Physical and rehabilitation medicine, medical rehabilitationPhysical and rehabilitation medicine, medical rehabilitation2658-68432949-1436Eco-Vector6594910.36425/rehab65949Research ArticleHardware and Software Complex for Restoring Motor Functions Based on Virtual Reality and Brain-Computer InterfaceNekrasovaIuliia Y.<p>Cand. Sci. (Tech), research associate</p>nekrasova84@yandex.ruhttps://orcid.org/0000-0002-4435-8501VorontsovaViktoriya S.<p>junior research associate</p>vvorontsova@fnkcrr.ruhttps://orcid.org/0000-0002-1490-1331KanarskiiMikhail M.<p>junior research associate</p>kanarmm@yandex.ruhttps://orcid.org/0000-0002-7635-1048PradhanPranil M.<p>junior research associate</p>pranilpr@yandex.ruhttps://orcid.org/0000-0002-3505-7504ShunenkovDenis A.<p>research associate</p>dshunenkov@fnkcrr.ruhttps://orcid.org/0000-0003-3902-0095PuzinSergey S.<p>graduate student</p>pusinserg@mail.ruhttps://orcid.org/0000-0002-9711-3532PaskoIvan V.ipasko@fnkcrr.ruPodolskayaJulia A.<p>research associate</p>julia031181@yandex.ruhttps://orcid.org/0000-0003-3158-8209KriuchkovaAlina Y.<p>laboratory research assistant</p>alinacriuchkova@yandex.ruFederal Scientific and Clinical Center of Intensive Care Medicine and Rehabilitology15062021322312422704202122062021Copyright © 2021, Nekrasova I.Y., Vorontsova V.S., Kanarskii M.M., Pradhan P.M., Shunenkov D.A., Puzin S.S., Pasko I.V., Podolskaya J.A., Kriuchkova A.Y.2021<p>In this paper, we consider a hardware-software complex based on virtual reality and a non-invasive EEG neurocomputer interface, designed to restore motor functions of the limbs in patients with the consequences of severe acquired brain lesions through ideomotor training. The complex is a flexible system that allows to train any movements of both the upper and lower extremities in any virtual environment with varying degrees of immersiveness. The proposed method for assessing desynchronization of the sensorimotor rhythm during imagining movements and the developed algorithm for ideomotor training have been successfully tested on healthy volunteers.</p>VRvirtual realityneurocomputer interfacerehabilitationVRвиртуальная реальностьнейрокомпьютерный интерфейсреабилитация[Riener R, Harders M. Virtual reality in medicine. London: Springer; 2012.][Попов А.П., Баев М.С., Сютина В.И. Применение мультисенсорной стимуляции для восстановления произвольной мышечной силы у больных с последствиями острого нарушения мозгового кровообращения в ранний восстановительный период // European research. 2017. № 7. С. 55–60. [Popov AР, Baev MS, Syutina VI. Application of multisensor stimulation for restoration of the artificial muscle power in patients with effects of acute disorder of cerebral circulation in the early reducing period. European research. 2017;(7):55–60. (In Russ).]][Johansson BB. Multisensory stimulation in stroke rehabilitation. Front Hum Neurosci. 2012;6:60. doi: 10.3389/fnhum.2012.00060][Цинзерлинг В.А., Сапаргалиева А.Д., Вайншенкер Ю.И., Медведев С.В. Проблемы нейропластичности и нейропротекции // Вестник СПбГУ. 2013. № 4. С. 3–13. [Tsinzerling VA, Sapargalieva AD, Vainshenker YI, Medvedev SV. Problems of neuroplasticity and neuroprotection. Bulletin of St. Petersburg State University. 2013;(4):3–13. (In Russ).]][Carr JH, Shepherd RB. Motor relearning programme for stroke. Rockville: Aspen Publishers; 1983.][Wüest S, van de Langenberg R, de Bruin ED. Design considerations for a theory-driven exergame-based rehabilitation program to improve walking of persons with stroke. Eur Rev Aging Phys Act. 2014;11(2):119–129. doi: 10.1007/s11556-013-0136-6][Lledó LD, Díez JA, Bertomeu-Motos A, et al. A comparative analysis of 2D and 3D tasks for virtual reality therapies based on robotic-assisted neurorehabilitation for post-stroke patients. Front Aging Neurosci. 2016;8:205. doi: 10.3389/fnagi.2016.00205][Schmid L, Glässel A, Schuster-Amft C. Therapists’ perspective on virtual reality training in patients after stroke: a qualitative study reporting focus group results from three hospitals. Stroke Res Treat. 2016;2016:6210508. doi: 10.1155/2016/6210508][Saposnik G. Virtual reality in stroke rehabilitation. In: Ovbiagele B. (editor). Ischemic stroke therapeutics. Springer, Cham; 2016; p. 225–233. doi: 10.1007/978-3-319-17750-2_22][Brunner I, Skouen JS, Hofstad H, et al. Virtual reality training for upper extremity in subacute stroke (VIRTUES). Neurology. 2017;89(24):2413–2421. doi: 10.1212/WNL.0000000000004744][Stockley RC, O’Connor DA, Smith P, et al. A mixed methods small pilot study to describe the effects of upper limb training using a virtual reality gaming system in people with chronic stroke. Rehabil Res Pract. 2017;2017:9569178. doi: 10.1155/2017/9569178][Faria AL, Andrade A, Soares L, Badia SB. Benefits of virtual reality based cognitive rehabilitation through simulated activities of daily living: a randomized controlled trial with stroke patients. J Neuroeng Rehabil. 2016;13(1):96–107. doi: 10.1186/s12984-016-0204-z][Kiper P, Agostini M, Luque-Moreno C, et al. Reinforced feedback in virtual environment for rehabilitation of upper extremity dysfunction after stroke: preliminary data from a randomized controlled trial. Biomed Res Int. 2014;2014:752128. doi: 10.1155/2014/752128][Grimm F, Naros G, Gharabaghi A. Closed-loop task difficulty adaptation during virtual reality reach-to-grasp training assisted with an exoskeleton for stroke. Front Neurosci. 2016;10:518. doi: 10.3389/fnins.2016.00518][Lohse KR, Hilderman CG, Cheung KL, et al. Virtual reality therapy for adults poststroke: a systematic review and meta-analysis exploring virtual environments and commercial games in therapy. PLoS One. 2014;9(3):e93318. doi: 10.1371/journal.pone.0093318][Thomson K, Pollock A, Bugge C, Brady M. Commercial gaming devices for stroke upper limb rehabilitation: a systematic review. Int J Stroke. 2014;9(4):479–488. doi: 10.1111/ijs.12263][Tieri G, Tidoni E, Pavone EF, et al. Body visual discontinuity affects feeling of ownership and skin conductance responses. Sci Rep. 2015;5:17139. doi: 10.1038/srep17139][Fusaro M, Tieri G, Aglioti SM. Seeing pain and pleasure on self and others: behavioral and psychophysiological reactivity in immersive virtual reality. J Neurophysiol. 2016;116(6):2656–2662. doi: 10.1152/jn.00489.2016][Slater M, Perez-Marcos D, Ehrsson HH, et al. Towards a digital body: the virtual arm illusion. Front Hum Neurosci. 2008;2:6. doi: 10.3389/neuro.09.006.2008][González-Franco M, Peck TC, Rodríguez-Fornells A, et al. A threat to a virtual hand elicits motor cortex activation. Exp Brain Res. 2014;232(3):875–887. doi: 10.1007/s00221-013-3800-1][Pavone EF, Tieri G, Rizza G, et al. Embodying others in immersive virtual reality: electro-cortical signatures of monitoring the errors in the actions of an avatar seen from a first-person perspective. J Neurosci. 2016;36(2):268–279. doi: 10.1523/JNEUROSCI.0494-15.2016][Baumgartner T. Feeling present in arousing virtual reality worlds: prefrontal brain regions differentially orchestrate presence experience in adults and children. Front Hum Neurosci. 2008;2:1–12. doi: 10.3389/neuro.09.008.2008][Lutz OH, Burmeister C, Ferreira L, et al. Application of headmounted devices with eye-tracking in virtual reality therapy. Curr Dir Biomed Eng. 2017;3(1):53–56. doi: 10.1515/cdbme-2017-0012][Subramanian S, Prasanna S. Virtual reality and non-invasive brain stimulation in stroke: how effective is their combination for upper limb motor improvement? Int Conf Virtual Rehabil. 2017. doi: 10.1109/ICVR.2017.8007539][Tieri G, Gioia A, Scandola M, et al. Visual appearance of a virtual upper limb modulates the temperature of the real hand: a thermal imaging study in Immersive Virtual Reality. Eur J Neurosci. 2017;45(9):1141–1151. doi: 10.1111/ejn.13545][Slobounov SM, Ray W, Johnson B, et al. Modulation of cortical activity in 2D versus 3D virtual reality environments: an EEG study. Int J Psychophysiol. 2015;95(3):254–260. doi: 10.1016/j.ijpsycho.2014.11.003][Yin C, Hsueh YH, Yeh CY, et al. A virtual reality-cycling training system for lower limb balance improvement. Biomed Res Int. 2016;2016:9276508. doi: 10.1155/2016/9276508][Flowers A, Herve JY. BioPresence: a virtual reality biofeedback system. 2018.][Revi. Мультисенсорный тренажер пассивной реабилитации [Интернет]. [Revi. Multisensory simulator of passive rehabilitation [Internet]. (In Russ).] Режим доступа: https://revi.life/revivr/. Дата обращения: 15.03.2021.][Motorica.org. Виртуальная реабилитация в Attilan [Интернет]. [Motorica.org. Virtual rehabilitation in Attilan [Internet]. (In Russ).] Режим доступа: https://motorica.org/virtualnaya-reabilitaciya-v-attilan. Дата обращения: 15.03.2021.][Дудоров Е.А., Богданов А.А., Пермяков А.Ф. Роботизированные комплексы интеллектуального ассистирования специального и медицинского назначения // Наука и инновации в медицине. 2016. Т. 1, № 3. [Dudorov EA, Bogdanov AA, Permyakov AF. Robotized complexes of intellectual assistance for special and medical purposes. Science and innovation in medicine. 2016;1(3). (In Russ).] doi: 10.35693/2500-1388-2016-0-3-83-88][Carmena, JM, Lebedev MA, Crist RE, et al. Learning to control a brain-machine interface for reaching and grasping by primates. PLoS Biol. 2003;1(2):E42. doi: 10.1371/journal.pbio.0000042][Кондур А.А., Котов С.В., Турбина Л.Г., и др. Клиническая эффективность применения высокотехнологичного комплекса интерфейса «мозг, компьютер и экзоскелет кисти» в восстановлении двигательной функции руки после инсульта на основе результатов мультицентрового плацебоконтролируемого клинического исследования // XI Международный конгресс «Нейрореабилитация-2019», Москва, 14–15 марта. Москва, 2019. [Kondur AA, Kotov SV, Turbina LG, et al. Clinical effectiveness of the application of the high-tech complex of the interface «brain, computer and hand exoskeleton» in restoring the motor function of the hand after a stroke based on the results of a multicenter placebo-controlled clinical trial. XI International Congress «Neurorehabilitation-2019», Moscow, March 14–15. Moscow; 2019. (In Russ).]][Pascual-Leone A, Amedi A, Fregni F, Merabet LB. The plastic human brain cortex. Annu Rev Neurosci. 2005;28: 377–401. doi: 10.1146/annurev.neuro.27.070203.144216][Nyberg L, Eriksson J, Larsson A, Marklund P. Learning by doing versus learning by thinking: an MRI study of motor and mental training. Neuropsychologia. 2006;44(5): 711–717. doi: 10.1016/j.neuropsychologia.2005.08.006][Фролов А.А., Бирюкова Е.В., Бобров П.Д., и др. Эффективность комплексной нейрореабилитации пациентов с постинсультным парезом руки с применением нейроинтерфейса «мозг + компьютер + экзоскелет» // Альманах клинической медицины. 2016. Т. 44, № 3. С. 280–286. [Frolov AA, Biryukova EV, Bobrov PD, et al. Efficiency of complex neurorehabilitation of patients with post-stroke paresis of the hand using the «brain + computer interface + exoskeleton». Almanac of Clinical Medicine. 2016;44(3):280–286. (In Russ).] doi: 10.18786/2072-0505-2016-44-3-280-286][Daly JJ, Huggins JE. Brain-computer interface: current and emerging rehabilitation applications. Arch Phys Med Rehabil. 2015;96(3 Suppl):S1–S7. doi: 10.1016/j.apmr.2015.01.007][Bensmaia, SJ, Miller LE. Restoring sensorimotor function through intracortical interfaces: progress and looming challenges. Nat Rev Neurosci. 2014.15(5):313–325. doi: 10.1038/nrn3724][Бирюкова Е.В., Бушкова Ю.В. Объективная оценка состояния двигательной функции до и после реабилитации по технологии ИМК + экзоскелет: биомеханический анализ тестов шкалы Fugl-Meyer // XI Международный конгресс «Нейрореабилитация-2019», Москва, 14–15 марта. Москва, 2019. [Biryukova EV, Bushkova YuV. Objective assessment of the state of motor function before and after rehabilitation using the BCI + exoskeleton technology: biomechanical analysis of Fugl-Meyer scale tests. XI International Congress «Neurorehabilitation-2019», Moscow, March 14–15. Moscow; 2019. (In Russ).]][Rooij M, Lobel A, Owen H, et al. DEEP: a biofeedback virtual reality game for children atrisk for anxiety. In: Proceedings of the 2016 CHI conference extended abstracts on human factors in computing systems — CHI EA’16. ACM Press; 2016. P. 1989–1997. doi: 10.1145/2851581.2892452][Bohil CJ, Alicea B, Biocca FA. Virtual reality in neuroscience research and therapy. Nat Rev Neurosci Nature Publishing Group. 2011;12(12):752–762. doi: 10.1038/nrn3122][Kilteni K, Normand JM, Sanchez-Vives MV, et al. Extending body space in immersive virtual reality: a very long arm illusion. PLoS One. 2012;7(7):e40867. doi: 10.1371/journal.pone.0040867][Peck TC, Seinfeld S, Aglioti SM, et al. Putting yourself in the skin of a black avatar reduces implicit racial bias. Conscious Cogn. 2013;22(3):779–787. doi: 10.1016/j.concog.2013.04.016][Martini M, Perez-Marcos D, Sanchez-Vives MV. What color is my arm? Changes in skin color of an embodied virtual arm modulates pain threshold. Front Hum Neurosci. 2013;7:438. doi: 10.3389/fnhum.2013.00438 eCollection 2013][Normand JM, Giannopoulos E, Spanlang B, et al. Multisensory stimulation can induce an illusion of larger belly size in immersive virtual reality. PLoS One. 2011;6(1):e16128. doi: 10.1371/journal.pone.0016128][Slater M, Spanlang B, Sanchez-Vives MV, et al. First person experience of body transfer in virtual reality. PLoS One. 2010;5(5):e10564. doi: 10.1371/journal.pone.0010564][Maselli A, Slater M. Sliding perspectives: dissociating ownership from self-location during full body illusions in virtual reality. Front Hum Neurosci. 2014;8:1–19. doi: 10.3389/fnhum.2014.00693][Morone G, Paolucci S, Mattia D, et al. The 3Ts of the new millennium neurorehabilitation gym: therapy, technology, translationality. Expert Rev Med Devices. 2016;13(9): 785–787. doi: 10.1080/17434440.2016.1218275][Perez-Marcos D, Solazzi M, Steptoe W, et al. A fully immersive setup for remote interaction and neurorehabilitation based on virtual body ownership. Front Neurol. 2012;3:110. doi: 10.3389/fneur.2012.00110. eCollection 2012][Rizzo AS. Is clinical virtual reality ready for primetime? Neuropsychology, in press 5. Bohil CJ, Alicea B, Biocca FA. Virtual reality in neuroscience research and therapy. Nat Rev Neurosci. 2011;12(12):752–762. doi: 10.1038/nrn3122][Tarr MJ, Warren WH. Virtual reality in behavioral neuroscience and beyond. Nat Neurosci. 2002;5 Suppl:1089–1092. doi: 10.1038/nn948]