<?xml version="1.0" encoding="UTF-8"?>
<!DOCTYPE root>
<article xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" xmlns:ali="http://www.niso.org/schemas/ali/1.0/" article-type="review-article" dtd-version="1.2" xml:lang="en"><front><journal-meta><journal-id journal-id-type="publisher-id">Annals of Clinical and Experimental Neurology</journal-id><journal-title-group><journal-title xml:lang="en">Annals of Clinical and Experimental Neurology</journal-title><trans-title-group xml:lang="ru"><trans-title>Анналы клинической и экспериментальной неврологии</trans-title></trans-title-group></journal-title-group><issn publication-format="print">2075-5473</issn><issn publication-format="electronic">2409-2533</issn><publisher><publisher-name xml:lang="en">Eco-Vector</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="publisher-id">814</article-id><article-id pub-id-type="doi">10.54101/ACEN.2022.3.9</article-id><article-categories><subj-group subj-group-type="toc-heading" xml:lang="en"><subject>Technologies</subject></subj-group><subj-group subj-group-type="toc-heading" xml:lang="ru"><subject>Технологии</subject></subj-group><subj-group subj-group-type="article-type"><subject>Review Article</subject></subj-group></article-categories><title-group><article-title xml:lang="en">Metaplasticity and non-invasive brain stimulation: the search for new biomarkers and directions for therapeutic neuromodulation</article-title><trans-title-group xml:lang="ru"><trans-title>Метапластичность и неинвазивная стимуляция мозга: поиск новых биомаркеров и направлений терапевтической нейромодуляции</trans-title></trans-title-group></title-group><contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0003-0716-3737</contrib-id><name-alternatives><name xml:lang="en"><surname>Bakulin</surname><given-names>Ilya S.</given-names></name><name xml:lang="ru"><surname>Бакулин</surname><given-names>Илья Сергеевич</given-names></name></name-alternatives><address><country country="RU">Russian Federation</country></address><bio xml:lang="en"><p>Cand. Sci. (Med.), researcher, Head, Non-invasive neuromo- dulation group, Institute of Neurorehabilitation</p></bio><bio xml:lang="ru"><p>к.м.н., н.с., рук. группы неинвазивной нейромодуляции Института нейрореабилитации и восстановительных технологий</p></bio><email>bakulinilya@gmail.com</email><xref ref-type="aff" rid="aff1"/></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0003-1841-1177</contrib-id><name-alternatives><name xml:lang="en"><surname>Poydasheva</surname><given-names>Alexandra G.</given-names></name><name xml:lang="ru"><surname>Пойдашева</surname><given-names>Александра Георгиевна</given-names></name></name-alternatives><address><country country="RU">Russian Federation</country></address><bio xml:lang="en"><p>junior researcher, Non-invasive neuromodulation group, Institute of Neurorehabilitation</p></bio><bio xml:lang="ru"><p>м.н.с. группы неинвазивной нейромодуляции Института нейрореабилитации и восстановительных технологий</p></bio><email>alexandra.poydasheva@gmail.com</email><xref ref-type="aff" rid="aff1"/></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0001-8544-3107</contrib-id><name-alternatives><name xml:lang="en"><surname>Zabirova</surname><given-names>Alfiia H.</given-names></name><name xml:lang="ru"><surname>Забирова</surname><given-names>Альфия Ходжаевна</given-names></name></name-alternatives><address><country country="RU">Russian Federation</country></address><bio xml:lang="en"><p>postgraduate student, neurologist</p></bio><bio xml:lang="ru"><p>аспирант, врач-невролог</p></bio><email>alfijasabirowa@gmail.com</email><xref ref-type="aff" rid="aff1"/></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0003-3956-6362</contrib-id><name-alternatives><name xml:lang="en"><surname>Suponeva</surname><given-names>Natalia A.</given-names></name><name xml:lang="ru"><surname>Супонева</surname><given-names>Наталья Александровна</given-names></name></name-alternatives><address><country country="RU">Russian Federation</country></address><bio xml:lang="en"><p>D. Sci. (Med.), Corresponding Member of RAS, Director, Institute of Neurorehabilitation</p></bio><bio xml:lang="ru"><p>д.м.н., профессор, член-корреспондент РАН, директор Института нейрореабилитации и восстановительных технологий</p></bio><email>nasu2709@mail.ru</email><xref ref-type="aff" rid="aff1"/></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0002-6338-0392</contrib-id><name-alternatives><name xml:lang="en"><surname>Piradov</surname><given-names>Michael A.</given-names></name><name xml:lang="ru"><surname>Пирадов</surname><given-names>Михаил Александрович</given-names></name></name-alternatives><address><country country="RU">Russian Federation</country></address><bio xml:lang="en"><p>D. Sci. (Med.), Professor, Academician of RAS, Director</p></bio><bio xml:lang="ru"><p>д.м.н., профессор, академик РАН, директор</p></bio><email>Mpi711@gmail.com</email><xref ref-type="aff" rid="aff1"/></contrib></contrib-group><aff-alternatives id="aff1"><aff><institution xml:lang="en">Research Center of Neurology</institution></aff><aff><institution xml:lang="ru">ФГБНУ «Научный центр неврологии»</institution></aff></aff-alternatives><pub-date date-type="pub" iso-8601-date="2022-10-10" publication-format="electronic"><day>10</day><month>10</month><year>2022</year></pub-date><volume>16</volume><issue>3</issue><issue-title xml:lang="en"/><issue-title xml:lang="ru"/><fpage>74</fpage><lpage>82</lpage><history><date date-type="received" iso-8601-date="2022-01-24"><day>24</day><month>01</month><year>2022</year></date><date date-type="accepted" iso-8601-date="2022-02-15"><day>15</day><month>02</month><year>2022</year></date></history><permissions><copyright-statement xml:lang="en">Copyright ©; 2022, Bakulin I.S., Poydasheva A.G., Zabirova A.H., Suponeva N.A., Piradov M.A.</copyright-statement><copyright-statement xml:lang="ru">Copyright ©; 2022, Бакулин И.С., Пойдашева А.Г., Забирова А.Х., Супонева Н.А., Пирадов М.А.</copyright-statement><copyright-year>2022</copyright-year><copyright-holder xml:lang="en">Bakulin I.S., Poydasheva A.G., Zabirova A.H., Suponeva N.A., Piradov M.A.</copyright-holder><copyright-holder xml:lang="ru">Бакулин И.С., Пойдашева А.Г., Забирова А.Х., Супонева Н.А., Пирадов М.А.</copyright-holder><ali:free_to_read xmlns:ali="http://www.niso.org/schemas/ali/1.0/"/><license><ali:license_ref xmlns:ali="http://www.niso.org/schemas/ali/1.0/">https://creativecommons.org/licenses/by/4.0</ali:license_ref></license></permissions><self-uri xlink:href="https://annaly-nevrologii.com/pathID/article/view/814">https://annaly-nevrologii.com/pathID/article/view/814</self-uri><abstract xml:lang="en"><p>Metaplasticity (plasticity of synaptic plasticity) is defined as a change in the direction or degree of synaptic plasticity in response to preceding neuronal activity. Recent advances in brain stimulation methods have enabled us to non-invasively examine cortical metaplasticity, including research in a clinical setting. According to current knowledge, non-invasive neuromodulation affects synaptic plasticity by inducing cortical processes that are similar to long-term potentiation and depression. Two stimulation blocks are usually used to assess metaplasticity — priming and testing blocks. The technology of studying metaplasticity involves assessing the influence of priming on the testing protocol effect.</p> <p>Several dozen studies have examined the effects of different stimulation protocols in healthy persons. They found that priming can both enhance and weaken, or even change the direction of the testing protocol effect. The interaction between priming and testing stimulation depends on many factors: the direction of their effect, duration of the stimulation blocks, and the interval between them.</p> <p>Non-invasive brain stimulation can be used to assess aberrant metaplasticity in nervous system diseases, in order to develop new biomarkers. Metaplasticity disorders are found in focal hand dystonia, migraine with aura, multiple sclerosis, chronic disorders of consciousness, and age-related cognitive changes.</p> <p>The development of new, metaplasticity-based, optimized, combined stimulation protocols appears to be highly promising for use in therapeutic neuromodulation in clinical practice.</p></abstract><trans-abstract xml:lang="ru"><p>Метапластичность (пластичность синаптической пластичности) определяется как изменение направленности или выраженности синаптической пластичности в ответ на предшествующую нейрональную активность. Активное развитие в последние годы методов стимуляции мозга позволяет изучать метапластичность коры неинвазивно, в том числе в клинических условиях. Согласно современным представлениям, эффект неинвазивной нейромодуляции основан на её влиянии на синаптическую пластичность за счёт индукции в коре процессов, сходных с долговременной потенциацией и депрессией. Для оценки метапластичности обычно используются 2 блока стимуляции — прайминговый и тестовый. Суть технологии изучения метапластичности состоит в оценке влияния прайминга на эффект тестового протокола.</p> <p>В нескольких десятках исследований изучены эффекты различных комбинаций протоколов стимуляции у здоровых лиц, при этом показано, что прайминг может как усиливать, так и ослаблять или даже менять направленность эффекта тестового протокола. Особенности взаимодействия прайминговой и тестовой стимуляции зависят от многих факторов: направленности их эффекта, продолжительности блоков стимуляции и интервала между ними.</p> <p>Неинвазивная стимуляция мозга может использоваться для оценки аберрантной метапластичности при заболеваниях нервной системы с целью разработки новых биомаркеров. Нарушения метапластичности выявляются при писчем спазме, мигрени с аурой, рассеянном склерозе, хронических нарушениях сознания и возрастных когнитивных нарушениях.</p> <p>Большие перспективы связаны с разработкой новых, основанных на метапластичности оптимизированных комбинированных протоколов стимуляции для использования терапевтической нейромодуляции в клинической практике.</p></trans-abstract><kwd-group xml:lang="en"><kwd>synaptic plasticity</kwd><kwd>metaplasticity</kwd><kwd>non-invasive brain stimulation</kwd><kwd>neuromodulation</kwd><kwd>transcranial magnetic stimulation</kwd><kwd>depression</kwd></kwd-group><kwd-group xml:lang="ru"><kwd>синаптическая пластичность</kwd><kwd>метапластичность</kwd><kwd>неинвазивная стимуляция мозга</kwd><kwd>нейромодуляция</kwd><kwd>транскраниальная магнитная стимуляция</kwd><kwd>депрессия</kwd></kwd-group><funding-group><award-group><funding-source><institution-wrap><institution xml:lang="ru">Российский научный фонд</institution></institution-wrap><institution-wrap><institution xml:lang="en">Russian Science Foundation</institution></institution-wrap></funding-source><award-id>21-75-00040</award-id></award-group></funding-group></article-meta></front><body></body><back><ref-list><ref id="B1"><label>1.</label><mixed-citation>Пирадов М.А., Черникова Л.А., Супонева Н.А. Пластичность мозга и современные технологии нейрореабилитации. Вестник РАН. 2018; 88(4): 299–312. Piradov M.A., Chernikova L.A., Suponeva N.A. Brain plasticity and mo-dern neurorehabilitation technologies. Vestnik RAN. 2018; 88(4): 299–312. (In Russ.) DOI: 10.7868/S0869587318040023</mixed-citation></ref><ref id="B2"><label>2.</label><mixed-citation>Sweatt J.D. Neural plasticity and behavior — sixty years of conceptual advan- ces. J. Neurochem. 2016; 139(Suppl 2): 179–199. DOI: 10.1111/jnc.13580</mixed-citation></ref><ref id="B3"><label>3.</label><mixed-citation>Magee J.C., Grienberger C. Synaptic plasticity forms and functions. Annu. Rev. Neurosci. 2020; 43: 95–117. DOI: 10.1146/annurev-neuro-090919-022842</mixed-citation></ref><ref id="B4"><label>4.</label><mixed-citation>Bonfanti L., Charvet C.J. Brain plasticity in humans and model systems: advances, challenges, and future directions. Int. J. Mol. Sci. 2021; 22(17): 9358. DOI: 10.3390/ijms22179358</mixed-citation></ref><ref id="B5"><label>5.</label><mixed-citation>Diering G.H., Huganir R.L. The AMPA receptor code of synaptic plasticity. Neuron. 2018; 100(2): 314–329. DOI: 10.1016/j.neuron.2018.10.018</mixed-citation></ref><ref id="B6"><label>6.</label><mixed-citation>Cheyne J.E., Montgomery J.M. The cellular and molecular basis of in vivo synaptic plasticity in rodents. Am. J. Physiol. Cell Physiol. 2020; 318(6): C1264–C1283. DOI: 10.1152/ajpcell.00416.2019</mixed-citation></ref><ref id="B7"><label>7.</label><mixed-citation>Abraham W.C., Bear M.F. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 1996; 19(4): 126–130. DOI: 10.1016/s0166-2236(96)80018-x</mixed-citation></ref><ref id="B8"><label>8.</label><mixed-citation>Abraham W.C. Metaplasticity: tuning synapses and networks for plasticity. Nat. Rev. Neurosci. 2008; 9(5): 387. DOI: 10.1038/nrn2356</mixed-citation></ref><ref id="B9"><label>9.</label><mixed-citation>Bliss T.V., Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 1973; 232(2): 331–356. DOI: 10.1113/jphysiol.1973.sp010273</mixed-citation></ref><ref id="B10"><label>10.</label><mixed-citation>Ito M. Long-term depression. Annu. Rev. Neurosci. 1989; 12: 85–102. DOI: 10.1146/annurev.ne.12.030189.000505</mixed-citation></ref><ref id="B11"><label>11.</label><mixed-citation>Bolshakov V.Y., Siegelbaum S.A. Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science. 1994; 264(5162): 1148–1152. DOI: 10.1126/science.7909958</mixed-citation></ref><ref id="B12"><label>12.</label><mixed-citation>Linden D.J., Connor J.A. Long-term synaptic depression. Annu. Rev. Neurosci. 1995; 18: 319–357. DOI: 10.1146/annurev.ne.18.030195.001535</mixed-citation></ref><ref id="B13"><label>13.</label><mixed-citation>Гуляева Н.В. Молекулярные механизмы нейропластичности: расширяющаяся вселенная. Биохимия. 2017; 82(3): 365–371. Gulyaeva N.V. Molecular mechanisms of neuroplasticity: an expanding universe. Biokhimiya. 2017; 82(3): 365–371. (In Russ.)</mixed-citation></ref><ref id="B14"><label>14.</label><mixed-citation>Brown R.E., Donald O. Hebb and the Organization of behavior: 17 years in the writing. Mol. Brain. 2020; 13(1): 55. DOI: 10.1186/s13041-020-00567-8</mixed-citation></ref><ref id="B15"><label>15.</label><mixed-citation>Turrigiano G. Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb. Perspect. Biol. 2012; 4(1): a005736. DOI: 10.1101/cshperspect.a005736</mixed-citation></ref><ref id="B16"><label>16.</label><mixed-citation>Fernandes D., Carvalho A.L. Mechanisms of homeostatic plasticity in the excitatory synapse. J. Neurochem. 2016; 139(6): 973–996. DOI: 10.1111/jnc.13687</mixed-citation></ref><ref id="B17"><label>17.</label><mixed-citation>Vose L., Stanton P. Synaptic plasticity, metaplasticity and depression. Curr. Neuropharmacol. 2016; 15(1): 71–86. DOI: 10.2174/1570159x14666160202121111</mixed-citation></ref><ref id="B18"><label>18.</label><mixed-citation>Delvendahl I., Müller M. Homeostatic plasticity-a presynaptic perspective. Curr. Opin. Neurobiol. 2019; 54: 155–162. DOI: 10.1016/j.conb.2018.10.003</mixed-citation></ref><ref id="B19"><label>19.</label><mixed-citation>Coan E.J., Irving A.J., Collingridge G.L. Low-frequency activation of the NMDA receptor system can prevent the induction of LTP. Neurosci. Lett. 1989; 105(1-2): 205–10. DOI: 10.1016/0304-3940(89)90038-4</mixed-citation></ref><ref id="B20"><label>20.</label><mixed-citation>Huang Y.Y., Colino A., Selig D.K., Malenka R.C. The influence of prior synaptic activity on the induction of long-term potentiation. Science. 1992; 255(5045): 730–733. DOI: 10.1126/science.1346729</mixed-citation></ref><ref id="B21"><label>21.</label><mixed-citation>Larkman A., Hannay T., Stratford K., Jack J. Presynaptic release probability influences the locus of long-term potentiation. Nature. 1992; 360(6399): 70–73. DOI: 10.1038/360070a0</mixed-citation></ref><ref id="B22"><label>22.</label><mixed-citation>O’Dell T.J., Kandel E.R. Low-frequency stimulation erases LTP through an NMDA receptor-mediated activation of protein phosphatases. Learn. Mem. 1994; 1(2): 129–139.</mixed-citation></ref><ref id="B23"><label>23.</label><mixed-citation>Müller-Dahlhaus F., Ziemann U. Metaplasticity in human cortex. Neuroscientist. 2015; 21(2): 185–202. DOI: 10.1177/1073858414526645</mixed-citation></ref><ref id="B24"><label>24.</label><mixed-citation>Yger P., Gilson M. Models of metaplasticity: a review of concepts. Front. Comput. Neurosci. 2015; 9: 138. DOI: 10.3389/fncom.2015.00138</mixed-citation></ref><ref id="B25"><label>25.</label><mixed-citation>Thomson A.C., Sack A.T. How to design optimal accelerated rTMS protocols capable of promoting therapeutically beneficial metaplasticity. Front. Neurol. 2020; 11: 599918. DOI: 10.3389/fneur.2020.599918</mixed-citation></ref><ref id="B26"><label>26.</label><mixed-citation>Hulme S.R., Jones O.D., Abraham W.C. Emerging roles of metaplasticity in behaviour and disease. Trends Neurosci. 2013; 36(6): 353–362. DOI: 10.1016/j.tins.2013.03.007</mixed-citation></ref><ref id="B27"><label>27.</label><mixed-citation>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(1): 32–48. DOI: 10.1523/JNEUROSCI.02-01-00032.1982</mixed-citation></ref><ref id="B28"><label>28.</label><mixed-citation>Jedlicka P. Synaptic plasticity, metaplasticity and BCM theory. Bratisl. Lek. Listy. 2002; 103(4–5): 137–143.</mixed-citation></ref><ref id="B29"><label>29.</label><mixed-citation>Li J., Park E., Zhong L.R., Chen L. Homeostatic synaptic plasticity as a metaplasticity mechanism - a molecular and cellular perspective. Curr. Opin. Neurobiol. 2019; 54: 44–53. DOI: 10.1016/j.conb.2018.08.010</mixed-citation></ref><ref id="B30"><label>30.</label><mixed-citation>Hurley R., Machado L. Using tDCS priming to improve brain function: can metaplasticity provide the key to boosting outcomes? Neurosci. Biobehav. Rev. 2017; 83: 155–159. DOI: 10.1016/j.neubiorev.2017.09.029</mixed-citation></ref><ref id="B31"><label>31.</label><mixed-citation>Hassanzahraee M., Zoghi M., Jaberzadeh S. How different priming stimulations affect the corticospinal excitability induced by noninvasive brain stimulation techniques: a systematic review and meta-analysis. Rev. Neurosci. 2018; 29(8): 883–899. DOI: 10.1515/revneuro-2017-0111</mixed-citation></ref><ref id="B32"><label>32.</label><mixed-citation>Cantone M., Lanza G., Ranieri F. et al. Editorial: non-invasive brain stimulation in the study and modulation of metaplasticity in neurological disorders. Front. Neurol. 2021; 12: 721906. DOI: 10.3389/fneur.2021.721906</mixed-citation></ref><ref id="B33"><label>33.</label><mixed-citation>Chervyakov A.V., Chernyavsky A.Y., Sinitsyn D.O., Piradov M.A. Possible mechanisms underlying the therapeutic effects of transcranial magnetic stimulation. Front. Hum. Neurosci. 2015; 9: 303. DOI: 10.3389/fnhum.2015.00303</mixed-citation></ref><ref id="B34"><label>34.</label><mixed-citation>Valero-Cabré A., Amengual J.L., Stengel C. et al. Transcranial magnetic stimulation in basic and clinical neuroscience: a comprehensive review of fundamental principles and novel insights. Neurosci. Biobehav. Rev. 2017; 83: 381–404. DOI: 10.1016/j.neubiorev.2017.10.006</mixed-citation></ref><ref id="B35"><label>35.</label><mixed-citation>Burke M.J., Fried P.J., Pascual-Leone A. Transcranial magnetic stimulation: Neurophysiological and clinical applications. Handb. Clin. Neurol. 2019; 163: 73–92. DOI: 10.1016/B978-0-12-804281-6.00005-7</mixed-citation></ref><ref id="B36"><label>36.</label><mixed-citation>Larson J., Munkácsy E. Theta-burst LTP. Brain Res. 2015; 1621: 38–50. DOI: 10.1016/j.brainres.2014.10.034</mixed-citation></ref><ref id="B37"><label>37.</label><mixed-citation>Suppa A., Huang Y.Z., Funke K. et al. Ten years of theta burst stimulation in humans: established knowledge, unknowns and prospects. Brain Stimul. 2016; 9(3): 323–335. DOI: 10.1016/j.brs.2016.01.006</mixed-citation></ref><ref id="B38"><label>38.</label><mixed-citation>Huang Y.Z., Edwards M.J., Rounis E. et al. Theta burst stimulation of the human motor cortex. Neuron. 2005; 45(2): 201–206. DOI: 10.1016/j.neuron.2004.12.033</mixed-citation></ref><ref id="B39"><label>39.</label><mixed-citation>Rounis E., Huang Y.Z. Theta burst stimulation in humans: a need for better understanding effects of brain stimulation in health and disease. Exp. Brain Res. 2020; 238(7-8): 1707–1714. DOI: 10.1007/s00221-020-05880-1</mixed-citation></ref><ref id="B40"><label>40.</label><mixed-citation>Wischnewski M., Schutter D.J. Efficacy and time course of theta burst sti- mulation in healthy humans. Brain Stimul. 2015; 8(4): 685–692. DOI: 10.1016/j.brs.2015.03.004</mixed-citation></ref><ref id="B41"><label>41.</label><mixed-citation>Classen J., Wolters A., Stefan K. et al. Paired associative stimulation. Suppl. Clin. Neurophysiol. 2004; 57: 563–569.</mixed-citation></ref><ref id="B42"><label>42.</label><mixed-citation>Stagg C.J., Antal A., Nitsche M.A. Physiology of transcranial direct current stimulation. J. ECT. 2018; 34(3): 144–152. DOI: 10.1097/YCT.0000000000000510</mixed-citation></ref><ref id="B43"><label>43.</label><mixed-citation>Chase H.W., Boudewyn M.A., Carter C.S., Phillips M.L. Transcranial direct current stimulation: a roadmap for research, from mechanism of action to clinical implementation. Mol. Psychiatry. 2020; 25(2): 397–407. DOI: 10.1038/s41380-019-0499-9</mixed-citation></ref><ref id="B44"><label>44.</label><mixed-citation>Lang N., Siebner H.R., Ernst D. et al. Preconditioning with transcranial direct current stimulation sensitizes the motor cortex to rapid-rate transcranial magnetic stimulation and controls the direction of after-effects. Biol. Psychiatry. 2004; 56(9): 634–639. DOI: 10.1016/j.biopsych.2004.07.017</mixed-citation></ref><ref id="B45"><label>45.</label><mixed-citation>Cosentino G., Fierro B., Paladino P. et al. Transcranial direct current stimulation preconditioning modulates the effect of high-frequency repetitive transcranial magnetic stimulation in the human motor cortex. Eur. J. Neurosci. 2012; 35(1): 119–124. DOI: 10.1111/j.1460-9568.2011.07939.x</mixed-citation></ref><ref id="B46"><label>46.</label><mixed-citation>Siebner H.R., Lang N., Rizzo V. et al. Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J. Neurosci. 2004; 24(13): 3379–85. DOI: 10.1523/JNEUROSCI.5316-03.2004</mixed-citation></ref><ref id="B47"><label>47.</label><mixed-citation>Todd G., Flavel S.C., Ridding M.C. Priming theta-burst repetitive transcranial magnetic stimulation with low- and high-frequency stimulation. Exp. Brain Res. 2009; 195(2): 307–315. DOI: 10.1007/s00221-009-1791-8</mixed-citation></ref><ref id="B48"><label>48.</label><mixed-citation>Gentner R., Wankerl K., Reinsberger C. et al. Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. Cereb Cortex. 2008; 18(9): 2046–2053. DOI: 10.1093/cercor/bhm239</mixed-citation></ref><ref id="B49"><label>49.</label><mixed-citation>Gamboa O.L., Antal A., Moliadze V., Paulus W. Simply longer is not better: reversal of theta burst after-effect with prolonged stimulation. Exp. Brain Res. 2010; 204(2): 181–187. DOI: 10.1007/s00221-010-2293-4</mixed-citation></ref><ref id="B50"><label>50.</label><mixed-citation>Tse N.Y., Goldsworthy M.R., Ridding M.C. et al. The effect of stimulation interval on plasticity following repeated blocks of intermittent theta burst stimulation. Sci. Rep. 2018; 8(1): 8526. DOI: 10.1038/s41598-018-26791-w</mixed-citation></ref><ref id="B51"><label>51.</label><mixed-citation>Gamboa O.L., Antal A., Laczo B. et al. Impact of repetitive theta burst stimulation on motor cortex excitability. Brain Stimul. 2011; 4(3): 145–151. DOI: 10.1016/j.brs.2010.09.008</mixed-citation></ref><ref id="B52"><label>52.</label><mixed-citation>Mastroeni C., Bergmann T.O., Rizzo V. et al. Brain-derived neurotrophic factor—a major player in stimulation-induced homeostatic metaplasticity of human motor cortex? PLoS One. 2013; 8(2): e57957. DOI: 10.1371/journal.pone.0057957</mixed-citation></ref><ref id="B53"><label>53.</label><mixed-citation>Opie G.M., Vosnakis E., Ridding M.C. et al. Priming theta burst stimulation enhances motor cortex plasticity in young but not old adults. Brain Stimul. 2017; 10(2): 298–304. DOI: 10.1016/j.brs.2017.01.003</mixed-citation></ref><ref id="B54"><label>54.</label><mixed-citation>Frey U., Schollmeier K., Reymann K.G., Seidenbecher T. Asymptotic hippocampal long-term potentiation in rats does not preclude additional potentiation at later phases. Neuroscience. 1995; 67(4): 799–807. DOI: 10.1016/0306-4522(95)00117-2</mixed-citation></ref><ref id="B55"><label>55.</label><mixed-citation>Kramár E.A., Babayan A.H., Gavin C.F. et al. Synaptic evidence for the efficacy of spaced learning. Proc. Natl. Acad. Sci. USA. 2012; 109(13): 5121–5126. DOI: 10.1073/pnas.1120700109</mixed-citation></ref><ref id="B56"><label>56.</label><mixed-citation>Cao G., Harris K.M. Augmenting saturated LTP by broadly spaced episodes of theta-burst stimulation in hippocampal area CA1 of adult rats and mice. J. Neurophysiol. 2014; 112(8): 1916–1924. DOI: 10.1152/jn.00297.2014</mixed-citation></ref><ref id="B57"><label>57.</label><mixed-citation>Bergmann T.O. Brain state-dependent brain stimulation. Front. Psychol. 2018; 9: 2108. DOI: 10.3389/fpsyg.2018.02108</mixed-citation></ref><ref id="B58"><label>58.</label><mixed-citation>Baur D., Galevska D., Hussain S. et al. Induction of LTD-like corticospinal plasticity by low-frequency rTMS depends on pre-stimulus phase of sensorimotor μ-rhythm. Brain Stimul. 2020; 13(6): 1580–1587. DOI: 10.1016/j.brs.2020.09.005</mixed-citation></ref><ref id="B59"><label>59.</label><mixed-citation>Guerra A., López-Alonso V., Cheeran B., Suppa A. Variability in non-invasive brain stimulation studies: Reasons and results. Neurosci. Lett. 2020; 719: 133330. DOI: 10.1016/j.neulet.2017.12.058</mixed-citation></ref><ref id="B60"><label>60.</label><mixed-citation>Ozdemir R.A., Boucher P., Fried P.J. et al. Reproducibility of cortical response modulation induced by intermittent and continuous theta-burst stimulation of the human motor cortex. Brain Stimul. 2021; 14(4): 949–964. DOI: 10.1016/j.brs.2021.05.013</mixed-citation></ref><ref id="B61"><label>61.</label><mixed-citation>Chervyakov A.V., Sinitsyn D.O., Piradov M.A. Variability of neuronal responses: types and functional significance in neuroplasticity and neural darwinism. Front. Hum. Neurosci. 2016; 10: 603. DOI: 10.3389/fnhum.2016.00603</mixed-citation></ref><ref id="B62"><label>62.</label><mixed-citation>Li S., Jin M., Koeglsperger T. et al. Soluble Aβ oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J. Neurosci. 2011; 31(18): 6627–6638. DOI: 10.1523/JNEUROSCI.0203-11.2011</mixed-citation></ref><ref id="B63"><label>63.</label><mixed-citation>Rönicke R., Mikhaylova M., Rönicke S. et al. Early neuronal dysfunction by amyloid β oligomers depends on activation of NR2B-containing NMDA receptors. Neurobiol. Aging. 2011; 32(12): 2219–2228. DOI: 10.1016/j.neurobiolaging.2010.01.011</mixed-citation></ref><ref id="B64"><label>64.</label><mixed-citation>Balducci C., Tonini R., Zianni E. et al. Cognitive deficits associated with alteration of synaptic metaplasticity precede plaque deposition in AβPP23 transgenic mice. J. Alzheimers Dis. 2010; 21(4): 1367–1381. DOI: 10.3233/jad-2010-100675</mixed-citation></ref><ref id="B65"><label>65.</label><mixed-citation>Giordano N., Iemolo A., Mancini M. et al. Motor learning and metaplasticity in striatal neurons: relevance for Parkinson’s disease. Brain. 2018; 141(2): 505–520. DOI: 10.1093/brain/awx351</mixed-citation></ref><ref id="B66"><label>66.</label><mixed-citation>Chiamulera C., Piva A., Abraham W.C. Glutamate receptors and metaplasticity in addiction. Curr. Opin. Pharmacol. 2021; 56: 39–45. DOI: 10.1016/j.coph.2020.09.005</mixed-citation></ref><ref id="B67"><label>67.</label><mixed-citation>Quartarone A., Rizzo V., Bagnato S. et al. Homeostatic-like plasticity of the primary motor hand area is impaired in focal hand dystonia. Brain. 2005; 128 (Pt 8): 1943–1950. DOI: 10.1093/brain/awh527</mixed-citation></ref><ref id="B68"><label>68.</label><mixed-citation>Kang J.S., Terranova C., Hilker R. et al. Deficient homeostatic regulation of practice-dependent plasticity in writer’s cramp. Cereb. Cortex. 2011; 21(5): 1203–1212. DOI: 10.1093/cercor/bhq204</mixed-citation></ref><ref id="B69"><label>69.</label><mixed-citation>Antal A., Lang N., Boros K. et al. Homeostatic metaplasticity of the motor cortex is altered during headache-free intervals in migraine with aura. Cereb. Cortex. 2008; 18(11): 2701–2705. DOI: 10.1093/cercor/bhn032</mixed-citation></ref><ref id="B70"><label>70.</label><mixed-citation>Baione V., Belvisi D., Cortese A. et al. Cortical M1 plasticity and metaplasticity in patients with multiple sclerosis. Mult. Scler. Relat. Disord. 2020; 38: 101494. DOI: 10.1016/j.msard.2019.101494</mixed-citation></ref><ref id="B71"><label>71.</label><mixed-citation>Naro A., Bramanti A., Leo A. et al. Metaplasticity: a promising tool to disentangle chronic disorders of consciousness differential diagnosis. Int. J. Neural. Syst. 2018; 28(6): 1750059. DOI: 10.1142/S0129065717500599</mixed-citation></ref><ref id="B72"><label>72.</label><mixed-citation>Sundman M.H., Lim K., Ton That V. et al. Transcranial magnetic stimulation reveals diminished homoeostatic metaplasticity in cognitively impaired adults. Brain Commun. 2020; 2(2): fcaa203. DOI: 10.1093/braincomms/fcaa203</mixed-citation></ref><ref id="B73"><label>73.</label><mixed-citation>Бакулин И.С., Пойдашева А.Г., Лагода Д.Ю. и др. Перспективы развития терапевтической транскраниальной магнитной стимуляции. Нервные болезни. 2021; 4: 3–10. Bakulin I.S., Poydasheva A.G., Lagoda D.Yu. et al. Prospects for the development of therapeutic transcranial magnetic stimulation. Nervnye bolezni. 2021; 4: 3–10. (In Russ.) DOI: 10.24412/2226-0757-2021-12371</mixed-citation></ref><ref id="B74"><label>74.</label><mixed-citation>Hordacre B., Ridding M.C., Goldsworthy M.R. Response variability to non-invasive brain stimulation protocols. Clin. Neurophysiol. 2015; 126(12): 2249–2250. DOI: 10.1016/j.clinph.2015.04.052</mixed-citation></ref><ref id="B75"><label>75.</label><mixed-citation>Fitzgerald P.B., Hoy K., McQueen S. et al. Priming stimulation enhances the effectiveness of low-frequency right prefrontal cortex transcranial magnetic stimulation in major depression. J. Clin. Psychopharmacol. 2008; 28(1): 52–58. DOI: 10.1097/jcp.0b013e3181603f7c</mixed-citation></ref><ref id="B76"><label>76.</label><mixed-citation>Bolognini N., Pascual-Leone A., Fregni F. Using non-invasive brain stimulation to augment motor training-induced plasticity. J. Neuroeng. Rehabil. 2009; 6: 8. DOI: 10.1186/1743-0003-6-8</mixed-citation></ref><ref id="B77"><label>77.</label><mixed-citation>Cassidy J.M., Gillick B.T., Carey J.R. Priming the brain to capitalize on meta- plasticity in stroke rehabilitation. Phys. Ther. 2014; 94(1): 139–150. DOI: 10.2522/ptj.20130027</mixed-citation></ref><ref id="B78"><label>78.</label><mixed-citation>Takeuchi N, Izumi S. Combinations of stroke neurorehabilitation to facilitate motor recovery: perspectives on Hebbian plasticity and homeostatic metaplasticity. Front. Hum. Neurosci. 2015; 9: 349. DOI: 10.3389/fnhum.2015.00349</mixed-citation></ref><ref id="B79"><label>79.</label><mixed-citation>Kang N., Summers J.J., Cauraugh J.H. Transcranial direct current stimulation facilitates motor learning post-stroke: a systematic review and meta-analysis. J. Neurol. Neurosurg. Psychiatry. 2016; 87(4): 345–355. DOI: 10.1136/jnnp-2015-311242</mixed-citation></ref><ref id="B80"><label>80.</label><mixed-citation>Giacobbe V., Krebs H.I., Volpe B.T. et al. Transcranial direct current stimulation (tDCS) and robotic practice in chronic stroke: the dimension of timing. NeuroRehabilitation. 2013; 33(1): 49–56. DOI: 10.3233/NRE-130927</mixed-citation></ref><ref id="B81"><label>81.</label><mixed-citation>Cabral M.E., Baltar A., Borba R. et al. Transcranial direct current stimulation: before, during, or after motor training? Neuroreport. 2015; 26(11): 618–622. DOI: 10.1097/WNR.0000000000000397</mixed-citation></ref><ref id="B82"><label>82.</label><mixed-citation>Avenanti A., Coccia M., Ladavas E. et al. Low-frequency rTMS promotes use-dependent motor plasticity in chronic stroke: a randomized trial. Neurology. 2012; 78(4): 256–264. DOI: 10.1212/WNL.0b013e3182436558</mixed-citation></ref><ref id="B83"><label>83.</label><mixed-citation>Carey J.R., Deng H., Gillick B.T. et al. Serial treatments of primed low-frequency rTMS in stroke: characteristics of responders vs. nonresponders. Restor. Neurol. Neurosci. 2014; 32(2): 323–335. DOI: 10.3233/RNN-130358</mixed-citation></ref><ref id="B84"><label>84.</label><mixed-citation>Cassidy J.M., Chu H., Anderson D.C. et al. A comparison of primed low-frequency repetitive transcranial magnetic stimulation treatments in chronic stroke. Brain Stimul. 2015; 8(6): 1074–1084. DOI: 10.1016/j.brs.2015.06.007</mixed-citation></ref><ref id="B85"><label>85.</label><mixed-citation>Zhang J.J., Fong K.N.K. Effects of priming intermittent theta burst stimulation on upper limb motor recovery after stroke: study protocol for a proof-of-concept randomised controlled trial. BMJ Open. 2020; 10(3): e035348. DOI: 10.1136/bmjopen-2019-035348</mixed-citation></ref><ref id="B86"><label>86.</label><mixed-citation>Cheng I., Scarlett H., Zhang M., Hamdy S. Preconditioning human pharyngeal motor cortex enhances directional metaplasticity induced by repetitive transcranial magnetic stimulation. J. Physiol. 2020; 598(22): 5213–5230. DOI: 10.1113/JP279977</mixed-citation></ref><ref id="B87"><label>87.</label><mixed-citation>Sonmez A.I., Camsari D.D., Nandakumar A.L. et al. Accelerated TMS for Depression: A systematic review and meta-analysis. Psychiatry Res. 2019; 273: 770–781. DOI: 10.1016/j.psychres.2018.12.041</mixed-citation></ref><ref id="B88"><label>88.</label><mixed-citation>Cheng C.M., Li C.T., Tsai S.J. Current updates on newer forms of transcranial magnetic stimulation in major depression. Adv. Exp. Med. Biol. 2021; 1305: 333–349. DOI: 10.1007/978-981-33-6044-0_18</mixed-citation></ref><ref id="B89"><label>89.</label><mixed-citation>Cole E.J., Phillips A.L., Bentzley B.S. et al. Stanford Neuromodulation Therapy (SNT): a double-blind randomized controlled trial. Am. J. Psychiatry. 2022; 179(2):132–141. DOI: 10.1176/appi.ajp.2021.20101429</mixed-citation></ref><ref id="B90"><label>90.</label><mixed-citation>Baeken C., Vanderhasselt M.A., Remue J. et al. Intensive HF-rTMS treatment in refractory medication-resistant unipolar depressed patients. J. Affect. Disord. 2013; 151(2): 625–631. DOI: 10.1016/j.jad.2013.07.008</mixed-citation></ref><ref id="B91"><label>91.</label><mixed-citation>Duprat R., Desmyter S., Rudi de R. et al. Accelerated intermittent theta burst stimulation treatment in medication-resistant major depression: a fast road to remission? J. Affect. Disord. 2016; 200: 6–14. DOI: 10.1016/j.jad.2016.04.015</mixed-citation></ref><ref id="B92"><label>92.</label><mixed-citation>Desmyter S., Duprat R., Baeken C. et al. Accelerated intermittent theta burst stimulation for suicide risk in therapy-resistant depressed patients: a randomized, sham-controlled trial. Front. Hum. Neurosci. 2016; 10: 480. DOI: 10.3389/fnhum.2016.00480</mixed-citation></ref><ref id="B93"><label>93.</label><mixed-citation>Blumberger D.M., Vila-Rodriguez F., Wang W. et al. A randomized sham controlled comparison of once vs twice-daily intermittent theta burst stimulation in depression: A Canadian rTMS treatment and biomarker network in depression (CARTBIND) study. Brain Stimul. 2021; 14(6): 1447–1455. DOI: 10.1016/j.brs.2021.09.003</mixed-citation></ref><ref id="B94"><label>94.</label><mixed-citation>Fitzgerald P.B., Hoy K.E., Elliot D. et al. Accelerated repetitive transcranial magnetic stimulation in the treatment of depression. Neuropsychopharmacology. 2018; 43(7): 1565–1572. DOI: 10.1038/s41386-018-0009-9</mixed-citation></ref><ref id="B95"><label>95.</label><mixed-citation>Loo C.K., Mitchell P.B., McFarquhar T.F et al. A sham-controlled trial of the efficacy and safety of twice-daily rTMS in major depression. Psychol. Med. 2007; 37(3): 341–349. DOI: 10.1017/S0033291706009597</mixed-citation></ref><ref id="B96"><label>96.</label><mixed-citation>Cole E.J., Stimpson K.H., Bentzley B.S. et al. Stanford accelerated intelligent neuromodulation therapy for treatment-resistant depression. Am. J. Psychiatry. 2020; 177(8): 716–726. DOI: 10.1176/appi.ajp.2019.19070720</mixed-citation></ref></ref-list></back></article>
