Журнал высшей нервной деятельности им. И.П. Павлова, 2023, T. 73, № 4, стр. 435-453

Показатели нейропластических и функциональных перестроек при восстановлении двигательной функции в ходе реабилитации после инсульта

И. Р. Федотова 1, П. Д. Бобров 12*, А. А. Кондур 3

1 Институт высшей нервной деятельности и нейрофизиологии Российской академии наук
Москва, Россия

2 Российский Национальный Исследовательский Медицинский Университет им. Н.И. Пирогова
Москва, Россия

3 Московский областной научно-исследовательский клинический институт им. М.Ф. Владимирского
Москва, Россия

* E-mail: bobrov.pavel@ihna.ru

Поступила в редакцию 25.01.2023
После доработки 27.02.2023
Принята к публикации 27.02.2023

Аннотация

В статье представлены обзорные данные по изменению показателей, полученных из многоканальной ЭЭГ, МРТ, фМРТ и диффузионной тензорной трактографии у больных после инсульта в процессе двигательного восстановления. Рассмотрены основные показатели, которые чаще всего анализируются в литературе, посвященной изменениям в головном мозге, происходящим как в ходе традиционной двигательной реабилитации, так и при применении реабилитационных процедур, использующих технологию “интерфейс мозг—компьютер”. Изменение обсуждаемых показателей отражает динамику вовлеченности полушарий, отдельных областей мозга и связей между ними в решение двигательной задачи и является проявлением как мгновенных функциональных перестроек работы сети, так и реальных нейропластических (структурных) изменений в мозге. Обсуждается функциональная роль полушарий, отдельных областей и связей между областями в процессе двигательной реабилитации после инсульта.

Ключевые слова: инсульт, двигательная реабилитация, ЭЭГ, МРТ, фМРТ, диффузионная тензорная трактография, коэффициент латеральности, функциональная и эффективная связность

Список литературы

  1. Пирадов М.А., Супонева Н.А., Селиверстов Ю.А., Лагода Д.Ю., Сергеев Д.В., Кремнева Е.И., Пойдашева А.Г. Возможности современных методов нейровизуализации в изучении спонтанной активности головного мозга в состоянии покоя. Неврологический журн. 2016. 21 (1): 4–12.

  2. Ackerley S.J., Stinear C.M., Byblow W.D. Promoting use-dependent plasticity with externally-paced training. Clin Neurophysiol. 2011. 122 (12): 2462–2468.

  3. Almeida S.R., Vicentini J., Bonilha L., De Campos B.M., Casseb R.F., Min L.L. Brain Connectivity and Functional Recovery in Patients With Ischemic Stroke. J. Neuroimaging. 2017. 27 (1): 65–70.

  4. Ameli M., Grefkes C., Kemper F., Riegg F.P., Rehme A.K., Karbe H., Fink G.R., Nowak D.A. Differential effects of high-frequency repetitive transcranial magnetic stimulation over ipsilesional primary motor cortex in cortical and subcortical middle cerebral artery stroke. Ann Neurol. 2009. 66 (3): 298–309.

  5. Ang K.K., Chua K.S., Phua K.S., Wang C., Chin Z.Y., Kuah C.W., Low W., Guan C. A Randomized Controlled Trial of EEG-Based Motor Imagery Brain-Computer Interface Robotic Rehabilitation for Stroke. Clin EEG Neurosci. 2015. 46 (4): 310–320.

  6. Ang K.K., Guan C., Chua K.S.G., Ang B.T., Kuah C.W.K., Wang C., Phua K.S., Chin Z.Y., Zhang H. A large clinical study on the ability of stroke patients to use an EEG-based motor imagery brain-computer interface. Clinical EEG and Neuroscience. 2011. 42 (4): 253–258.

  7. Ang K.K., Guan C., Phua K.S., Wang C., Zhou L., Tang K.Y., Ephraim Joseph G.J., Kuah C.W., Chua K.S. Brain-computer interface-based robotic end effector system for wrist and hand rehabilitation: results of a three-armed randomized controlled trial for chronic stroke. Front Neuroeng. 2014. 7, 30.

  8. Backhaus W., Braass H., Higgen F.L., Gerloff C., Schulz R. Early parietofrontal network upregulation relates to future persistent deficits after severe stroke-a prospective cohort study. Brain Commun. 2021. 3 (2): fcab097.

  9. Baron J.C., Cohen L.G., Cramer S.C., Dobkin B.H., Johansen-Berg H., Loubinoux I., Marshall R.S., Ward N.S., First International Workshop on N., Stroke R. Neuroimaging in stroke recovery: a position paper from the First International Workshop on Neuroimaging and Stroke Recovery. Cerebrovasc Dis. 2004. 18 (3): 260–267.

  10. Bledowski C., Prvulovic D., Goebel R., Zanella F.E., Linden D.E. Attentional systems in target and distractor processing: a combined ERP and fMRI study. Neuroimage. 2004. 22 (2): 530–540.

  11. Buch E.R., Rizk S., Nicolo P., Cohen L.G., Schnider A., Guggisberg A.G. Predicting motor improvement after stroke with clinical assessment and diffusion tensor imaging. Neurology. 2016. 86 (20): 1924–1925.

  12. Buetefisch C.M. Role of the contralesional hemisphere in post-stroke recovery of upper extremity motor function. Frontiers in neurology. 2015. 6, 214.

  13. Calautti C., Baron J.-C. Functional neuroimaging studies of motor recovery after stroke in adults: a review. Stroke. 2003. 34 (6): 1553–1566.

  14. Carey J.R., Kimberley T.J., Lewis S.M., Auerbach E.J., Dorsey L., Rundquist P., Ugurbil K. Analysis of fMRI and finger tracking training in subjects with chronic stroke. Brain. 2002. 125 (Pt 4): 773–788.

  15. Carey L.M., Seitz R.J., Parsons M.W., Levi C.R., Farquharson S., Tournier J.D., Palmer S., Connelly A. Beyond the lesion: neuroimaging foundations for post-stroke recovery. Future Neurology. 2013. 8, 507–527.

  16. Caria A., Weber C., Brötz D., Ramos A., Ticini L.F., Gharabaghi A., Braun C., Birbaumer N. Chronic stroke recovery after combined BCI training and physiotherapy: a case report. Psychophysiology. 2011. 48 (4): 578–582.

  17. Carter A.R., Astafiev S.V., Lang C.E., Connor L.T., Rengachary J., Strube M.J., Pope D.L., Shulman G.L., Corbetta M. Resting interhemispheric functional magnetic resonance imaging connectivity predicts performance after stroke. Annals of neurology. 2010. 67 (3): 365–375.

  18. Catalan M.J., Honda M., Weeks R.A., Cohen L.G., Hallett M. The functional neuroanatomy of simple and complex sequential finger movements: a PET study. Brain. 1998. 121 (Pt 2): 253–264.

  19. Cervera M.A., Soekadar S.R., Ushiba J., Millán J.d.R., Liu M., Birbaumer N., Garipelli G. Brain-computer interfaces for post-stroke motor rehabilitation: a meta-analysis. Annals of clinical and translational neurology. 2018. 5 (5): 651–663.

  20. Chen Z., Ni P., Zhang J., Ye Y., Xiao H., Qian G., Xu S., Wang J., Yang X., Chen J., Zhang B., Zeng Y. Evaluating ischemic stroke with diffusion tensor imaging. Neurol Res. 2008. 30 (7): 720–726.

  21. Corbet T., Leeb R., Biasiucci A., Zhang H., Perdikis S., Millán J.D.R. (2016). BCI-NMES therapy enhances effective connectivity in the damaged hemisphere in stroke patients. Paper presented at the Proceedings of the 6th International Brain-Computer Interface Meeting.

  22. Corbetta M., Patel G., Shulman G.L. The reorienting system of the human brain: from environment to theory of mind. Neuron. 2008. 58 (3): 306–324.

  23. Dancause N., Barbay S., Frost S.B., Plautz E.J., Chen D., Zoubina E.V., Stowe A.M., Nudo R.J. Extensive cortical rewiring after brain injury. J Neurosci. 2005. 25 (44): 10167–10179.

  24. Desmurget M., Epstein C., Turner R., Prablanc C., Alexander G., Grafton S. Role of the posterior parietal cortex in updating reaching movements to a visual target. Nature neuroscience. 1999. 2 (6): 563.

  25. Desowska A., Turner D.L. Dynamics of brain connectivity after stroke. Rev Neurosci. 2019. 30 (6): 605–623.

  26. Di Pino G., Pellegrino G., Assenza G., Capone F., Ferreri F., Formica D., Ranieri F., Tombini M., Ziemann U., Rothwell J.C. Modulation of brain plasticity in stroke: a novel model for neurorehabilitation. Nature Reviews Neurology. 2014. 10 (10): 597.

  27. Dodd K.C., Nair V.A., Prabhakaran V. Role of the contralesional vs. ipsilesional hemisphere in stroke recovery. Frontiers in human neuroscience. 2017. 11: 469.

  28. Dum R.P., Strick P.L. Motor areas in the frontal lobe of the primate. Physiol Behav. 2002. 77 (4–5): 677–682.

  29. Eickhoff S.B., Jbabdi S., Caspers S., Laird A.R., Fox P.T., Zilles K., Behrens T.E. Anatomical and functional connectivity of cytoarchitectonic areas within the human parietal operculum. J. Neuroscience. 2010. 30 (18): 6409–6421.

  30. Fan Y.T., Wu C.Y., Liu H.L., Lin K.C., Wai Y.Y., Chen Y.L. Neuroplastic changes in resting-state functional connectivity after stroke rehabilitation. Front Hum Neurosci. 2015. 9: 546.

  31. Fregni F., Boggio P.S., Mansur C.G., Wagner T., Ferreira M.J., Lima M.C., Rigonatti S.P., Marcolin M.A., Freedman S.D., Nitsche M.A. Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. Neuroreport. 2005. 16 (14): 1551–1555.

  32. Fregni F., Boggio P.S., Valle A.C., Rocha R.R., Duarte J., Ferreira M.J., Wagner T., Fecteau S., Rigonatti S.P., Riberto M., Freedman S.D., Pascual-Leone A. A sham-controlled trial of a 5-day course of repetitive transcranial magnetic stimulation of the unaffected hemisphere in stroke patients. Stroke. 2006. 37 (8): 2115–2122.

  33. Fridman E.A., Hanakawa T., Chung M., Hummel F., Leiguarda R.C., Cohen L.G. Reorganization of the human ipsilesional premotor cortex after stroke. Brain. 2004. 127 (Pt 4): 747–758.

  34. Frolov A.A., Mokienko O., Lyukmanov R., Biryukova E., Kotov S., Turbina L., Nadareyshvily G., Bushkova Y. Post-stroke Rehabilitation Training with a Motor-Imagery-Based Brain-Computer Interface (BCI)-Controlled Hand Exoskeleton: A Randomized Controlled Multicenter Trial. Front Neurosci. 2017. 11: 400.

  35. Frost S., Barbay S., Friel K., Plautz E., Nudo R. Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. J. neurophysiology. 2003. 89 (6): 3205–3214.

  36. Gerloff C., Bushara K., Sailer A., Wassermann E.M., Chen R., Matsuoka T., Waldvogel D., Wittenberg G.F., Ishii K., Cohen L.G., Hallett M. Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke. Brain. 2006. 129 (Pt 3): 791–808.

  37. Golestani A.-M., Tymchuk S., Demchuk A., Goodyear B.G., Group V.-S. Longitudinal evaluation of resting-state FMRI after acute stroke with hemiparesis. Neurorehabilitation and neural repair. 2013. 27 (2): 153–163.

  38. Grefkes C., Fink G.R. Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches. Brain. 2011. 134 (Pt 5): 1264–1276.

  39. Grefkes C., Nowak D.A., Wang L.E., Dafotakis M., Eickhoff S.B., Fink G.R. Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling. Neuroimage. 2010. 50 (1): 233–242.

  40. Guggisberg A.G., Nicolo P., Cohen L.G., Schnider A., Buch E.R. Longitudinal Structural and Functional Differences Between Proportional and Poor Motor Recovery After Stroke. Neurorehabil Neural Repair. 2017. 31 (12): 1029–1041.

  41. Hallett M. Transcranial magnetic stimulation and the human brain. Nature. 2000. 406 (6792): 147–150.

  42. Halsband U., Ito N., Tanji J., Freund H.-J. The role of premotor cortex and the supplementary motor area in the temporal control of movement in man. Brain. 1993. 116 (1): 243–266.

  43. Hétu S., Grégoire M., Saimpont A., Coll M.-P., Eugène F., Michon P.-E., Jackson P.L. The neural network of motor imagery: an ALE meta-analysis. Neuroscience & Biobehavioral Reviews. 2013. 37 (5): 930–949.

  44. Hong W., Lin Q., Cui Z., Liu F., Xu R., Tang C. Diverse functional connectivity patterns of resting-state brain networks associated with good and poor hand outcomes following stroke. Neuroimage Clin. 2019. 24: 102065.

  45. Hordacre B., Lotze M., Jenkinson M., Lazari A., Barras C.D., Boyd L., Hillier S. Fronto-parietal involvement in chronic stroke motor performance when corticospinal tract integrity is compromised. Neuroimage Clin. 2021. 29: 102558.

  46. Hoshi E., Tanji J. Distinctions between dorsal and ventral premotor areas: anatomical connectivity and functional properties. Current opinion in neurobiology. 2007. 17 (2): 234–242.

  47. Hoyer E.H., Celnik P.A. Understanding and enhancing motor recovery after stroke using transcranial magnetic stimulation. Restorative neurology and neuroscience. 2011. 29 (6): 395–409.

  48. James G.A., Lu Z.L., VanMeter J.W., Sathian K., Hu X.P., Butler A.J. Changes in resting state effective connectivity in the motor network following rehabilitation of upper extremity poststroke paresis. Top Stroke Rehabil. 2009. 16 (4): 270–281.

  49. Jang S.H., Chang C.H., Lee J., Kim C.S., Seo J.P., Yeo S.S. Functional role of the corticoreticular pathway in chronic stroke patients. Stroke. 2013. 44 (4): 1099–1104.

  50. Johansen-Berg H., Rushworth M.F., Bogdanovic M.D., Kischka U., Wimalaratna S., Matthews P.M. The role of ipsilateral premotor cortex in hand movement after stroke. Proceedings of the National Academy of Sciences. 2002. 99 (22): 14518–14523.

  51. Kasashima Y., Fujiwara T., Matsushika Y., Tsuji T., Hase K., Ushiyama J., Ushiba J., Liu M. Modulation of event-related desynchronization during motor imagery with transcranial direct current stimulation (tDCS) in patients with chronic hemiparetic stroke. Exp Brain Res. 2012. 221 (3): 263–268.

  52. Khan A., Chen C., Yuan K., Wang X., Mehra P., Liu Y., Tong K.Y. Changes in electroencephalography complexity and functional magnetic resonance imaging connectivity following robotic hand training in chronic stroke. Top Stroke Rehabil. 2021. 28 (4): 276–288.

  53. Kobayashi M., Hutchinson S., Theoret H., Schlaug G., Pascual-Leone A. Repetitive TMS of the motor cortex improves ipsilateral sequential simple finger movements. Neurology. 2004. 62 (1): 91–98.

  54. Koch P., Schulz R., Hummel F.C. Structural connectivity analyses in motor recovery research after stroke. Ann Clin Transl Neurol. 2016. 3 (3): 233–244.

  55. Kraeutner S.N., Rubino C., Rinat S., Lakhani B., Borich M.R., Wadden K.P., Boyd L.A. Resting State Connectivity Is Modulated by Motor Learning in Individuals After Stroke. Neurorehabil Neural Repair. 2021. 35 (6): 513–524.

  56. Kruse A., Suica Z., Taeymans J., Schuster-Amft C. Effect of brain-computer interface training based on non-invasive electroencephalography using motor imagery on functional recovery after stroke-a systematic review and meta-analysis. BMC neurology. 2020. 20 (1): 1–14.

  57. Lau C.C., Yuan K., Wong P., Chu W.C., Leung T.W., Wong W.-W., Tong R.K. Modulation of Functional Connectivity and Low-Frequency Fluctuations After Brain-Computer Interface-Guided Robot Hand Training in Chronic Stroke: A 6-Month Follow-Up Study. Frontiers in human neuroscience. 2021. 614.

  58. Lee J., Park E., Lee A., Chang W.H., Kim D.S., Kim Y.H. Alteration and Role of Interhemispheric and Intrahemispheric Connectivity in Motor Network After Stroke. Brain Topogr. 2018. 31 (4): 708–719.

  59. Li M., Liu Y., Wu Y., Liu S., Jia J., Zhang L. Neurophysiological substrates of stroke patients with motor imagery-based Brain-Computer Interface training. Int. J. Neurosci. 2014. 124 (6): 403–415.

  60. Li Y., Wang D., Zhang H., Wang Y., Wu P., Zhang H., Yang Y., Huang W. Changes of Brain Connectivity in the Primary Motor Cortex After Subcortical Stroke: A Multimodal Magnetic Resonance Imaging Study. Medicine (Baltimore). 2016. 95 (6): e2579.

  61. Lin L.Y., Ramsey L., Metcalf N.V., Rengachary J., Shulman G.L., Shimony J.S., Corbetta M. Stronger prediction of motor recovery and outcome post-stroke by cortico-spinal tract integrity than functional connectivity. PloS one. 2018. 13 (8): e0202504.

  62. Lindberg P.G., Schmitz C., Engardt M., Forssberg H., Borg J. Use-dependent up- and down-regulation of sensorimotor brain circuits in stroke patients. Neurorehabil Neural Repair. 2007. 21 (4): 315–326.

  63. Lotze M., Markert J., Sauseng P., Hoppe J., Plewnia C., Gerloff C. The role of multiple contralesional motor areas for complex hand movements after internal capsular lesion. J Neurosci. 2006. 26 (22): 6096–6102.

  64. Loubinoux I., Dechaumont-Palacin S., Castel-Lacanal E., De Boissezon X., Marque P., Pariente J., Albucher J.F., Berry I., Chollet F. Prognostic value of FMRI in recovery of hand function in subcortical stroke patients. Cereb Cortex. 2007. 17 (12): 2980–2987.

  65. Lu Q., Huang G., Chen L., Li W., Liang Z. Structural and functional reorganization following unilateral internal capsule infarction contribute to neurological function recovery. Neuroradiology. 2019. 61 (10): 1181–1190.

  66. Mansur C.G., Fregni F., Boggio P.S., Riberto M., Gallucci-Neto J., Santos C.M., Wagner T., Rigonatti S.P., Marcolin M.A., Pascual-Leone A. A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology. 2005. 64 (10): 1802–1804.

  67. Marshall R.S., Perera G.M., Lazar R.M., Krakauer J.W., Constantine R.C., DeLaPaz R.L. Evolution of cortical activation during recovery from corticospinal tract infarction. Stroke. 2000. 31 (3): 656–661.

  68. Marshall R.S., Zarahn E., Alon L., Minzer B., Lazar R.M., Krakauer J.W. Early imaging correlates of subsequent motor recovery after stroke. Ann Neurol. 2009. 65 (5): 596–602.

  69. Meehan S.K., Randhawa B., Wessel B., Boyd L.A. Implicit sequence-specific motor learning after subcortical stroke is associated with increased prefrontal brain activations: an fMRI study. Hum Brain Mapp. 2011. 32 (2): 290–303.

  70. Mihara M., Hattori N., Hatakenaka M., Yagura H., Kawano T., Hino T., Miyai I. Near-infrared spectroscopy–mediated neurofeedback enhances efficacy of motor imagery–based training in poststroke victims: a pilot study. Stroke. 2013. 44 (4): 1091–1098.

  71. Min Y.S., Park J.W., Park E., Kim A.R., Cha H., Gwak D.W., Jung S.H., Chang Y., Jung T.D. Interhemispheric Functional Connectivity in the Primary Motor Cortex Assessed by Resting-State Functional Magnetic Resonance Imaging Aids Long-Term Recovery Prediction among Subacute Stroke Patients with Severe Hand Weakness. J. Clin. Med. 2020. 9 (4).

  72. Mori S., Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron. 2006. 51 (5): 527–539.

  73. Murase N., Duque J., Mazzocchio R., Cohen L.G. Influence of interhemispheric interactions on motor function in chronic stroke. Annals of Neurology: Official Journal of the American Neurological Association and the Child Neurology Society. 2004. 55 (3): 400–409.

  74. Murphy T.H., Corbett D. Plasticity during stroke recovery: from synapse to behaviour. Nature Reviews Neuroscience. 2009. 10 (12): 861.

  75. Nachev P., Kennard C., Husain M. Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci. 2008. 9 (11): 856–869.

  76. Newton J.M., Ward N.S., Parker G.J., Deichmann R., Alexander D.C., Friston K.J., Frackowiak R.S. Non-invasive mapping of corticofugal fibres from multiple motor areas–relevance to stroke recovery. Brain. 2006. 129 (Pt 7): 1844–1858.

  77. Nudo R.J., Wise B.M., SiFuentes F., Milliken G.W. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. science. 1996. 272 (5269): 1791–1794.

  78. O’Shea J., Johansen-Berg H., Trief D., Gobel S., Rushworth M.F. Functionally specific reorganization in human premotor cortex. Neuron. 2007. 54 (3): 479–490.

  79. Ocklenburg S., Ball A., Wolf C.C., Genç E., Güntürkün O. Functional cerebral lateralization and interhemispheric interaction in patients with callosal agenesis. Neuropsychology. 2015. 29 (5): 806–815.

  80. Ono T., Shindo K., Kawashima K., Ota N., Ito M., Ota T., Mukaino M., Fujiwara T., Kimura A., Liu M. Brain-computer interface with somatosensory feedback improves functional recovery from severe hemiplegia due to chronic stroke. Frontiers in neuroengineering. 2014. 7: 19.

  81. Ono T., Tomita Y., Inose M., Ota T., Kimura A., Liu M., Ushiba J. Multimodal sensory feedback associated with motor attempts alters BOLD responses to paralyzed hand movement in chronic stroke patients. Brain Topogr. 2015. 28 (2): 340–351.

  82. Park C.-h., Chang W.H., Ohn S.H., Kim S.T., Bang O.Y., Pascual-Leone A., Kim Y.-H. Longitudinal changes of resting-state functional connectivity during motor recovery after stroke. Stroke. 2011. 42 (5): 1357–1362.

  83. Pfurtscheller G., Da Silva F.L. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clinical Neurophysiology. 1999. 110 (11): 1842–1857.

  84. Picard N., Strick P.L. Imaging the premotor areas. Curr Opin Neurobiol. 2001. 11 (6): 663–672.

  85. Platz T., Kim I.H., Pintschovius H., Winter T., Kieselbach A., Villringer K., Kurth R., Mauritz K.H. Multimodal EEG analysis in man suggests impairment-specific changes in movement-related electric brain activity after stroke. Brain. 2000. 123 (Pt 12): 2475–2490.

  86. Pool E.M., Leimbach M., Binder E., Nettekoven C., Eickhoff S.B., Fink G.R., Grefkes C. Network dynamics engaged in the modulation of motor behavior in stroke patients. Hum Brain Mapp. 2018. 39 (3): 1078–1092.

  87. Ramos-Murguialday A., Broetz D., Rea M., Laer L., Yilmaz O., Brasil F.L., Liberati G., Curado M.R., Garcia-Cossio E., Vyziotis A., Cho W., Agostini M., Soares E., Soekadar S., Caria A., Cohen L.G., Birbaumer N. Brain-machine interface in chronic stroke rehabilitation: a controlled study. Ann Neurol. 2013. 74 (1): 100–108.

  88. Ramos-Murguialday A., Broetz D., Rea M., Läer L., Yilmaz Ö., Brasil F.L., Liberati G., Curado M.R., Garcia-Cossio E., Vyziotis A. Brain–machine interface in chronic stroke rehabilitation: a controlled study. Annals of neurology. 2013. 74 (1): 100–108.

  89. Rehme A.K., Eickhoff S.B., Rottschy C., Fink G.R., Grefkes C. Activation likelihood estimation meta-analysis of motor-related neural activity after stroke. Neuroimage. 2012. 59 (3): 2771–2782.

  90. Rehme A.K., Eickhoff S.B., Wang L.E., Fink G.R., Grefkes C. Dynamic causal modeling of cortical activity from the acute to the chronic stage after stroke. Neuroimage. 2011. 55 (3): 1147–1158.

  91. Rehme A.K., Grefkes C. Cerebral network disorders after stroke: evidence from imaging-based connectivity analyses of active and resting brain states in humans. J Physiol. 2013. 591 (1): 17–31.

  92. Riecker A., Gröschel K., Ackermann H., Schnaudigel S., Kassubek J., Kastrup A. The role of the unaffected hemisphere in motor recovery after stroke. Human brain mapping. 2010. 31 (7): 1017–1029.

  93. Rossini P., Altamura C., Ferreri F., Melgari J., Tecchio F., Tombini M., Pasqualetti P., Vernieri F. Neuroimaging experimental studies on brain plasticity in recovery from stroke. Europa medicophysica. 2007. 43 (2): 241.

  94. Rouiller E.M., Babalian A., Kazennikov O., Moret V., Yu X.-H., Wiesendanger M. Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys. Experimental brain research. 1994. 102 (2): 227–243.

  95. Ruber T., Schlaug G., Lindenberg R. Compensatory role of the cortico-rubro-spinal tract in motor recovery after stroke. Neurology. 2012. 79 (6): 515–522.

  96. Sakai K., Hikosaka O., Miyauchi S., Takino R., Sasaki Y., Putz B. Transition of brain activation from frontal to parietal areas in visuomotor sequence learning. J. Neurosci. 1998. 18 (5): 1827–1840.

  97. Sanes J.N., Suner S., Donoghue J.P. Dynamic organization of primary motor cortex output to target muscles in adult rats. I. Long-term patterns of reorganization following motor or mixed peripheral nerve lesions. Exp. Brain Res. 1990. 79 (3): 479–491.

  98. Schaechter J.D., Fricker Z.P., Perdue K.L., Helmer K.G., Vangel M.G., Greve D.N., Makris N. Microstructural status of ipsilesional and contralesional corticospinal tract correlates with motor skill in chronic stroke patients. Hum Brain Mapp. 2009. 30 (11): 3461–3474.

  99. Schlaug G., Marchina S., Wan C.Y. The use of non-invasive brain stimulation techniques to facilitate recovery from post-stroke aphasia. Neuropsychology review. 2011. 21 (3): 288.

  100. Schubotz R.I., von Cramon D.Y. Predicting perceptual events activates corresponding motor schemes in lateral premotor cortex: an fMRI study. Neuroimage. 2002. 15 (4): 787–796.

  101. Sebastián-Romagosa M., Udina E., Ortner R., Dinarès-Ferran J., Cho W., Murovec N., Matencio-Peralba C., Sieghartsleitner S., Allison B.Z., Guger C. EEG biomarkers related with the functional state of stroke patients. Frontiers in neuroscience. 2020. 14: 582.

  102. Seitz R.J., Canavan A.G., Yaguez L., Herzog H., Tellmann L., Knorr U., Huang Y., Homberg V. Representations of graphomotor trajectories in the human parietal cortex: evidence for controlled processing and automatic performance. Eur. J. Neurosci. 1997. 9 (2): 378–389.

  103. Serrien D.J., Strens L.H., Cassidy M.J., Thompson A.J., Brown P. Functional significance of the ipsilateral hemisphere during movement of the affected hand after stroke. Exp Neurol. 2004. 190 (2): 425–432.

  104. Sharma N., Simmons L.H., Jones P.S., Day D.J., Carpenter T.A., Pomeroy V.M., Warburton E.A., Baron J.-C. Motor imagery after subcortical stroke: a functional magnetic resonance imaging study. Stroke. 2009. 40 (4): 1315–1324.

  105. Siegel J.S., Ramsey L.E., Snyder A.Z., Metcalf N.V., Chacko R.V., Weinberger K., Baldassarre A., Hacker C.D., Shulman G.L., Corbetta M. Disruptions of network connectivity predict impairment in multiple behavioral domains after stroke. Proc Natl Acad Sci U S A. 2016. 113 (30): E4367–4376.

  106. Sinha A.M., Nair V.A., Prabhakaran V. Brain-Computer Interface Training With Functional Electrical Stimulation: Facilitating Changes in Interhemispheric Functional Connectivity and Motor Outcomes Post-stroke. Front Neurosci. 2021. 15, 670953.

  107. Stępień M., Conradi J., Waterstraat G., Hohlefeld F.U., Curio G., Nikulin V.V. Event-related desynchronization of sensorimotor EEG rhythms in hemiparetic patients with acute stroke. Neuroscience letters. 2011. 488 (1): 17–21.

  108. Stinear C.M., Barber P.A., Smale P.R., Coxon J.P., Fleming M.K., Byblow W.D. Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain. 2007. 130 (Pt 1): 170–180.

  109. Stinear C.M., Byblow W.D. Predicting and accelerating motor recovery after stroke. Current opinion in neurology. 2014. 27 (6): 624–630.

  110. Takenobu Y., Hayashi T., Moriwaki H., Nagatsuka K., Naritomi H., Fukuyama H. Motor recovery and microstructural change in rubro-spinal tract in subcortical stroke. Neuroimage Clin. 2014. 4, 201–208.

  111. Talelli P., Greenwood R., Rothwell J. Exploring Theta Burst Stimulation as an intervention to improve motor recovery in chronic stroke. Clinical Neurophysiology. 2007. 118 (2): 333–342.

  112. Tang C., Zhao Z., Chen C., Zheng X., Sun F., Zhang X., Tian J., Fan M., Wu Y., Jia J. Decreased Functional Connectivity of Homotopic Brain Regions in Chronic Stroke Patients: A Resting State fMRI Study. PloS one. 2016. 11 (4): e0152875.

  113. Tavazzi E., Bergsland N., Pirastru A., Cazzoli M., Blasi V., Baglio F. MRI markers of functional connectivity and tissue microstructure in stroke-related motor rehabilitation: A systematic review. NeuroImage: Clinical. 2022. 33: 102931.

  114. van den Heuvel M.P., Hulshoff Pol H.E. Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol. 2010. 20 (8): 519–534.

  115. Várkuti B., Guan C., Pan Y., Phua K.S., Ang K.K., Kuah C.W.K., Chua K., Ang B.T., Birbaumer N., Sitaram R. Resting state changes in functional connectivity correlate with movement recovery for BCI and robot-assisted upper-extremity training after stroke. Neurorehabilitation and neural repair. 2013. 27 (1): 53–62.

  116. Wadden K.P., Woodward T.S., Metzak P.D., Lavigne K.M., Lakhani B., Auriat A.M., Boyd L.A. Compensatory motor network connectivity is associated with motor sequence learning after subcortical stroke. Behav Brain Res. 2015. 286: 136–145.

  117. Wang L., Yu C., Chen H., Qin W., He Y., Fan F., Zhang Y., Wang M., Li K., Zang Y. Dynamic functional reorganization of the motor execution network after stroke. Brain. 2010. 133 (4): 1224–1238.

  118. Ward N.S., Brown M.M., Thompson A.J., Frackowiak R.S. Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain. 2003. 126 (Pt 11): 2476–2496.

  119. Ward N.S., Cohen L.G. Mechanisms underlying recovery of motor function after stroke. Arch Neurol. 2004. 61 (12): 1844–1848.

  120. Ward N.S., Newton J.M., Swayne O.B., Lee L., Thompson A.J., Greenwood R.J., Rothwell J.C., Frackowiak R.S. Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain. 2006. 129 (Pt 3): 809–819.

  121. Weiller C., Juptner M., Fellows S., Rijntjes M., Leonhardt G., Kiebel S., Muller S., Diener H.C., Thilmann A.F. Brain representation of active and passive movements. Neuroimage. 1996. 4 (2): 105–110.

  122. Werhahn K.J., Conforto A.B., Kadom N., Hallett M., Cohen L.G. Contribution of the ipsilateral motor cortex to recovery after chronic stroke. Ann Neurol. 2003. 54 (4): 464–472.

  123. Westlake K.P., Nagarajan S.S. Functional connectivity in relation to motor performance and recovery after stroke. Front Syst Neurosci. 2011. 5: 8.

  124. Xia Y., Huang G., Quan X., Qin Q., Li H., Xu C., Liang Z. Dynamic Structural and Functional Reorganizations Following Motor Stroke. Med Sci Monit. 2021. 27: e929092.

  125. Xu H., Qin W., Chen H., Jiang L., Li K., Yu C. Contribution of the resting-state functional connectivity of the contralesional primary sensorimotor cortex to motor recovery after subcortical stroke. PloS one. 2014. 9 (1): e84729.

  126. Young B.M., Nigogosyan Z., Walton L.M., Song J., Nair V.A., Grogan S.W., Tyler M.E., Edwards D.F., Caldera K., Sattin J.A. Changes in functional brain organization and behavioral correlations after rehabilitative therapy using a brain-computer interface. Frontiers in neuroengineering. 2014. 7: 26.

  127. Young B.M., Stamm J.M., Song J., Remsik A.B., Nair V.A., Tyler M.E., Edwards D.F., Caldera K., Sattin J.A., Williams J.C., Prabhakaran V. Brain-Computer Interface Training after Stroke Affects Patterns of Brain-Behavior Relationships in Corticospinal Motor Fibers. Front Hum Neurosci. 2016. 10: 457.

  128. Yuan K., Wang X., Chen C., Lau C.C.-Y., Chu W.C.-W., Tong R.K.-Y. Interhemispheric functional reorganization and its structural base after BCI-guided upper-limb training in chronic stroke. IEEE Transactions on Neural Systems and Rehabilitation Engineering. 2020. 28 (11): 2525–2536.

  129. Zhang Y., Liu H., Wang L., Yang J., Yan R., Zhang J., Sang L., Li P., Wang J., Qiu M. Relationship between functional connectivity and motor function assessment in stroke patients with hemiplegia: a resting-state functional MRI study. Neuroradiology. 2016. 58 (5): 503–511.

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