Becker D., Jedlicka P., Winkels R., Roeper J., Deller T. Entorhinal denervation induces homeostatic synaptic scaling of excitatory postsynapses of dentate granule cells in mouse organotypic slice cultures. PLoS ONE 2012 Mar; 7(3): e32883.
  29. Desai N.S., Cudmore R.H., Nelson S.B., Turrigiano G.G. Critical periods for experience-dependent synaptic scaling in visual cortex. Nat Neurosci 2002; 5: 783–789.
  30. Goel A., Jiang B., Xu L.W., Song L., Kirkwood A., Lee H.K. Cross-modal regulation of synaptic AMPA receptors in primary sensory cortices by visual experience. Nat Neurosci 2006; 9: 1001–1003.
  31. Goel A., Xu L.W., Snyder K.P., Song L., Goenaga-Vazquez Y., Megill A., Takamiya K., Huganir R.L., Lee H.K. Phosphorylation of AMPA receptors is required for sensory deprivation-induced homeostatic synaptic plasticity. PLoS One 2011; 6: e18264. doi: 10.1371/journal.pone.0018264.
  32. Goel A., Lee H.K. Persistence of experience-induced homeostatic synaptic plasticity through adulthood in superficial layers of mouse visual cortex. J Neurosci 2007; 27: 6692–6700.
  33. Maffei A., Turrigiano G.G. Multiple modes of network homeostasis in visual cortical layer 2/3. J Neurosci 2008; 28: 4377–4384.
  34. Petrus E., Anguh T.T., Pho H., Lee A., Gammon N., Lee H.K. Developmental switch in the polarity of experience-dependent synaptic changes in layer 6 of mouse visual cortex. J Neurophysiol 2011; 106: 2499–2505.
  35. Shepherd J.D. Memory, plasticity, and sleep — a role for calcium permeable AMPA receptors? Frontiers in Molecular Neuroscience 2012; 5: 49.
  36. Pozo K., Goda Y. Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 2010; 66(3): 337–351.
  37. Leslie K.R., Nelson S.B., Turrigiano G.G. Postsynaptic depolarization scales quantal amplitude in cortical pyramidal neurons. J Neurosci 2001; 21: RC170.
  38. Kim J., Tsien R.W., Alger B.E. An improved test for detecting multiplicative homeostatic synaptic scaling. PLoS ONE 2012 May; 7(5): e37364.
  39. Thiagarajan T.C., Lindskog M., Tsien R.W. Adaptation to synaptic inactivity in hippocampal neurons. Neuron 2005; 47: 775–737.
  40. O’Brien R.J., Kamboj S., Ehlers M.D., Rosen K.R., Fischbach G.D., and Huganir R.L. Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron 1998; 21: 1067–1078.
  41. Kim J., Tsien R.W. Synapse-specific adaptations to inactivity in hippocampal circuits achieve homeostatic gain control while dampening network reverberation. Neuron 2008; 58: 925–937.
  42. Wierenga C.J., Walsh M.F., Turrigiano G.G. Temporal regulation of the expression locus of homeostatic plasticity. J Neurophysiol 2006; 96: 2127–2133.
  43. Ju W., Morishita W., Tsui J., Gaietta G., Deerinck T.J., Adams S.R., Garner C.C., Tsien R.Y., Ellisman M.H., Malenka R.C. Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nat Neurosci 2004; 7: 244–253.
  44. Sutton M.A., Ito H.T., Cressy P., Kempf C., Woo J.C., Schuman E.M. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 2006; 125: 785–799.
  45. Thiagarajan T.C., Piedras-Renteria E.S., Tsien R.W. Alpha- and beta-CaMKII. Inverse regulation by neuronal activity and opposing effects on synaptic strength. Neuron 2002; 36: 1103–1114.
  46. Aoto J., Nam C.I., Poon M.M., Ting P., Chen L. Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron 2008; 60: 308–320.
  47. Beique J.C., Na Y., Kuhl D., Worley P.F., and Huganir R.L. Arc-dependent synapse-specific homeostatic plasticity. Proc Natl Acad Sci USA 2011; 108: 816–821.
  48. Freund T.F., Gulyas A.I. Inhibitory control of GABAergic interneurons in the hippocampus. Can J Physiol Pharmacol 1997; 75: 479–487.
  49. Zilberter Y. Dendritic release of glutamate suppresses synaptic inhibition of pyramidal neurons in rat neocortex. J Physiol 2000; 528: 489–496.
  50. McBain C.J., Fisahn A. Interneurons unbound. Nat Rev Neurosci 2001; 2: 11–23.
  51. Freund T.F. Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 2003; 26: 489–495.
  52. Tamas G., Buhl E.H., Lorincz A., Somogyi P. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat Neurosci 2000; 3: 366–371.
  53. Bradler J.E., Barrioneuvo G. Long-term potentiation in hippocampal CA3 neurons: tetanized input regulates heterosynaptic efficacy. Synapse 1989; 4: 132–142.
  54. Steele P.M., Mauk M.D. Inhibitory control of LTP and LTD: stability of synapse strength. J Neurophysiol 1999; 81: 1559–1566.
  55. Lu Y.M., Mansuy I.M., Kandel E.R., Roder J. Calcineurin-mediated LTD of GABAergic inhibition underlies the increased excitability of CA1 neurons associated with LTP. Neuron 2000; 26: 197–205.
  56. Nugent F.S., Penick E.C., Kauer J.A. Opioids block long-term potentiation of inhibitory synapses. Nature 2007; 446: 1086–1090.
  57. Traynelis S.F., Wollmuth L.P., McBain C.J., Menniti F.S., Vance K.M., Ogden K.K., Hansen K.B., Yuan H., Myers S.J., Dingledine R., Sibley D. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 2010; 62: 405–496.
  58. Sommer B., Kohler M., Sprengel R., Seeburg P.H. RNA editing in brain controls a determinant of ion fiow in glutamate-gated channels. Cell 1991; 67: 11–19.
  59. Burnashev N., Monyer H., Seeburg P.H., Sakmann B. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 1992; 8: 189–198.
  60. Hollmann M., Hartley M., Heinemann S. Ca2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 1991; 252; 851–853.
  61. Bowie D., Mayer M.L. Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 1995; 15: 453–462.
  62. Donevan S.D., Rogawski M.A. Intracellular polyamines mediate inward rectification of Ca(2+)-permeable alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Proc Natl Acad Sci USA 1995; 92: 9298–9302.
  63. McBain C.J., Dingledine R. Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatuminterneurones of rat hippocampus. J Physiol 1993; 462: 373–392.
  64. Bochet P., Audinat E., Lambolez B., Crepel F., Rossier J., Iino M., Tsuzuki K., Ozawa S. Subunit composition at the single-cell level explains functional properties of a glutamate-gated channel. Neuron 1994; 12: 383–388.
  65. Isa T., Iino M., Ozawa S. Spermine blocks synaptic transmission mediated by Ca(2+)-permeable AMPA receptors. Neuroreport 1996; 7: 749–692.
  66. Otis T.S., Raman I.M., Trussell L.O. AMPA receptors with high Ca2+ permeability mediate synaptic transmission in the avian auditory pathway. J Physiol 1995; 482(Pt 2): 309–315.
  67. Washburn M.S., Numberger M., Zhang S., Dingledine R. Differential dependence on GluR2 expression of three characteristic features of AMPA receptors. J Neurosci 1997; 17: 9393–9406.
  68. Isaac J.T., Ashby M., McBain C.J. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 2007; 54: 859–871.
  69. Liu S.J., Zukin R.S. Ca2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci 2007; 30: 126–134.
  70. Anggono V., Clem R.L., Huganir R.L. PICK1 loss of function occludes homeostatic synaptic scaling. J Neurosci 2011; 31: 2188–2196.
  71. Gainey M.A., Hurvitz-Wolff J.R., Lambo M.E., Turrigiano G.G. Synaptic scaling requires the GluR2 subunit of the AMPA receptor. J Neurosci 2009; 29: 6479–6489.
  72. Xie A.X., Sun M.-Y., Murphy T., Lauderdale K., Tiglao E., Fiacco T.A. Bidirectional scaling of astrocytic metabotropic glutamate receptor signaling following long-term changes in neuronal firing rates. PLoS ONE 2012; 7(11): e49637.
  73. Thiagarajan T.C., Lindskog M., Tsien R.W. Adaptation to synaptic inactivity in hippocampal neurons. Neuron 2005; 47: 725–737.
  74. Murthy V.N., Schikorski T., Stevens C.F., Zhu Y. Inactivity produces increases in neurotransmitter release and synapse size. Neuron 2001; 32: 673–682.
  75. Bacci A., Coco S., Pravettoni E., Schenk U., Armano S., Frassoni C., Verderio C., De Camilli P., Matteoli M. Chronic blockade of glutamate receptors enhances presynaptic release and downregulates the interaction between synaptophysin–synaptobrevin-vesicle-associated membrane protein 2. J Neurosci 2001; 21: 6588–6596.
  76. De Gois S., Schafer M.K., Defamie N., Chen C., Ricci A., Weihe E., Varoqui H., Erickson J.D. Homeostatic scaling of vesicular glutamate and GABA transporter expression in rat neocortical circuits. J Neurosci 2005; 25: 7121–7133.
  77. Frank C.A., Kennedy M.J., Goold C.P., Marek K.W., Davis G.W. Mechanisms underlying the rapid induction and sustained expression of synaptic homeostasis. Neuron 2006; 52: 663–677.
  78. Frank C.A., Pielage J., Davis G.W. A presynaptic homeostatic signaling system composed of the Eph receptor, ephexin, Cdc42, and CaV2.1 calcium channels. Neuron 2009; 61: 556–569.
  79. Wang X., Engisch K.L., Li Y., Pinter M.J., Cope T.C., Rich M.M. Decreased synaptic activity shifts the calcium dependence of release at the mammalian neuromuscular junction in vivo. J Neurosci 2004; 24: 10687–10692.
  80. Zhao C., Dreosti E., Lagnado L. Homeostatic synaptic plasticity through changes in presynaptic calcium influx. J Neurosci 2011; 31: 7492–7496.
  81. Custer K.L., Austin N.S., Sullivan J.M., Bajjalieh S.M. Synaptic vesicle protein 2 enhances release probability at quiescent synapses. J Neurosci 2006; 26: 1303–1313.
  82. Lazarevic V., Schone C., Heine M., Gundelfinger E.D., Fejtova A. Extensive remodeling of the presynaptic cytomatrix upon homeostatic adaptation to network activity silencing. J Neurosci 2011; 31: 10189–10200.
  83. Müller M., Pym E.C.G., Tong A., Davis G.W. Rab3-GAP controls the progression of synaptic homeostasis at a late stage of vesicle release. Neuron 2011 February 24; 69(4): 749–762.
  84. Dickman D.K., Tong A., Davis G.W. Snapin is critical for presynaptic homeostatic plasticity. J Neurosci 2012 Jun 20; 32(25): 8716–8724.
  85. Wang Z., Low P.A., Vernino S. Antibody-mediated impairment and homeostatic plasticity of autonomic ganglionic synaptic transmission. Exp Neurol 2010 March; 222(1): 114–119.
  86. Zhao C.J., Dreosti E., Lagnado L. Homeostatic synaptic plasticity through changes in presynaptic calcium influx. J Neurosci 2011; 31(20): 7492–7496.
  87. Stellwagen D., Malenka R.C. Synaptic scaling mediated by glial TNF-alpha. Nature 2006; 440: 1054–1059.
  88. Haydon P.G. GLIA: listening and talking to the synapse. Nat Rev Neurosci 2001; 2; 185–193.
  89. Huie J.R., Baumbauer K.M., Lee K.H., Bresnahan J.C., Beattie M.S., Ferguson A.R., Grau J.W. Glial tumor necrosis factor alpha (TNFa) generates metaplastic inhibition of spinal learning. PLoS ONE 2012; 7(6): e39751.
  90. Steinmetz C.C., Turrigiano G.G. TNF? signaling maintains the ability of cortical synapses to express synaptic scaling. J Neurosci 2010; 30(44): 14745–14690.
  91. Stöck E.D., Christensen R.N., Huie J.R., Tovar C.A., Miller B.A., Nout Y.S., Bresnahan J.C., Beattie M.S., Ferguson A.R. Tumor necrosis factor alpha mediates GABA(A) receptor trafficking to the plasma membrane of spinal cord neurons in vivo. Neural Plasticity 2012; 2012: 261345.
  92. Wenner P. Mechanisms of GABAergic homeostatic plasticity. Neural Plasticity 2011; 2011: 489470.
  93. Matsumoto T., Rauskolb S., Polack M., Klose J., Kolbeck R., Korte M., Barde Y.A. Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF. Nat Neurosci 2008; 11: 131–133.
  94. Lu Y., Christian K., Lu B. BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 2008; 89: 312–323.
  95. Balkowiec A., Katz D.M. Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J Neurosci 2002; 22: 10399–10407.
  96. Dean C., Liu H., Dunning F.M., Chang P.Y., Jackson M.B., Chapman E.R. Synaptotagmin-IV modulates synaptic function and long-term potentiation by regulating BDNF release. Nat Neurosci 2009; 12: 767–776.
  97. Carvalho A.L., Caldeira M.V., Santos S.D., Duarte C.B. Role of the brain-derived neurotrophic factor at glutamatergic synapses. Br J Pharmacol 2008; 153: S310–S324.
  98. Minichiello L. TrkB signalling pathways in LTP and learning. Nat Rev Neurosci 2009; 10: 850–860.
  99. Desai N.S., Rutherford L.C., Turrigiano G.G. Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat Neurosci 1999; 2: 515–520.
  100. Swanwick C.C., Murthy N.R., Kapur J. Activity-dependent scaling of GABAergic synapse strength is regulated by brain-derived neurotrophic factor. Mol Cell Neurosci 2006; 31: 481–492.
  101. Aakalu G., Smith W.B., Nguyen N., Jiang C., Schuman E.M. Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 2001; 30: 489–502.
  102. Bramham C.R., Wells D.G. Dendritic mRNA: transport, translation and function. Neuron 2007; 8: 776–789.
  103. Lane M.A., Bailey S.J. Role of retinoid signalling in the adult brain. Prog Neurobiol 2005; 75: 275–293.
  104. Chiang M.-Y., Misner D., Kempermann G., Schikorski T., Giguère V., Sucov H.M., Gage F.H., Stevens C.F., Evans R.M. An essential role for retinoid receptors RAR? and RXR? in long-term potentiation and depression. Neuron 1998; 21: 1353–1361.
  105. Tai C.Y., Mysore S.P., Chiu C., Schuman E.M. Activity-regulated N-cadherin endocytosis. Neuron 2007; 54: 771–785.
  106. Yasuda S., Tanaka H., Sugiura H., Okamura K., Sakaguchi T., Tran U., Takemiya T., Mizoguchi A., Yagita Y., Sakurai T., De Robertis E.M., Yamagata K. Activity-induced protocadherin arcadlin regulates dendritic spine number by triggering N-cadherin endocytosis via TAO2beta and p38 MAP kinases. Neuron 2007; 56: 456–471.
  107. Mysore S., Tai C., Schuman E. N-cadherin, spine dynamics, and synaptic function. Front Neurosci 2008; 2: 174–175.
  108. Takeichi M., Abe K. Synaptic contact dynamics controlled by cadherin and catenins. Trends Cell Biol 2005; 15: 216–221.
  109. Bamji S.X., Rico B., Kimes N., Reichardt L.F. BDNF mobilizes synaptic vesicles and enhances synapse formation by disrupting cadherin-{beta}-catenin interactions. J Cell Biol 2006; 174: 289–299.
  110. Bamji S.X., Shimazu K., Kimes N., Huelsken J., Birchmeier W., Lu B., Reichardt L.F. Role of 2-catenin in synaptic vesicle localization and presynaptic assembly. Neuron 2003; 40: 719–731.
  111. Murase S., Mosser E., Schuman E.M. Depolarization drives 2-catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 2002; 35: 91–105.
  112. Okuda T., Yu L.M., Cingolani L.A., Kemler R., Goda Y. beta-Catenin regulates excitatory postsynaptic strength at hippocampal synapses. Proc Natl Acad Sci USA 2007; 104: 13479–13484.
  113. Tang L., Hung C.P., Schuman E.M. A Role for the cadherin family of cell adhesion molecules in hippocampal long-term potentiation. Neuron 1998; 20: 1165–1175.
  114. Nuriya M., Huganir R.L. Regulation of AMPA receptor trafficking by N-cadherin. J Neurochem 2006; 97: 652–661.
  115. Saglietti L., Dequidt C., Kamieniarz K., Rousset M.-C., Valnegri P., Thoumine O., Beretta F., Fagni L., Choquet D., Sala C., et al. Extracellular interactions between GluR2 and N-Cadherin in spine regulation. Neuron 2007; 54: 461–477.
  116. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 2002; 110: 673–747.
  117. McGeachie A.B., Cingolania L.A., Goda Y.A. stabilising influence: integrins in regulation of synaptic plasticity. Neurosci Res 2011 May; 70(1): 24–29.
  118. Chan C.-S., Weeber E.J., Kurup S., Sweatt J.D., Davis R.L. Integrin requirement for hippocampal synaptic plasticity and spatial memory. J Neurosci 2003; 23: 7107–7116.
  119. Chavis P., Westbrook G. Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature 2001; 411: 317–321.
  120. Shi Y., Ethell I.M. Integrins control dendritic spine plasticity in hippocampal neurons through NMDA receptor and Ca2+/calmodulin-dependent protein kinase II-mediated actin reorganization. J Neurosci 2006; 26: 1813–1822.
  121. Cingolani L.A., Goda Y. Differential involvement of ?3 integrin in pre- and postsynaptic forms of adaptation to chronic activity deprivation. Neuron Glia Biol 2009; 4: 179–187.
  122. Cingolani L.A., Thalhammer A., Yu L.M., Catalano M., Ramos T., Colicos M.A., Goda Y. Activity-dependent regulation of synaptic AMPA receptor composition and abundance by beta3 integrins. Neuron 2008; 58: 749–762.
  123. Remme M.W.H., Wadman W.J. Homeostatic scaling of excitability in recurrent neural networks. PLoS Comput Biol 2012; 8(5): e1002494.
  124. Yoon Y.J., White S.L., Ni X., Gokin A.P., Martin-Caraballo M. Downregulation of GluA2 AMPA receptor subunits reduces the dendritic arborization of developing spinal motoneurons. PLoS ONE 2012; 7(11): e49879.
  125. Jakawich S.K., Neely R.M., Djakovic S.N., Patrick G.N., Sutton M.A. An essential postsynaptic role for the ubiquitin proteasome system in slow homeostatic synaptic plasticity in cultured hippocampal neurons. Neuroscience 2010 Dec 29; 171(4): 1016–1031.
  126. Cajigas I.J., Will T., Schuman E.M. Protein homeostasis and synaptic plasticity. The EMBO Journal 2010; 29: 2746–2752.
  127. Craig T.J., Jaafari N., Petrovic M.M., Rubin P.P., Mellor J.R., Henley J.M. Homeostatic synaptic scaling is regulated by protein SUMOylation. J Biol Chem 2012 Jun 29; 287(27): 22781–22788.
  128. Cohen J.E., Lee P.R., Chen Sh., Li W., Fields D.R. MicroRNA regulation of homeostatic synaptic plasticity. PNAS 2011; 108(28): 11650–11655.
  129. Volman V. Synaptic scaling stabilizes persistent activity driven by asynchronous neurotransmitter release. Neural Comput 2011 April; 23(4): 927–957.
  130. Kazantsev V., Gordleeva S., Stasenko S., Dityatev A. A homeostatic model of neuronal firing governed by feedback signals from the extracellular matrix. PLoS One 2012; 7(7): e41646.
  131. Baroncelli L., Braschi Ch., Spolidoro M., Begenisic T., Maffei L., Sale A. Brain plasticity and disease: a matter of inhibition. Neural Plasticity 2011; 2001: 286073.
  132. Spires-Jones T., Knafo Sh. Spines, plasticity, and cognition in Alzheimer’s model mice. Neural Plasticity 2012; 2012: 319836.
  133. Robison A.J., Nestler E.J. Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurocsi 2011; 12: 623–637.
  134. Huang Y.H., Schülter O.M., Dong Y. Cocaine-induced homeostatic regulation and dysregulation of nucleus accumbens neurons. Behav Brain Res 2011; 216(1): 9–18.
  135. Hu J.-H., Park J.M., Park S., Xiao B., Dehoff M.H., Kim S., Hayashi T., Schwarz M.K., Huganir R.L., Seeburg P.H., Linden D.J., Worley P.F. Homeostatic scaling requires group I mGluR activation mediated by Homer1a. Neuron 2010 Dec 22; 74(6): 1128–1142.
Balashova A.N., Dityatev A.E., Mukhina I.V. Forms and Mechanisms of Homeostatic Synaptic Plasticity. Sovremennye tehnologii v medicine 2013; 5(2): 98


Journal in Databases

pubmed_logo.jpg

web_of_science.jpg

scopus.jpg

crossref.jpg

ebsco.jpg

embase.jpg

ulrich.jpg

cyberleninka.jpg

e-library.jpg

lan.jpg

ajd.jpg

SCImago Journal & Country Rank