Neuromuscular DiseasesNeuromuscular DiseasesНервно-мышечные болезни2222-87212413-0443Publishing House ABV Press37410.17650/2222-8721-2020-10-1-64-74ORIGINAL REPORTSОРИГИНАЛЬНЫЕ ИССЛЕДОВАНИЯDiagnostic capabilities of transcranial magnetic stimulation to predict motor recovery after a strokeДиагностические возможности транскраниальной магнитной стимуляции для прогнозирования двигательного восстановления после инсультаhttps://orcid.org/0000-0001-5347-5948NazarovaM. A.НазароваМ. А.
Russian Federation

3 Krivokolenniy sidewalk, Moscow 101000, Russia

Build. 10, 1 Ostrovityanova St., Moscow 117342, Russia

Мария Александровна Назарова

Россия, 101000 Москва, Кривоколенный переулок, 3

Россия, 117342 Москва, ул. Островитянова, 1, стр. 10

chantante@gmail.comhttps://orcid.org/0000-0003-4102-1580NovikovP. A.НовиковП. А.
Russian Federation

3 Krivokolenniy sidewalk, Moscow 101000, Russia

Россия, 117342 Москва, ул. Островитянова, 1, стр. 10

https://orcid.org/0000-0001-6082-3859NikulinV. V.НикулинВ. В.
Russian Federation

3 Krivokolenniy sidewalk, Moscow 101000, Russia

1a Stefanstrasse, Leipzig 04103, Germany

Россия, 117342 Москва, ул. Островитянова, 1, стр. 10

Германия, 04103 Лейпциг, Штефанштрассе, 1a

IvanovaG. E.ИвановаГ. Е.
Russian Federation

Build. 10, 1 Ostrovityanova St., Moscow 117342, Russia

Россия, 117342 Москва, ул. Островитянова, 1, стр. 10

Centre for Cognition and Decision making, Institute for Cognitive Neuroscience, National Research University Higher School of EconomicsЦентр нейроэкономики и когнитивных исследований, Институт когнитивных нейронаук, Национальный исследовательский университет «Высшая школа экономики»Federal centre for brain and neurotechnology of the Ministry of Health of RussiaФГБУ «Федеральный центр мозга и нейротехнологий» Минздрава РоссииDepartment of Neurology, Max Planck Institute for Human Cognitive and Brain SciencesДепартамент неврологии, Институт Макса Планка по изучению когнитивных и мозговых процессов0306202010164740306202003062020Copyright ©; 2020, Nazarova M.A., Novikov P.A., Nikulin V.V., Ivanova G.E.Copyright ©; 2020, Назарова М.А., Новиков П.А., Никулин В.В., Иванова Г.Е.2020Nazarova M.A., Novikov P.A., Nikulin V.V., Ivanova G.E.Назарова М.А., Новиков П.А., Никулин В.В., Иванова Г.Е.https://creativecommons.org/licenses/by/4.0https://nmb.abvpress.ru/jour/article/view/374

Transcranial magnetic stimulation is a method of focal non-invasive brain stimulation, characterized by high spatial and temporal resolution. To date, diagnostic transcranial magnetic stimulation has been used in clinical practice primarily to assess an involvement of the upper motor neurons and to measure the velocity of the neuronal impulse propagation. However, in the last 10 years, a possible range of transcranial magnetic stimulation diagnostic applications has significantly expanded. Many transcranial magnetic stimulation approaches are coming from scientific laboratories to clinical practice due to an increased availability of transcranial magnetic stimulation equipment, in particular, magnetic resonance imaging navigation for transcranial magnetic stimulation and a combination of the transcranial magnetic stimulation with electroencephalography and also due to an increased awareness of the clinicians. The diagnostic potential of transcranial magnetic stimulation in relation to motor recovery after a stroke can be classified into 4 directions:

1) assessment of the vertical tracts integrity (primarily, the cortico-spinal tract); 2) an assessment of the cortical excitation-inhibition balance;

3) probing of the functional and effective connectivity among brain regions (primarily, cortical convexity and cerebellum);

4) motor mapping to evaluate cortical reorganization.

In this article we will present these 4 directions of the transcranial magnetic stimulation application to study motor system pathophysiology and to predict motor outcome in stroke, including both existing and developing approaches.

Транскраниальная магнитная стимуляция – метод фокальной неинвазивной стимуляции мозга, характеризующийся высоким пространственным и временным разрешением. До настоящего времени в рутинной клинической практике диагностическая транс- краниальная магнитная стимуляция использовалась в первую очередь для оценки вовлеченности центральных мотонейронов и измерения скорости проведения по различным участкам нервной системы. Однако в последние 10 лет возможный спектр диагностического применения этого метода существенно расширился. Многие подходы транскраниальной магнитной стимуляции переходят из научных лабораторий в клиническую практику благодаря повышению доступности оборудования, в особенности транскраниальной магнитной стимуляции с навигацией по данным магнитно-резонансной томографии и комбинации транскраниальной магнитной стимуляции c электроэнцефалографией, а также благодаря повышению информированности специалистов. Диагностический потенциал транскраниальной магнитной стимуляции в отношении двигательных нарушений после инсульта можно условно разделить на 4 направления: 1) оценка сохранности вертикальных трактов, в первую очередь кортико-спинального тракта из конкретной зоны коры; 2) оценка баланса возбуждения–торможения в коре; 3) оценка функциональной и эффективной связности между доступными для транскраниальной магнитной стимуляции регионами мозга (прежде всего конвекситальные зоны коры и мозжечок); 4) картирование двигательных областей коры для оценки пластических перестроек. В настоящей статье рассмотрены эти 4 направления, включая как существующие, так и разрабатываемые диагностические подходы транскраниальной магнитной стимуляции для исследования патофизиологии двигательной системы в целом и для пред- сказания двигательного восстановления после инсульта в частности.

transcranial magnetic stimulationstrokemotor rehabilitationmotor recovery prognosisтранскраниальная магнитная стимуляцияинсультдвигательное восстановлениепрогноз двигательного восстановленияOvadia-Caro S., Khalil A.A., Sehm B. et al. Predicting the response to noninvasive brain stimulation in stroke. Front Neurol 2019;10:302. DOI: 10.3389/fneur.2019.00302. PMID: 31001190.Byblow W.D., Stinear C.M., Barber P.A. et al. Proportional recovery after stroke depends on corticomotor integrity. Ann Neurol 2015;78(6):848–59. DOI: 10.1002/ana.24472. PMID: 26150318.Kwakkel G., Winters C., Van Wegen E.E.H. et al. Effects of unilateral upper limb training in two distinct prognostic groups early after stroke: The EXPLICIT-Stroke randomized clinical trial. Neurorehabil Neural Repair 2016;30(9):804–16. DOI: 10.1177/1545968315624784. PMID: 26747128.Sankarasubramanian V., Machado A.G., Conforto A.B. et al. Inhibition versus facilitation of contralesional motor cortices in stroke: deriving a model to tailor brain stimulation. Clin Neurophysiol 2017;128(6):892–902. DOI: 10.1016/j.clinph.2017.03.030. PMID: 28402865.Ruohonen J., Karhu J. Navigated transcranial magnetic stimulation. Neurophysiol Clin Neurophysiol 2010;40(1):7–17. DOI: 10.1016/j.neucli.2010.01.006. PMID: 20230931.Romero M.C., Davare M., Armendariz M. et al. Neural effects of transcranial magnetic stimulation at the single-cell level. Nat Commun 2019;10(1):2642. DOI: 10.1038/s41467-019-10638-7. PMID: 31201331.Epstein C.M., Wassermann E.M., Ziemann U. Oxford Handbook of Transcranial Stimulation. Oxford University Press. 764 p. DOI: 10.1001/archneurol.2010.93.Rossini P.M., Burke D., Chen R. et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 2015;126(6):1071–107. DOI: 10.1016/j.clinph.2015.02.001. PMID: 25797650.Conforto A.B., Moraes M.S., Amaro E. et al. Increased variability of motor cortical excitability to transcranial magnetic stimulation in migraine: a new clue to an old enigma. J Headache Pain 2012;13(1):29–37. DOI: 10.1007/s10194-011-0379-4. PMID: 21881905.Fedele T., Blagovechtchenski E., Nazarova M. et al. Long-Range Temporal Correlations in the amplitude of alpha oscillations predict and reflect strength of intracortical facilitation: Combined TMS and EEG study. Neuroscience 2016;331:109–19. DOI: 10.1016/j.neuroscience.2016.06.015. PMID: 27318302.Новиков П.А., Решетников М.Л., Назарова М.А. и др. Нейронавигация TMSphi. Свидетельство о государственной регистрации программы для ЭВМ RU2020611493 2020; заявл. 27.12.2019; опубл. 03.02.2020. Бюл. №2, Реестр программ для ЭВМ. 1 с. [Novikov P.A., Reshetnikov M.L., Nazarova M.A. et al. Neuronavigation TMSphi. Certificate of state registration of a computer program RU2020611493 2020; appl. 27.12.2019; published 03.02.2020. Bull. №2, Computer program registry. 1 p. (In Russ.)].Boyd L.A., Hayward K.S., Ward N.S. et al. Biomarkers of stroke recovery: consensus-based core recommendations from the stroke recovery and rehabilitation roundtable. Neurorehabil Neural Repair 2017;31(10–11):864–76. DOI: 10.1177/1545968317732680. PMID: 29233071.Stinear C.M., Byblow W.D., Ackerley S.J. et al. PREP2: a biomarker-based algorithm for predicting upper limb function after stroke. Ann Clin Transl Neurol 2017; 4(11):811–20. DOI: 10.1002/acn3.488. PMID: 29159193.Назарова М.А. Мультимодальная оценка реорганизации двигательной системы руки после полушарного инсульта: МРТ-ТМС исследование. Автореф. дис. … канд. мед. наук. М., 2015. [Nazarova M.A. Multimodal assessment of the reorganization of the hand motor system after a hemispheric stroke: MRI- TMS study. Abstract. dis. … сand. med. sciences. Moscow, 2015. (In Russ.)].Stinear C.M., Barber P.A., Smale P.R. et al. Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain 2007;130(1):170–80. DOI: 10.1093/brain/awl333. PMID: 17148468.Koski L., Mernar T.J., Dobkin B.H. Immediate and long-term changes in corticomotor output in response to rehabilitation: correlation with functional improvements in chronic stroke. Neurorehabil Neural Repair 2004;18(4):230–49. DOI: 10.1177/1545968304269210. PMID: 15537994.Hayward K.S., Lohse K.R., Bernhardt J. et al. Characterising Arm Recovery in People with Severe Stroke (CARPSS): protocol for a 12-month observational study of clinical, neuroimaging and neurophysiological biomarkers. BMJ Open 2018;8(11):e26435. DOI: 10.1136/bmjopen-2018-026435. PMID: 30478130.Stinear C.M., Barber P.A., Petoe M. et al. The PREP algorithm predicts potential for upper limb recovery after stroke. Brain 2012;135(8):2527–35. DOI: 10.1093/brain/aws146. PMID: 22689909.Hoonhorst M.H.J., Nijland R.H.M., van den Berg P.J.S. et al. Does transcranial magnetic stimulation have an added value to clinical assessment in predicting upperlimb function very early after severe stroke? Neurorehabil Neural Repair 2018;32(8):682–90. DOI: 10.1177/1545968318785044. PMID: 29972088.Lee J.W., Kwon Y.M., Jang S.H. Predictability of motor outcome according to the time of motor evoked potentials from the onset of stroke in patients with putaminal hemorrhage. Ann Rehabil Med 2015;39(4):553–9. DOI:10.5535/arm.2015.39.4.553. PMID: 26361591.Yarossi M., Patel J., Qiu Q. et al. The association between reorganization of bilateral M1 topography and function in response to early intensive hand focused upper limb rehabilitation following stroke is dependent on ipsilesional corticospinal tract integrity. Front Neurol Frontiers 2019;10:258. DOI: 10.3389/fneur.2019.00258. PMID: 30972004.Schambra H.M., Xu J., Branscheidt M. et al. Differential poststroke motor recovery in an arm versus hand muscle in the absence of motor evoked potentials. Neurorehabil Neural Repair 2019;33(7):568–80. DOI: 10.1177/1545968319850138. PMID: 31170880.Nazarova M., Kulikova S., Piradov M. et al. Multimodal DTI-TMS assessment of the motor system in patients with chronic ischemic stroke. BioRxiv Cold Spring Harbor Laboratory, 2019. DOI: 10.1101/2019.12.24.886754. URL: https://www.biorxiv.org/content/10.1101/2019.12.24.886754v1.article-info.Kesar T.M., Stinear J.W., Wolf S.L. et al. The use of transcranial magnetic stimulation to evaluate cortical excitability of lower limb musculature: сhallenges and opportunities. Restor Neurol Neurosci 2018;36(3):333–48. DOI: 10.3233/RNN-170801. PMID: 29758954.Ziemann U., Reis J., Schwenkreis P. et al. TMS and drugs revisited 2014. Clin Neurophysiol 2015;126(10):1847–68. DOI: 10.1016/j.clinph.2014.08.028. PMID: 25534482.Di Pino G., Pellegrino G., Assenza G. et al. Modulation of brain plasticity in stroke: A novel model for neurorehabilitation . Nat Rev Neurol 2014;10(10):597–608. DOI: 10.1038/nrneurol.2014.162. PMID: 25201238.Lefaucheur J.-P., Aleman A., Baeken C. et al. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS): an update (2014–2018). Clin Neurophysiol 2020;131(2):474–528. DOI: 10.1016/j.clinph.2019.11.002. PMID: 31901449.Krakauer J.W., Carmichael S.T. Broken movement : the neurobiology of motor recovery after stroke. The MIT press, 2017. 269 p.Harvey R.L., Edwards D., Dunning K. et al. Randomized sham-controlled trial of navigated repetitive transcranial magnetic stimulation for motor recovery in stroke. Stroke 2018;49(9):2138–46. DOI: 10.1161/STROKEAHA.117.020607. PMID: 30354990.Hermsen A.M., Haag A., Duddek C. et al. Test-retest reliability of single and paired pulse transcranial magnetic stimulation parameters in healthy subjects. J Neurol Sci 2016;362:209–16. DOI: 10.1016/j.jns.2016.01.039. PMID: 26944150.Rossini P.M., Di Iorio R., Bentivoglio M. et al. Methods for analysis of brain connectivity: an IFCN-sponsored review . Clin Neurophysiol 2019;130(10):1833–58. DOI: 10.1016/j.clinph.2019.06.006. PMID: 31401492.Rosso C., Lamy J.-C.C. Does resting motor threshold predict motor hand recovery after stroke? Front Neurol 2018;9:1020. DOI: 10.3389/fneur.2018.01020. PMID: 30555404.Rotenberg A., Horvath J., Pascual-Leone A. Transcranial Magnetic Stimulation Series Editor. Humana Press, 2014. 386 p.Beck S., Hallett M. Surround inhibition in the motor system. Exp Brain Res 2011;210(2):165–72. DOI: 10.1007/s00221-011-2610-6. PMID: 21424259.McDonnell M.N., Stinear C.M. TMS measures of motor cortex function after stroke: A meta-analysis. Brain Stimul 2017;10(4):721–34. DOI: 10.1016/j.brs.2017.03.008. PMID: 28385535.Heise K.-F., Zimerman M., Hoppe J. et al. The aging motor system as a model for plastic changes of GABA-mediated intracortical inhibition and their behavioral relevance. J Neurosci 2013;33(21):9039–49. DOI: 10.1523/JNEUROSCI.4094-12.2013 PMID: 23699515.Guggisberg A.G., Koch P.J., Hummel F.C. et al. Brain networks and their relevance for stroke rehabilitation. Clin Neurophysiol 2019;130(7):1098–124. DOI: 10.1016/j.clinph.2019.04.004. PMID: 31082786.Hummel F.C., Steven B., Hoppe J. et al. Deficient intracortical inhibition (SICI) during movement preparation after chronic stroke. Neurology 2009;72(20):1766–72. DOI: 10.1212/WNL.0b013e3181a609c5. PMID: 19451532.Liuzzi G., Hörniss V., Lechner P. et al. Development of intracortical inhibition during movement preparation in acute to chronic subcortical stroke. Neurology 2014; 82(3):198–205. PMID: 24353337.Nikulin V.V, Kicić D., Kähkönen S. et al. Modulation of electroencephalographic responses to transcranial magnetic stimulation: evidence for changes in cortical excitability related to movement. Eur J Neurosci 2003;18(5):1206–12. DOI: 10.1046/j.1460-9568.2003.02858.x. PMID: 12956719.Tremblay S., Rogasch N.C., Premoli I. et al. Clinical utility and prospective of TMS–EEG. Clin Neurophysiol 2019;130(5):802–44. DOI:1 0.1016/j.clinph.2019.01.001. PMID: 30772238.Nazarova M.A., Blagoveschenskiy E.D., Nikulin V.V. et al. Transcranial magnetic stimulation with electroencephalography: methodology, applications for research and cilinics. Neuromuscul Dis 2017; 7(4):20–32. DOI: 10.17650/2222-8721-2017-7-4-20-32.Premoli I., Castellanos N., Rivolta D. et al. TMS-EEG Signatures of GABAergic Neurotransmission in the Human Cortex. J Neurosci 2014;34(16):5603–12. DOI: 10.1523/JNEUROSCI.5089-13.2014. PMID: 24741050.Manganotti P., Acler M., Masiero S. et al. TMS-evoked N100 responses as a prognostic factor in acute stroke. Funct Neurol 2019;30(2):125–30. DOI:10.11138/FNEUR/2015.30.2.125. PMID: 26415785.Pellicciari M.C., Bonnì S., Ponzo V. et al. Dynamic reorganization of TMS-evoked activity in subcortical stroke patients. Neuroimage 2018;175:365–78. DOI: 10.1016/j.neuroimage.2018.04.011. PMID: 29635028.Rossini P.M., Di Iorio R., Bentivoglio M. et al. Methods for analysis of brain connectivity: An IFCN-sponsored review. Clin Neurophysiol 2019;130(10):1833–58. DOI: 10.1016/j.clinph.2019.06.006. PMID: 31401492.Hallett M., Di Iorio R., Rossini P.M. et al. Contribution of transcranial magnetic stimulation to assessment of brain connectivity and networks. Clin Neurophysiol 2017;128(11):2125–39. DOI:10.1016/j.clinph.2017.08.007. PMID: 28938143.Mitina M., Nikulin V., Kulikova S. et al. P31-S Variability and interhemispheric asymmetry of the responses to paired-coil TMS of the primary motor cortex. Clin Neurophysiol 2019;130(7):e103–4. DOI: 10.1016/j.clinph.2019.04.569.Murase N., Duque J., Mazzocchio R., Cohen L.G. Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 2004;55(3):400–9. DOI: 10.1002/ana.10848. PMID: 14991818.Xu J., Branscheidt M., Schambra H. et al. Rethinking interhemispheric imbalance as a target for stroke neurorehabilitation. Ann Neurol 2019;85(4):502–13. DOI: 10.1002/ana.25452. PMID: 30805956.Ugawa Y., Uesaka Y., Terao Y. et al. Magnetic stimulation over the cerebellum in humans. Ann Neurol 1995;37(6):703–13. DOI: 10.1002/ana.410370603. PMID: 7778843.Celnik P. Understanding and modulating motor learning with cerebellar stimulation. Cerebellum 2015;14(2):171–4. DOI: 10.1007/s12311-014-0607-y. PMID: 25283180.Koponen L.M., Nieminen J.O., Ilmoniemi R.J. Multi-locus transcranial magnetic stimulation – theory and implementation. Brain Stimul 2018;11(4):849–55. DOI: 10.1016/j.brs.2018.03.014. PMID: 29627272.Bestmann S., Swayne O., Blankenburg F. et al. The role of contralesional dorsal premotor cortex after stroke as studied with concurrent TMS-fMRI. J Neurosci 2010;30(36):11926–37. DOI: 10.1523/JNEUROSCI.5642-09.2010. PMID: 20826657.Portnow L.H., Vaillancourt D.E., Okun M.S. The history of cerebral PET scanning: From physiology to cuttingedge technology. Neurology 2013;80(10):952–6. DOI: 10.1212/WNL.0b013e318285c135. PMID: 23460618.Bandettini P.A. Sewer pipe, wire, epoxy, and finger tapping: the start of fMRI at the Medical College of Wisconsin. Neuroimage 2012;62(2):620–31. DOI:10.1016/j.neuroimage.2011.10.044. PMID: 22044784.Turner R. The NIH experience in first advancing fMRI . Neuroimage 2012;62(2):632–6. DOI: 10.1016/j.neuroimage.2011.07.074. PMID: 21855641.Grefkes C., Ward N.S. Cortical reorganization after stroke. Neuroscientist 2014;20(1):56–70. DOI:10.1177/1073858413491147. PMID: 23774218.Stinear C.M., Ward N.S. How useful is imaging in predicting outcomes in stroke rehabilitation? Int J Stroke 2013;8(1):33–7. DOI: 10.1111/j.1747-4949.2012.00970.x. PMID: 23280267.Krieg S.M., Lioumis P., Mäkelä J.P. et al. Protocol for motor and language mapping by navigated TMS in patients and healthy volunteers; workshop report. Acta Neurochir (Wien) 2017;159(7):1187–95. DOI:10.1007/s00701-017-3187-z. PMID: 28456870.Novikov P.A., Nazarova M.A., Nikulin V.V. TMSmap – software for quantitative analysis of TMS mapping results. Front Hum Neurosci 2018;12:239. DOI: 10.3389/fnhum.2018.00239. PMID: 30038562.Picht T., Mularski S., Kuehn B. et al. Navigated transcranial magnetic stimulation for preoperative functional diagnostics in brain tumor surgery. Neurosurgery 2009;65(6):93–8. DOI:10.1227/01. NEU.0000348009.22750.59. PMID: 19935007.Lioumis P., Zhdanov A., Mäkelä N. et al. A novel approach for documenting naming errors induced by navigated transcranial magnetic stimulation. J Neurosci Methods 2012;204(2):349–54. DOI: 10.1016/j.jneumeth.2011.11.003. PMID: 22108143.Vitikainen A.-M., Mäkelä E., Lioumis P. et al. Accelerometer-based automatic voice onset detection in speech mapping with navigated repetitive transcranial magnetic stimulation. J Neurosci Methods 2015;253:70–7. DOI: 10.1016/j.jneumeth.2015.05.015. PMID: 26026582.Wassermann E.M., Pascual-Leone A., Valls-Solé J. et al. Topography of the inhibitory and excitatory responses to transcranial magnetic stimulation in a hand muscle. Electroencephalogr Clin Neurophysiol 1993;89(6):424–33. DOI: 10.1016/0168-5597(93)90116-7. PMID: 7507429.Picht T., Schmidt S., Woitzik J. et al. Navigated brain stimulation for preoperative cortical mapping in paretic patients: case report of a hemiplegic patient. Neurosurgery 2011;68(5):E1475–80. DOI: 10.1227/NEU.0b013e318210c7df. PMID: 21307789.Tarapore P.E., Tate M.C., Findlay A.M. et al. Preoperative multimodal motor mapping: a comparison of magnetoencephalography imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation. J Neurosurg 2012;117(2):354–62. DOI: 10.3171/2012.5.JNS112124. PMID: 22702484.Corneal S.F., Butler A.J., Wolf S.L. Intraand intersubject reliability of abductor pollicis brevis muscle motor map characteristics with transcranial magnetic stimulation. Arch Phys Med Rehabil 2005; 86(8):1670–5. DOI: 10.1016/j.apmr.2004.12.039. PMID: 16084825.Espadaler J., Rogić M., Deletis V. et al. Representation of cricothyroid muscles at the primary motor cortex (M1) in healthy subjects, mapped by navigated transcranial magnetic stimulation (nTMS). Clin Neurophysiol 2012;123(11):2205–11. DOI: 10.1016/j.clinph.2012.04.008. PMID: 22621909.Schieber M.H. Constraints on somatotopic organization in the primary motor cortex. J Neurophysiol 2001;86(5):2125–43. DOI: 10.1152/jn.2001.86.5.2125. PMID: 11698506.Клочков А.С., Хижникова А.Е., Назарова М.А. и др. Патологические синергии в руке у пациентов с постинсультными гемипарезами. Журнал высшей нервной деятельности имени И.П. Павлова 2017;67(3):273–87. DOI: 10.7868/S0044467717030066. [Klochkov A.S., Khizhnikova A.E., Nazarova M.A. et al. Pathological synergies in the hand in patients with poststroke hemiparesis. Journal of higher nervous activity named I.P. Pavlova = Zhurnal vysshey nervnoy deyatelnosti imeni I.P. Pavlova 2017;67(3):273–87. (In Russ.)].Julkunen P. Methods for estimating cortical motor representation size and location in navigated transcranial magnetic stimulation. J Neurosci Methods 2014;232:125–33. DOI: 10.1016/j.jneumeth.2014.05.020. PMID: 24875623.Cavaleri R., Schabrun S.M., Chipchase L.S. The reliability and validity of rapid transcranial magnetic stimulation mapping . Brain Stimul 2018;11(6):1291–5. DOI: 10.1016/j.brs.2018.07.043. PMID: 30025980.Sinitsyn D.O., Chernyavskiy A.Y., Poydasheva A.G. et al. Optimization of the navigated TMS mapping algorithm for accurate estimation of cortical muscle representation characteristics. Brain Sci 2019;9(4):pii:E88. DOI: 1 0.1101/573220. PMID: 31010190.Weise K., Numssen O., Thielscher A. et al. A novel approach to localize cortical TMS effects. Neuroimage 2020;209:116486. DOI: 10.1016/j.neuroimage.2019.116486. PMID: 31877374.Программа для анализа результатов картирования мозга при помощи транскраниальной магнитной стимуляции (TMSmap). URL: https://tmsmap.ru.Classen J., Liepert J., Wise S.P. et al. Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 1998;79(2):1117–23. DOI: 10.1152/jn.1998.79.2.1117. PMID: 9463469.Liepert J., Miltner W.H., Bauder H. et al. Motor cortex plasticity during constraintinduced movement therapy in stroke patients. Neurosci Lett 1998;250(1):5–8. DOI: 10.1016/s0304-3940(98)00386-3. PMID: 9696052.Lüdemann-Podubecká J., Nowak D.A. Mapping cortical hand motor representation using TMS: A method to assess brain plasticity and a surrogate marker for recovery of function after stroke? Neurosci Biobehav Rev 2016;69:239–51. DOI: 10.1016/j.neubiorev.2016.07.006. PMID:27435238.Veldema J., Bösl K., Nowak D.A. Motor recovery of the affected hand in subacute stroke correlates with changes of contralesional cortical hand motor representation. Neural Plast 2017;2017:6171903. DOI: 10.1155/2017/6171903. PMID: 28286677.Massé-Alarie H., Bergin M.J.G., Schneider C. et al. “Discrete peaks” of excitability and map overlap reveal task- specific organization of primary motor cortex for control of human forearm muscles. Hum Brain Mapp 2017;38(12):6118–32. DOI: 10.1002/hbm.23816. PMID: 28921724.Elgueta‐Cancino E., Marinovic W., Jull G. et al. Motor cortex representation of deep and superficial neck flexor muscles in individuals with and without neck pain . Hum Brain Mapp 2019;40(9):2759–70. DOI: 10.1002/hbm.24558. PMID: 30835902.Levy R.M., Harvey R.L., Kissela B.M. et al. Epidural Electrical Stimulation for Stroke Rehabilitation.Neurorehabil Neural Repair 2016;30(2):107–19. DOI: 10.1177/1545968315575613. PMID: 25748452.