Журнал высшей нервной деятельности им. И.П. Павлова, 2023, T. 73, № 5, стр. 579-605

Координирующая роль актинового цитоскелета в кратковременной нейросетевой пластичности с участием возбуждающих и тормозных синапсов

И. В. Кудряшова *

Федеральное государственное бюджетное учреждение науки Институт высшей нервной деятельности и нейрофизиологии РАН
Москва, Россия

* E-mail: iv_kudryashova@mail.ru

Поступила в редакцию 19.04.2023
После доработки 20.06.2023
Принята к публикации 03.07.2023

Аннотация

Проблема частотного кодирования тесно связана с исследованиями механизмов участия тормозных интернейронов в нейросетевой пластичности. В работе изложены основные принципы интеграции тормозных интернейронов в формирование пространственно-временного паттерна активности нейронов при обработке сигнала. Анализируются современные представления о динамическом характере синаптических реакций и их нестабильности в ходе текущей активности. Представленные результаты свидетельствуют о том, что кратковременная пластичность осуществляется в тесном взаимодействии возбуждающих и тормозных синапсов. Обсуждается влияние тормозных потенциалов на активность внутриклеточных посредников, влияющих на динамику постсинаптических модификаций возбуждающих и тормозных синапсов. К настоящему времени многое известно о молекулярных механизмах таких модификаций, однако никаких концептуальных представлений о ключевых факторах, объединяющих реакции внутриклеточного сигналинга в единую систему, обеспечивающую сбалансированность и “адаптивность” модификаций возбуждающих и тормозных синапсов, до сих пор не предлагалось. Приводятся аргументы в пользу координирующей роли актинового цитоскелета. Предполагается, что источником постсинаптических модификаций тормозных синапсов является быстрая адаптация актинового цитоскелета и ассоциированных с ним белков к любым отклонениям от оптимального баланса между возбуждением и торможением.

Ключевые слова: кратковременная пластичность, тормозный контроль, актиновый цитоскелет, дестабилизация синапсов, латеральная диффузия ГАМКА-рецепторов

Список литературы

  1. Большаков А.П., Розов А.В. Механизмы фасилитации и депрессии в синапсах ЦНС: пресинаптические и постсинаптические компоненты. Нейрохимия. 2014. 31 (4): 276–286.

  2. Валиуллина-Рахматуллина Ф.Ф., Большаков А.П., Розов А.В. Три модальности синаптического выброса нейромедиатора: быстрый синхронный, мультивезикулярный и асинхронный. Сходства и различия в механизмах. Журн. высш нервн. деят. им. И.П.Павлова. 2019. 69 (1): 3–13.

  3. Ковалева Т.Ф., Максимова Н.С., Жуков И.Ю., Першин В.И., Мухина И.В., Гайнуллин М.Р. Кофилин: молекулярно-клеточные функции и роль в функционировании нервной системы. Нейрохимия. 2019. 36 (1): 14–23.

  4. Кудряшова И.В. Пластичность тормозных синапсов как фактор долговременных модификаций. Нейрохимия. 2015. 32 (3): 181–191.

  5. Кудряшова И.В. Молекулярные основы дестабилизации синапсов как фактор структурной пластичности. Нейрохимия. 2019. 36 (1): 3–13.

  6. Кудряшова И.В. Реорганизация актинового матрикса как фактор пресинаптической пластичности. Нейрохимия. 2021. 38 (3): 195–204.

  7. Кудряшова И.В. Тормозный контроль кратковременной пластичности при парной стимуляции зависит от полимеризации актина. Нейрохимия. 2022. 39 (2): 131–143.

  8. Розов А.В., Валиуллина Ф.Ф., Большаков А.П. Механизмы долговременной синаптической пластичности в ГАМКергических синапсах гиппокампа. Биохимия. 2017. 82 (3): 389–396.

  9. Al Awabdh S., Donneger F., Goutierre M., Séveno M., Vigy O., Weinzettl P., Russeau M., Moutkine I., Lévi S., Marin Ph., Poncer J.Ch. Gephyrin Interacts with the K-Cl Cotransporter KCC2 to regulate its surface expression and function in cortical neurons. J. Neurosci. 2022. 42 (22): 166–182.

  10. Arancibia-Cárcamo L., Yuen E.Y., Muir J., Lumb M.J., Michels G., Saliba R.S., Smart T.G., Yan Zh., Kittler J.T., Moss S.J. Ubiquitin-dependent lysosomal targeting of GABA(A) receptors regulates neuronal inhibition Proc. Natl. Acad. Sci. USA. 2009. 106 (41): 17552–17557.

  11. Bannai H., Lévi S., Schweizer C., Inoue T., Launey T., Racine V., Sibarita J.B., Mikoshiba K. Triller A. Activity-dependent tuning of inhibitory neurotransmission based on GABAAR diffusion dynamics. Neuron. 2009. 62: 670–682.

  12. Bannai H., Niwa F., Sherwood M.W., Shrivastava A.N., Arizono M., Miyamoto A., Sugiura K., Lévi S. Bidirectional control of synaptic GABAAR clustering by glutamate and calcium. Cell Rep. 2015. 13: 2768–2780.

  13. Bartley A.F., Dobrunz L.E. Short-term plasticity regulates the excitation/inhibition ratio and the temporal window for spike integration in CA1 pyramidal cells. Eur. J. Neurosci. 2015. 41: 1402–1415.

  14. Bausen M., Fuhrmann J.C., Betz H. O’Sullivan G.A. The state of the actin cytoskeleton determines its association with gephyrin: role of ena/VASP family members. Mol. Cell Neurosci. 2006. 31: 376–386.

  15. Bausen M., Weltzien F., Betz H., O’Sullivan G.A. Regulation of postsynaptic gephyrin cluster size by protein phosphatase 1. Mol. Cell Neurosci. 2010. 44: 201–209.

  16. Bleckert A., Photowala H., Alford S. Dual pools of actin at presynaptic terminals. J. Neurophysiol. 2012. 107 (12): 3479–3492.

  17. Bloss E.B., Cembrowski M.S., Karsh B., Colonell J., Fetter R.D., Spruston N. Structured dendritic inhibition supports branch-selective integration in CA1 pyramidal cells. Neuron. 2016. 89: 1016–1030.

  18. Bogdanov Y., Michels G., Armstrong-Gold C., Haydon P.G., Lindstrom J., Pangalos M., Moss S.J. Synaptic GABAA receptors are directly recruited from their extrasynaptic counterparts. EMBO J. 2006. 25: 4381–4389.

  19. Böhme M.A., McCarthy A.W., Grasskamp A.T., Beuschel C.B., Goel P., Jusyte M., Laber D., Huang Sh., Rey U., Petzoldt A.G., Lehmann M., Göttfert F., Haghighi P., Hell S.W., Owald D., Dickman D., Sigrist S.J., Walter A.M. Rapid active zone remodeling consolidates presynaptic potentiation. Nat. Commun. 2019. 10: 1085.

  20. Borovac J., Bosch M., Okamoto K. Regulation of actin dynamics during structural plasticity of dendritic spines: signaling messengers and actin-binding proteins. Mol. Cell. Neurosci. 2018. 91: 122–130.

  21. Bosch M., Castro J., Saneyoshi T., Matsuno H., Sur M., Hayashi Y. Structural and Molecular Remodeling of Dendritic Spine Substructures during Long-Term Potentiation. Neuron. 2014. 82: 444–459.

  22. Bourne J.N., Harris K.M. Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus. 2011. 21: 354–373.

  23. Boyken J., Grønborg M., Riedel D., Urlaub H., Jahn R., Chua J.J.E. Molecular profiling of synaptic vesicle docking sites reveals novel proteins but few differences between glutamatergic and GABAergic synapses. Neuron. 2013. 78: 285–297.

  24. Cao F., Zhou Z., Pan X., Leung C., Xie W., Collingridge G., Jia Z. Developmental regulation of hippocampal long-term depression by cofilin-mediated actin reorganization. Neuropharmacology. 2017. 112 (2): 66–75.

  25. Chamma I., Heubl M., Chevy Q., Renner M., Moutkine I., Eugène E., Poncer J.Ch., Lévi S. Activity-dependent regulation of the K/Cl transporter KCC2 membrane diffusion, clustering and function in hippocampal neurons. J. Neurosci. 2013. 33: 15488–15503.

  26. Chapman C.A., Nuwer J.L. Jacob T.C. The Yin and Yang of GABAergic and Glutamatergic Synaptic Plasticity: Opposites in Balance by Crosstalking Mechanisms. Front. Synapt. Neurosci. 2022. 14: 911020

  27. Chevy Q., Heubl M., Goutierre M., Backer S., Moutkine I., Eugène E., Bloch-Gallego E., Lévi S., Ponce J.Ch. KCC2 gates activity-driven AMPA receptor traffic through cofilin phosphorylation. J. Neurosci. 2015. 35 (48): 15772–15786.

  28. Chiu C.Q., Lur G., Morse T.M., Carnevale N.T., Ellis-Davies G.C. Higley M.J. Compartmentalization of GABAergic inhibition by dendritic spines. Science. 2013. 340: 759–762.

  29. Chiu C.Q., Barberis A., Higley M.J. Preserving the balance: Diverse forms of long-term GABAergic synaptic plasticity. Nat. Rev. Neurosci. 2019. 20: 272–281.

  30. Choquet D., Triller A. The dynamic synapse. Neuron. 2013. 80: 691–703.

  31. Chou W.-H., Wang D., McMahon T., Qi Z-H., Spong M., Zhang C., Shokat K.M., Messing R. GABA(A) receptor trafficking is regulated by PKCε and the N- ethylmaleimide-sensitive factor. J. Neurosci. 2010. 30: 13955–13965.

  32. Cingolani L.A., Goda Y. Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat. Rev. Neurosci. 2008. 9: 344–356.

  33. Davenport C.M., Rajappa R., Katchan L., Taylor C.R., Tsai M.-C., Smith C.M., de Jong J.W., Arnold D.B., Lammel S., Kramer R.H. Relocation of an extrasynaptic GABAA receptor to inhibitory synapses freezes excitatory synaptic strength and preserves memory. Neuron. 2021. 109: 123–134.

  34. Davis G.W., Muller M. Homeostatic control of presynaptic neurotransmitter release. Annu. Rev. Physiol. 2015. 77: 251–270.

  35. de Luca E., Ravasenga T., Petrini E.M., Polenghi A., Nieus T., Guazzi S., Barberis A. Inter-synaptic lateral diffusion of GABAA receptors shapes inhibitory synaptic currents. Neuron. 2017. 95 (1): 63–69.e5.

  36. Dejanovic B., Schwarz G. Neuronal nitric oxide synthase-dependent S-nitrosylation of gephyrin regulates gephyrin clustering at GABAergic synapses. J. Neurosci. 2014. 34: 7763–7768.

  37. Dejanovic B., Semtner M., Ebert S., Lamkemeyer T., Neuser F., Lüscher B., Meier J.C., Schwarz G. Palmitoylation of gephyrin controls receptor clustering and plasticity of GABAergic synapses. PLoS Biol. 2014. 12 (7): e1001908.

  38. Dityatev A., Schachner M., Sonderegger P. The dual role of the extracellular matrix in synaptic plasticity and homeostasis. Nat. Rev. Neurosci. 2010. 11: 735–746.

  39. Domínguez S., de Sevilla D.F. Buño W. Muscarinic Long-Term Enhancement of Tonic and Phasic GABAA Inhibition in Rat CA1 Pyramidal Neurons. Front. Cell. Neurosci. 2016. 10: 244.

  40. Fiumelli H., Briner A., Puskarjov M., Blaesse P., Belem B.J., Dayer A.G., Kaila K., Martin J.L., Vutskits L. An ion transport-independent role for the cation-chloride cotransporter KCC2 in dendritic spinogenesis in vivo. Cereb. Cortex. 2013. 23: 378–388.

  41. Fiumelli H., Cancedda L., Poo M.M. Modulation of GABAergic transmission by activity via postsynaptic Ca2+-dependent regulation of KCC2 function. Neuron. 2005. 48: 773–786.

  42. Flores C.E., Nikonenko I., Mendez P., Fritschy J.-M., Tyagarajan S.K., Muller D. Activity-dependent inhibitory synapse remodeling through gephyrin phosphorylation. Proc. Natl. Acad. Sci. USA. 2015. 112: E65–E72.

  43. Frias C.P., Liang J., Bresser T., Scheefhals L., van Kesteren M., van Dorland R., Hu H.Y., Bodzeta A., van Bergen en Henegouwen P.M.P., Hoogenraad C.C., Wierenga C.J. Semaphorin4D induces inhibitory synapse formation by rapid stabilization of presynaptic boutons via MET coactivation. J. Neurosci. 2019. 39 (22): 4221–4237.

  44. Fritschy J. Panzanelli P. GABAA receptors and plasticity of inhibitory neurotransmission in the central nervous system. Eur. J. Neurosci. 2014. 39 (11): 1845–1865.

  45. Fukazawa Y., Saitoh Y., Ozawa F., Ohta Y., Mizuno K., Inokuchi K. Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron. 2003. 38: 447–460.

  46. Galvez B., Gross N., Sumikawa K. Activation of α7 nicotinic acetylcholine receptors protects potentiated synapses from depotentiation during theta pattern stimulation in the hippocampal CA1 region of rats. Neuropharmacology. 2016. 105: 378–387.

  47. Gandolfi D., Bigiani A., Porro C.A., Mapelli J. Inhibitory plasticity: from molecules to computation and beyond. Int. J. Mol. Sci. 2020. 21 (5): 1805.

  48. Gauvain G., Chamma I., Chevy Q., Cabezas C., Irinopoulou T., Bodrug N., Carnaud M., Lévi S., Poncer J.C. The neuronal K-Cl cotransporter KCC2 influences postsynaptic AMPA receptor content and lateral diffusion in dendritic spines. Proc. Natl. Acad. Sci USA. 2011. 108: 15474–15479.

  49. Gerrow K. Triller A. GABAA receptor subunit composition and competition at synapses are tuned by GABAB receptor activity. Mol. Cell. Neurosci. 2014. 60: 97–107.

  50. Gidon A., Segev I. Principles governing the operation of synaptic inhibition in dendrites. Neuron. 2012. 75: 330–341.

  51. Giesemann T., Schwarz G., Nawrotzki R., Berhörster K., Rothkegel M., Schlüter K., Schrader N., Schindelin H., Mendel R.R., Kirsch J., Jockusch B.M. Complex formation between the postsynaptic scaffolding protein gephyrin, profilin, and Mena: a possible link to the microfilament system. J. Neurosci. 2003. 23 (23): 8330–8339.

  52. Goel P., Dufour Bergeron D., Böhme M.A., Nunnelly L., Lehmann M., Buser C., Walter A.M., Sigrist S.J., Dickman D. Homeostatic scaling of active zone scaffolds maintains global synaptic strength. J. Cell. Biol. 2019. 218 (5): 1706-1724.

  53. Gordon-Weeks P.R., Fournier A.E. Neuronal cytoskeleton in synaptic plasticity and regeneration. J. Neurochem. 2014. 129: 206–212.

  54. Gravielle M.C. Regulation of GABAA receptors induced by the activation of L-type voltage-gated calcium channels. Membranes. 2021. 11: 486.

  55. Gu J.C. Lee W., Fan Y., Komlos D., Tang X., Sun Ch., Yu K., Hartzell H.C., Chen G., Bamburg J.R, Zheng J.Q. ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat. Neurosci. 2010. 13 (10): 1208–1215.

  56. Gu Y., Chiu S.L., Liu B., Wu P.H., Delannoy M., Lin D.T., Wirtz D., Huganir R.L. Differential vesicular sorting of AMPA and GABAA receptors. Proc. Natl. Acad. Sci. USA. 2016. 113 (7): E922–E931.

  57. Guzman G.A., Guzman R.E., Jordan N., Hidalgo P. A Tripartite interaction among the calcium channel α1- and β-subunits and F-actin increases the readily releasable pool of vesicles and its recovery after depletion. Front. Cell. Neurosci. 2019. 13: 125.

  58. Halpain S. Actin in a supporting role. Nat. Neurosci. 2003. 6: 101–102.

  59. Hanus C., Ehrensperger M.-V., Triller A. Activity-dependent movements of postsynaptic scaffolds at inhibitory synapses. J. Neurosci. 2006. 26: 4586–4595.

  60. Hartmann K., Bruehl C., Golovko T., Draguhn A. Fast homeostatic plasticity of inhibition via activity-dependent vesicular filling. PLoS One. 2008. 3: e2979.

  61. Hausrat T.J., Muhia M., Gerrow K., Thomas Ph., Hirdes W., Tsukita S., Heisler F.F., Herich L., Dubroqua S., Breiden P., Feldon J., Schwarz J.R, Yee B.K., Smart T.G., Triller A., Kneussel M. Radixin regulates synaptic GABAA receptor density and is essential for reversal learning and short-term memory. Nat Commun. 2015. 6: 6872.

  62. Hayama T., Noguchi J., Watanabe S., Takahashi N., Hayashi-Takagi A., Ellis-Davies G.C., Matsuzaki M., Kasai H. GABA promotes the competitive selection of dendritic spines by controlling local Ca2+ signaling. Nat. Neurosci. 2013. 16 (10): 1409–1416.

  63. Hennequin G., Agnes E.J., Vogels T.P. Inhibitory plasticity: Balance, control, and codependence. Ann. Rev. Neurosci. 2017. 25: 557–579.

  64. Holtmaat A., Svoboda K. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci. 2009. 10: 647–658.

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

  66. Horn M.E., Nicoll R.A. Somatostatin and parvalbumin inhibitory synapses onto hippocampal pyramidal neurons are regulated by distinct mechanisms. Proc. Natl. Acad. Sci. USA. 2018. 115: 589–594.

  67. Houston C.M., He Q. Smart T.G. CaMKII phosphorylation of the GABAA receptor: receptor subtype- and synapse-specific modulation. J. Physiol. 2009. 587: 2115–2125.

  68. Imoukhuede P.I., Moss F.J., Michael D.J., Chow R.H., Lester H.A. Ezrin mediates tethering of the gamma-aminobutyric acid transporter GAT1 to actin filaments via a C-terminal PDZ-interacting domain. Biophys. J. 2009. 96: 2949–2960.

  69. Ivanov A., Esclapez M., Pellegrino Ch., Shirao T., Ferhat L. Drebrin A regulates dendritic spine plasticity and synaptic function in mature cultured hippocampal neurons. J. Cell. Sci. 2009. 122: 524–534.

  70. Jackman S.L., Regehr W.G. The mechanisms and functions of synaptic facilitation. Neuron. 2017. 94: 447–464.

  71. Jacob T.C., Wan Q., Vithlani M., Saliba R.S., Succol F., Pangalos M.N., Moss S.J. GABAA receptor membrane trafficking regulates spine maturity. Proc. Natl. Acad. Sci. USA. 2009. 106 (30): 12500–12505.

  72. Jacob T.C., Bogdanov Y.D., Magnus C., Saliba R.S., Kittler J.T., Haydon P.G., Moss S.J. Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J. Neurosci. 2005. 25: 10469–10478.

  73. Kelly M.T., Yao Y., Sondhi R., Sacktor T.C. Actin polymerization regulates the synthesis of PKMzeta in LTP. Neuropharmacology. 2007. 52: 41–45.

  74. Kitamura A., Ishibashi H., Watanabe M., Takatsuru Y., Brodwick M., Nabekura J. Sustained depolarizing shift of the GABA reversal potential by glutamate receptor activation in hippocampal neurons. Neurosci Res. 2008. 62: 270–277.

  75. Klausberger T. GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus. Eur. J. Neurosci. 2009. 306: 947–957.

  76. Klug A., Borst J.G., Carlson B.A., Kopp-Scheinpflug C., Klyachko V.A., Xu-Friedman M.A. How do short-term changes at synapses fine-tune information processing? J. Neurosci. 2012. 32 (41): 14 058–14 063.

  77. Kneussel M. Hausrat T.J. Postsynaptic neurotransmitter receptor reserve pools for synaptic potentiation. Trend. Neurosci. 2016. 39: 170–182.

  78. Korobova F. Svitkina T. Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol. Biol. Cell. 2010. 21: 165–176.

  79. Kowalczyk S., Winkelmann A., Smolinsky B., Förstera B., Neundorf I., Schwarz G., Meier J.C. Direct binding of GABAA receptor β2 and β3 subunits to gephyrin. Eur. J. Neurosci. 2013. 37 (4): 544–554.

  80. Kudryashova I.V. Presynaptic plasticity is fssociated with actin polymerization. Biochemistry (Moscow). 2023. 88 (3): 392-403.

  81. Kullmann D.M., Moreau A.W., Bakiri Y., Nicholson E. Plasticity of inhibition Neuron. 2012. 75: 951–962.

  82. Lee H.H., Deeb T.Z., Walker J.A., Davies P.A., Moss S.J. NMDA receptor activity downregulates KCC2 resulting in depolarizing GABA(A) receptor-mediated currents. Nat Neurosci. 2011. 14: 736–743.

  83. Li H., Khirug S., Cai C., Ludwig A., Blaesse P., Kolikova J., Afzalov R., Coleman S.K., Lauri S., Airaksinen M.S., Keinänen K., Khiroug L., Saarma M., Kaila K., Rivera C. KCC2 interacts with the dendritic cytoskeleton to promote spine development. Neuron. 2007. 56: 1019–1033.

  84. Lin W.H. Webb D.J. Actin and actin-binding proteins: masters of dendritic spine formation, morphology, and function. Open Neurosci. J. 2009. 3: 54–66.

  85. Loebrich S., Bähring R., Katsuno T., Tsukita S., Kneussel M. Activated radixin is essential for GABAA receptor α5 subunit anchoring at the actin cytoskeleton. EMBO J. 2006. 25(5): 987–999.

  86. Loebrich S., Benoit M.R., Konopka J.A., Cottrell J.R., Gibson J., Nedivi E. CPG2 recruits endophilin B2 to the cytoskeleton for activity-dependent endocytosis of synaptic glutamate receptors. Curr. Biol. 2016. 26: 296–308.

  87. Lu W., Bromley-Coolidge S., Li J. Regulation of GABAergic synapse development by postsynaptic membrane proteins. Brain Res. Bull. 2017. 129: 30–42.

  88. Luscher B., Fuchs T., Kilpatrick C.L. GABAA receptor trafficking-mediated plasticity of inhibitory synapses. Neuron. 2011. 70: 385–409.

  89. Lushnikova I., Skibo G., Muller D., Nikonenko I. Excitatory synaptic activity is associated with a rapid structural plasticity of inhibitory synapses on hippocampal CA1 pyramidal cells. Neuropharmacology. 2011. 60: 757–764.

  90. Mahadevan V., Woodin M.A. Regulation of neuronal chloride homeostasis by neuromodulators. J. Physiol. 2016. 594: 2593–2605.

  91. Mapelli J., Gandolfi D., Vilella A., Zoli M., Bigiani A. Heterosynaptic GABAergic plasticity bidirectionally driven by the activity of pre- and postsynaptic NMDA receptors. Proc. Natl. Acad. Sci. USA. 2016. 113: 9898–9903.

  92. Marsden K.C., Beattie J.B., Friedenthal J., Carroll R.C. NMDA receptor activation potentiates inhibitory transmission through GABA receptor-associated protein-dependent exocytosis of GABAA receptors. J. Neurosci. 2007. 27: 14326–14337.

  93. Marsden K.C., Shemesh A., Bayer K.U. Carroll R.C. Selective translocation of Ca2+/calmodulin protein kinase IIalpha (CaMKIIalpha) to inhibitory synapses. Proc. Natl Acad. Sci. USA. 2010. 107: 20559–20564.

  94. Marty A., Llano I. Excitatory effects of GABA in established brain networks. Trend. Neurosci. 2005. 28: 284–289.

  95. Matus A. Actin-based plasticity in dendritic spines. Science. 2000. 290: 754–758.

  96. Maynard S.A., Triller A. Inhibitory receptor diffusion dynamics. Front. Mol. Neurosci. 2019. 12: 313.

  97. McBain C.J. Kaue J.A. Presynaptic plasticity: targeted control of inhibitory networks. Curr. Opin. Neurobiol. 2009. 19 (3): 254–262.

  98. Mele M. Leal G. Duarte C.B. Role of GABAAR trafficking in the plasticity of inhibitory synapses. J. Neurochem. 2016. 139 (6): 997–1018.

  99. Mele M., Costa R.O., Duarte C.B. Alterations in GABAA-receptor trafficking and synaptic dysfunction in brain disorders. Front. Cell. Neurosci. 2019. 13: 77.

  100. Meyer D., Bonhoeffer T., Scheuss V. Balance and stability of synaptic structures during synaptic plasticity. Neuron. 2014. 82: 430–443.

  101. Miki T., Malagon G., Pulido C., Llano I., Neher E., Marty A. Actin- and myosin-dependent vesicle loading of presynaptic docking sites prior to exocytosis. Neuron. 2016. 91: 808–823.

  102. Mochida S. Presynaptic Calcium Channels. Int. J. Mol. Sci. 2019. 20 (9): 2217.

  103. Monday H.R., Younts T.J., Castillo P.E. Long-term plasticity of neurotransmitter release: Emerging mechanisms and contributions to brain function and disease. Annu. Rev. Neurosci. 2018. 41: 299–322.

  104. Muir J., Arancibia-Carcamo I.L., MacAskill A.F., Smith K.R., Griffin L.D., Kittler J.T. NMDA receptors regulate GABAA receptor lateral mobility and clustering at inhibitory synapses through serine 327 on the 2 subunit. Proc. Natl. Acad. Sci. USA. 2010. 107: 16679–16684.

  105. Mukherjee J., Kretschmannova K., Gouzer G., Maric H.-M., Ramsden S., Tretter V., Harvey K., Davies P.A., Triller A., Schindelin H., Moss S.J. The residence time of GABAARs at inhibitory synapses is determined by direct binding of the receptor 1 subunit to gephyrin. J. Neurosci. 2011. 31 (41): 14677–14687.

  106. Mullner F.E., Wierenga C.J. Bonhoeffer T. Precision of inhibition: dendritic inhibition by individual GABAergic synapses on hippocampal pyramidal cells is confined in space and time. Neuron. 2015. 87: 576–589.

  107. Nanou E., Catterall W.A. Calcium channels, synaptic plasticity, and neuropsychiatric disease. Neuron. 2018. 98: 466–481.

  108. Neuhoff H., Sassoe-Pognetto M., Panzanelli P., Maas C., Witke W., Kneussel M. The actin-binding protein profilin I is localized at synaptic sites in an activity-regulated manner. Eur. J. Neurosci. 2005. 21: 15–25.

  109. Niwa F., Bannai H., Arizono M., Fukatsu K., Triller A., Mikoshiba K. Gephyrin-independent GABA(A)R mobility and clustering during plasticity. PLoS One. 2012. 7: e36148.

  110. Oh W.C., Lutzu S., Castillo P.E., Kwon H.B. De novo synaptogenesis induced by GABA in the developing mouse cortex. Science. 2016. 353: 1037–1040.

  111. Okamoto K., Nagai T., Miyawaki A., Hayashi Y. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat. Neurosci. 2004. 7: 1104–1112.

  112. Ormond J., Woodin M.A. Disinhibition mediates a form of hippocampal long-term potentiation in area CA1. PLoS One. 2009. 4: e7224.

  113. Ouyang Y., Wong M., Capani F., Rensing N., Lee C.-S., Liu Q., Neusch C., Martone M.E., Wu J.Y., Yamada K., Ellisman M.H., Choi D.W. Transient decrease in F-actin may be necessary for translocation of proteins into dendritic spines. Eur. J. Neurosci. 2005. 22 (12): 2995–3005.

  114. Pennacchietti F., Vascon S., Nieus T., Rosillo C., Das S., Tyagarajan S.K. Diaspro A., Del Bue A., Petrini E.M., Barberis A., Zanacchi F.C. Nanoscale molecular reorganization of the inhibitory postsynaptic density is a determinant of gabaergic synaptic potentiation. J. Neurosci. 2017. 37 (7): 1747–1756.

  115. 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., Barberis A. Synaptic recruitment of gephyrin regulates surface GABAA receptor dynamics for the expression of inhibitory LTP. Nat. Commun. 2014. 5: 3921.

  116. Petrini E.M. Barberis A. Diffusion dynamics of synaptic molecules during inhibitory postsynaptic plasticity. Front. Cell. Neurosci. 2014. 8: 300.

  117. Pizzarelli R., Griguoli M., Zacchi P., Petrini E.M., Barberis A., Cattaneo A., Cherubini E. Tuning GABAergic inhibition: gephyrin molecular organization and functions. Neuroscience. 2020. 439: 125–136.

  118. Poulopoulos A., Aramuni G., Meyer G. Soykan T., Hoon M., Papadopoulos T., Zhang M., Paarmann I., Fuchs C., Harvey K., Jedlicka P., Schwarzacher S.W., Betz H., Harvey R.J., Brose N., Zhang W., Varoqueaux F. Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron. 2009. 63 (5): 628–642.

  119. Puskarjov M., Ahmad F., Kaila K., Blaesse P. Activity-dependent cleavage of the K-Cl cotransporter KCC2 mediated by calcium-activated protease calpain. J. Neurosci. 2012. 32: 11356–11364.

  120. Ramachandran B., Frey J.U. Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices in vitro. J. Neurosci. 2009. 29: 12167–12173.

  121. Rannals M.D., Kapur J. Homeostatic strengthening of inhibitory synapses is mediated by the accumulation of GABAA receptors. J. Neurosci. 2011. 31 (48): 17701–17712.

  122. Ravasenga T., Ruben M., Regio V., Polenghi A., Petrini E.M., Barberis A. Spatial regulation of coordinated excitatory and inhibitory synaptic plasticity at dendritic synapses. Cell. Rep. 2022. 38: 110347.

  123. Renner M., Schweizer C., Bannai H., Triller A., Lévi S. Diffusion barriers constrain receptors at synapses. PLoS ONE. 2012. 7: e43032.

  124. Rex C.S., Gavin C.F., Rubio M.D., Kramar E.A., Chen L.Y., Jia Y., Huganir R.L., Muzyczka N., Gall C.M., Miller C.A., Lynch G., Rumbaugh G. Myosin IIB regulates actin dynamics during synaptic plasticity and memory formation. Neuron. 2010. 67 (4): 603–617.

  125. Rex C.S., Chen L.Y., Sharma A., Liu J., Babayan A.H., Gall C.M., Lynch G. Different Rho GTPase-dependent signaling pathways initiate sequential steps in the consolidation of long-term potentiation. J. Cell. Biol. 2009. 186: 85–97.

  126. Rosenmund C., Westbrook G.L. Calcium-induced actin depolymerization reduces NMDA channel activity. Neuron. 1993. 10: 805–814.

  127. Runge K., Cardoso C. de Chevigny A. Dendritic spine plasticity: Function and mechanisms. Front. Synapt. Neurosci. 2020. 12: 36.

  128. Rust M.B., Gurniak C.B., Renner M., Vara H., Morando L., Görlich A., Sassoè-Pognetto M., Banchaabouchi M.A., Giustetto M., Triller A., Choquet D., Witke W. Learning, AMPA receptor mobility and synaptic plasticity depend on n-cofilin-mediated actin dynamics. EMBO J. 2010. 29 (11): 1889–1902.

  129. Saliba R.S., Kretschmannova K., Moss S.J. Activity-dependent phosphorylation of GABAA receptors regulates receptor insertion and tonic current. EMBO J. 2012. 31: 2937–2951.

  130. Saliba R.S., Michels G., Jacob T.C., Pangalos M.N., Moss S.J. Activity-dependent ubiquitination of GABA(A) receptors regulates their accumulation at synaptic sites. J. Neurosci. 2007. 27: 13341–13351.

  131. Saliba R.S., Pangalos M., Moss S.J. The ubiquitin-like protein Plic-1 enhances the membrane insertion of GABAA receptors by increasing their stability within the endoplasmic reticulum. J. Biol. Chem. 2008. 283: 18538–18544.

  132. Saliba R.S., Gu Z., Yan Z., Moss S.J. Blocking L-type voltage-gated Ca2+ channels with dihydropyridines reduces gamma-aminobutyric acid type A receptor expression and synaptic inhibition. J. Biol. Chem. 2009. 284: 32544–32550.

  133. Serwanski D.R. Miralles C.P., Christie S.B., Mehta A.K., Li X., De Blas A.L. Synaptic and nonsynaptic localization of GABAA receptors containing the alpha5 subunit in the rat brain. J. Comp. Neurol. 2006. 499 (3): 458–470.

  134. Shao C., Dong J., Zhao M., Liu S., Wang X., Yu Y., Fang L., Zhu Z., Chen Q., Xiao X., Zhang W.-N., Yang K. Presynaptic GABAB receptors differentially modulate GABA release from cholecystokinin and parvalbumin interneurons onto CA1 pyramidal neurons: A cell type-specific labeling and activating study. Neurosci. Lett. 2022. 772: 136448.

  135. Shrivastava A.N., Triller A., Sieghart W. GABAA receptors: post-synaptic co-localization and cross-talk with other receptors. Front. Cell. Neurosci. 2011. 5: 7.

  136. Smith K.R., Davenport E.C., Wei J., Li X., Pathania M., Vaccaro V., Yan Z. Kittler J.T. GIT1 and betaPIX are essential for GABAA receptor synaptic stability and inhibitory neurotransmission. Cell. Rep. 2014. 9: 298–310.

  137. Sprekeler H. Functional consequences of inhibitory plasticity: homeostasis, the excitation-inhibition balance and beyond. Curr. Opin. Neurobiol. 2017. 43: 198–203.

  138. Thalhammer A. Cingolani L.A. Cell adhesion and homeostatic synaptic plasticity. Neuropharmacology. 2014. 78: 23–30.

  139. Tong L., Prieto G.A., Cotman C.W. IL-1β suppresses cLTP-induced surface expression of GluA1 and actin polymerization via ceramide-mediated Src activation. J. Neuroinflammation. 2018. 15: 127.

  140. Tyagarajan S.K., Fritschy J.M. Gephyrin: a master regulator of neuronal function? Nat. Rev. Neurosci. 2014. 15: 141–156.

  141. Vargas-Caballero M., Martin L.J., Salter M.W., Orser B.A. Paulsen O. alpha5 Subunit-containing GABA(A) receptors mediate a slowly decaying inhibitory synaptic current in CA1 pyramidal neurons following Schaffer collateral activation. Neuropharmacology. 2009. 58: 668–675.

  142. Villa K.L., Berry K.P., Subramanian J., Cha J.W., Oh W.C., Kwon H.B., Kubota Y., So P.T., Nedivi E. Inhibitory synapses are repeatedly assembled and removed at persistent sites in vivo. Neuron. 2016. 89 (4): 756–769.

  143. Virtanen M.A., Uvarov P., Mavrovic M., Poncer J.C., Kaila K. The multifaceted roles of KCC2 in cortical development. Trend. Neurosci. 2021. 44: 378–392.

  144. Vithlani M., Moss S.J., Terunuma M. The dynamic modulation of GABAA receptor trafficking and its role in the formation of inhibitory synapses. Physiol. Rev. 2011. 91: 1009–1022.

  145. Vlachos A., Reddy-Alla S., Papadopoulos T., Deller T., Betz H. Homeostatic regulation of gephyrin scaffolds and synaptic strength at mature hippocampal GABAergic postsynapses. Cereb. Cortex. 2013. 23: 2700–2711.

  146. Wang J., Liu S., Haditsch U., Tu W., Cochrane K., Ahmadian G., Tran L., Paw J., Wang Y., Mansuy I., Salter M.M., Lu Y.M. Interaction of calcineurin and type-A GABA receptor gamma 2 subunits produces long-term depression at CA1 inhibitory synapses. J. Neurosci. 2003. 23: 826–836.

  147. Wang L., Maffei A. Inhibitory plasticity dictates the sign of plasticity at excitatory synapses. J. Neurosci. 2014. 34: 1083–1093.

  148. Wang W., Gong N., Xu T.L. Downregulation of KCC2 following LTP contributes to EPSP-spike potentiation in rat hippocampus. Biochem. Biophys. Res. Commun. 2006. 343: 1209–1215.

  149. Watanabe M., Fukuda A. Development and regulation of chloride homeostasis in the central nervous system. Front. Cell. Neurosci. 2015. 9: 371.

  150. Wei J., Zhang M., Zhu Y., Wang J.-H. Ca(2+)-calmodulin signalling pathway up-regulates GABA synaptic transmission through cytoskeleton-mediated mechanisms. Neuroscience. 2004. 127 (3): 637–647.

  151. Willadt S., Nenniger M., Vogt K.E. Hippocampal feedforward inhibition focuses excitatory synaptic signals into distinct dendritic compartments. PLoS One. 2013. 8 (11): e80984.

  152. Wright R., Newey S.E., Ilie A., Wefelmeyer W., Raimondo J.V., Ginham R., Mcllhinney R.A.J., Akerman C.J. Neuronal Chloride Regulation via KCC2 Is Modulated through a GABAB Receptor Protein Complex. J. Neurosci. 2017. 37 (22): 5447–5462.

  153. Wu X.S., Lee S.H., Sheng J., Zhang Z., Zhao W.D., Wang D., Jin Y., Charnay P., Ervasti J.M., Wu L.G. Actin is crucial for all kinetically distinguishable forms of endocytosis at synapses. Neuron. 2016. 92 (5): 1020–1035.

  154. Wu K., Castellano D., Tian Q., Lu W. Distinct regulation of tonic GABAergic inhibition by NMDA receptor subtypes. Cell. Rep. 2021. 37: 109960.

  155. Wyroślak M., Lebida K., Mozrzymas J.W. Induction of inhibitory synaptic plasticity enhances tonic current by increasing the content of α5-Subunit Containing GABAA Receptors in Hippocampal Pyramidal Neurons. Neuroscience. 2021. 467: 39–46.

  156. Xue J.-G., Masuoka T., Gong X.-D., Chen K.-S., Yanagawa Y., Law S.K. A., Konishi S. NMDA receptor activation enhances inhibitory GABAergic transmission onto hippocampal pyramidal neurons via presynaptic and postsynaptic mechanisms. J. Neurophysiol. 2011. 105 (6): 2897–2906.

  157. Yan Zh., Kim E., Datta D., Lewis D.A., Soderling S.H. Synaptic actin dysregulation, a convergent mechanism of mental disorders? J. Neurosci. 2016. 36 (45): 11411–11417.

  158. Yang Y., Wang X.B., Frerking M., Zhou Q. Spine expansion and stabilization associated with long-term potentiation. J. Neurosci. 2008. 28: 5740–5751.

  159. Yap E.L., Pettit N.L., Davis C.P., Nagy M.A., Harmin D.A., Golden E., Dagliyan O., Lin C., Rudolph S., Sharma N., Griffith E.C., Harvey C.D., Greenberg M.E. Bidirectional perisomatic inhibitory plasticity of a Fos neuronal network. Nature. 2020. 590: 115–121.

  160. Yoshihara Y., De Roo M., Muller D. Dendritic spine formation and stabilization. Curr. Opin. Neurobiol. 2009. 19: 146–153.

  161. Zarnowska E.D., Keist R., Rudolph U. Pearce R.A. GABAA receptor alpha5 subunits contribute to GABAA, slow synaptic inhibition in mouse hippocampus. J. Neurophysiol. 2009. 101: 1179–1191.

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