Abstract
Purpose
To assess if transfer learning strategies can improve stroke patients’ ability to control a Brain-computer interface (BCI) based on motor intention across an upper extremity neurorehabilitation intervention.
Methods
Three subject-specific session-to-session training strategies were retrospectively assessed in the present study, using information acquired during a BCI intervention in 12 stroke patients. One strategy used data from the previous therapy session (previous session), another used data from all previous sessions (accumulative) and another initially used previous session’s data and was updated with data acquired during the current session (instantaneous).
Results
Classification accuracy was significantly higher with the instantaneous strategy (median = 76.4%, IQR = [68.7%, 81.5%]) compared to the obtained with the accumulative (71.67%, [65.1%, 78.5%]) and previous session (69.2%, [59%, 77.4%]) strategies. Median classification accuracies across sessions were also higher with the instantaneous strategy in each BCI intervention session.
Conclusion
The instantaneous strategy could allow stroke patients to achieve a competitive level of BCI performance during a motor intention BCI intervention without reducing effective therapy time or requiring data from other patients.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Wolpaw, J. R., Birbaumer, N., McFarland, D. J., Pfurtscheller, G., & Vaughan, T. M. (2002). Brain–computer interfaces for communication and control. Clinical Neurophysiology, 113(6), 767–791. https://doi.org/10.1016/S1388-2457(02)00057-3
Kerous, B., Skola, F., & Liarokapis, F. (2018). EEG-based BCI and video games: A progress report. Virtual Reality, 22(2), 119–135. https://doi.org/10.1007/s10055-017-0328-x
Morin, C. (2011). Neuromarketing: The new science of consumer behavior. Society, 48(2), 131–135. https://doi.org/10.1007/s12115-010-9408-1
Bamdad, M., Zarshenas, H., & Auais, M. A. (2015). Application of BCI systems in neurorehabilitation: A scoping review. Disability and Rehabilitation Assistive Technology, 10(5), 355–364. https://doi.org/10.3109/17483107.2014.961569
Mane, R., Chouhan, T., & Guan, C. (2020). BCI for stroke rehabilitation: Motor and beyond. Journal of Neural Engineering, 17(4), 041001. https://doi.org/10.1088/1741-2552/aba162
Tsao, C. W., Aday, A. W., Almarzooq, Z. I., Alonso, A., Beaton, A. Z., Bittencourt, M. S., & Martin, S. S. (2022). Heart disease and stroke statistics—2022 update: A report from the american heart association. Circulation, 145(8). https://doi.org/10.1161/CIR.0000000000001052
Hatem, S. M., Saussez, G., della Faille, M., Prist, V., Zhang, X., Dispa, D., & Bleyenheuft, Y. (2016). Rehabilitation of motor function after stroke: A multiple systematic review focused on techniques to stimulate Upper Extremity Recovery. Frontiers in Human Neuroscience, 10. https://doi.org/10.3389/fnhum.2016.00442
Frolov, A. A., Mokienko, O., Lyukmanov, R., Biryukova, E., Kotov, S., Turbina, L., … Bushkova, Y. (2017). Post-stroke rehabilitation training with a motor-imagery-based brain-computer interface (BCI)-controlled hand exoskeleton: A randomized controlled multicenter trial. Frontiers in Neuroscience, 11. https://doi.org/10.3389/fnins.2017.00400
Ang, K. K., Chua, K. S. G., Phua, K. S., Wang, C., Chin, Z. Y., Kuah, C. W. K., … Guan, C. (2015). A randomized controlled trial of eeg-based motor imagery brain-computer interface robotic rehabilitation for stroke. Clinical EEG and Neuroscience, 46(4), 310–320. https://doi.org/10.1177/1550059414522229
Ang, K. K., Guan, C., Phua, K. S., Wang, C., Zhou, L., Tang, K. Y., … Chua, K. S. G. (2014). Brain-computer interface-based robotic end effector system for wrist and hand rehabilitation: results of a three-armed randomized controlled trial for chronic stroke. Frontiers in Neuroengineering, 7. https://doi.org/10.3389/fneng.2014.00030
Monteiro, K. B., Cardoso, M. S., Cabral, V. R. da, Santos, C., dos, A. O. B., Silva, P. S., de da, Castro, J. B. P., & de Vale, R. G. (2021). S. Effects of motor imagery as a complementary resource on the rehabilitation of stroke patients: A meta-analysis of randomized trials. Journal of Stroke and Cerebrovascular Diseases, 30(8), 105876. https://doi.org/10.1016/j.jstrokecerebrovasdis.2021.105876
Remsik, A. B., Dodd, K., Williams Jr, L., Thoma, J., Jacobson, T., Allen, J. D., … Prabhakaran, V. (2018). Behavioral outcomes following brain-computer interface intervention for upper extremity rehabilitation in stroke: A randomized controlled trial. Frontiers in neuroscience, 12, 752. https://doi.org/10.3389/fnins.2018.00752
Kim, T., Kim, S., & Lee, B. (2016). Effects of Action Observational Training Plus Brain-Computer interface-based functional electrical stimulation on paretic Arm Motor Recovery in patient with stroke: A randomized controlled trial. Occupational Therapy International, 23(1), 39–47. https://doi.org/10.1002/oti.1403
Jeunet, C., Jahanpour, E., & Lotte, F. (2016). Why standard brain-computer interface (BCI) training protocols should be changed: An experimental study. Journal of Neural Engineering, 13(3), 036024. https://doi.org/10.1088/1741-2560/13/3/036024
López-Larraz, E., Sarasola-Sanz, A., Irastorza-Landa, N., Birbaumer, N., & Ramos-Murguialday, A. (2018). Brain-machine interfaces for rehabilitation in stroke: A review. Neurorehabilitation, 43, 77–97. https://doi.org/10.3233/NRE-172394
McFarland, D. J., & Wolpaw, J. R. (2017). EEG-based brain–computer interfaces. Current Opinion in Biomedical Engineering, 4, 194–200. https://doi.org/10.1016/j.cobme.2017.11.004
Arias-Carrion, O. (2021). Brain-computer interface coupled to a robotic hand orthosis for stroke patients’ neurorehabilitation: A crossover feasibility study. Frontiers in Human Neuroscience, 15(June), 1–15. https://doi.org/10.3389/fnhum.2021.656975
Ramos-Murguialday, A., Broetz, D., Rea, M., Läer, L., Yilmaz, Ö., Brasil, F. L., … Birbaumer, N. (2013). Brain-machine interface in chronic stroke rehabilitation: A controlled study. Annals of Neurology, 74(1), 100–108. https://doi.org/10.1002/ana.23879
Biasiucci, A., Leeb, R., Iturrate, I., Perdikis, S., Al-Khodairy, A., Corbet, T., … Millán, J. D. R. (2018). Brain-actuated functional electrical stimulation elicits lasting arm motor recovery after stroke. Nature communications, 9(1), 2421. https://doi.org/10.1038/s41467-018-04673-z
Jayaram, V., Alamgir, M., Altun, Y., Scholkopf, B., & Grosse-Wentrup, M. (2016). Transfer learning in brain-computer interfaces. IEEE Computational Intelligence Magazine, 11(1), 20–31. https://doi.org/10.1109/MCI.2015.2501545
Ang, K. K., & Guan, C. (2017). EEG-Based strategies to detect motor imagery for control and rehabilitation. IEEE Transactions on Neural Systems and Rehabilitation Engineering, 25(4), 392–401. https://doi.org/10.1109/TNSRE.2016.2646763
López-Larraz, E., Ibáñez, J., Trincado-Alonso, F., Monge-Pereira, E., Pons, J. L., & Montesano, L. (2018). Comparing recalibration strategies for electroencephalography-based decoders of movement intention in neurological patients with motor disability. International Journal of Neural Systems, 28(07), 1750060. https://doi.org/10.1142/S0129065717500605
Giles, J., Ang, K. K., Phua, K. S., & Arvaneh, M. (2022). A transfer learning algorithm to reduce brain-computer interface calibration time for long-term users. Frontiers in Neuroergonomics, 3. https://doi.org/10.3389/fnrgo.2022.837307
Blankertz, B., Tomioka, R., Lemm, S., Kawanabe, M., & Müller, K. R. (2008). Optimizing spatial filters for robust EEG single-trial analysis. IEEE Signal Processing Magazine, 25(1), 41–56. https://doi.org/10.1109/MSP.2007.909009
Ang, K. K., Chin, Z. Y., Wang, C., Guan, C., & Zhang, H. (2012). Filter bank common spatial pattern algorithm on BCI Competition IV datasets 2a and 2b. Frontiers in Neuroscience, 6, 39. https://doi.org/10.3389/fnins.2012.00039
Carino-Escobar, R. I., Rodriguez-Barragan, M. A., Carrillo-Mora, P., & Cantillo-Negrete, J. (2022). Brain-computer interface as complementary therapy for hemiparesis in an astrocytoma patient. Neurological Sciences, 43(4), 2879–2881. https://doi.org/10.1007/s10072-022-05924-0
Cantillo-Negrete, J. (2022). A case report: Upper limb recovery from stroke related to SARS-CoV-2 infection during an intervention with a brain-computer interface. Frontiers in Neurology, 13. https://doi.org/10.3389/fneur.2022.1010328
Carino-Escobar, R. I., Rodríguez-García, M. E., Carrillo-Mora, P., Valdés-Cristerna, R., & Cantillo-Negrete, J. (2023). Continuous versus discrete robotic feedback for brain-computer interfaces aimed for neurorehabilitation. Frontiers in Neurorobotics, 17. https://doi.org/10.3389/fnbot.2023.1015464
Irimia, D. C., Ortner, R., Poboroniuc, M. S., Ignat, B. E., & Guger, C. (2018). High classification accuracy of a motor imagery based brain-computer interface for stroke rehabilitation training. Frontiers in Robotics and AI, 5, 130. https://doi.org/10.3389/frobt.2018.00130
Vourvopoulos, A., Jorge, C., Abreu, R., Figueiredo, P., Fernandes, J. C., & Bermúdez i Badia, S. (2019). Efficacy and brain imaging correlates of an immersive motor imagery BCI-Driven VR system for upper limb motor rehabilitation: A clinical case report. Frontiers in Human Neuroscience, 13. https://doi.org/10.3389/fnhum.2019.00244
Ang, K. K., Guan, C., Chua, K. S. G., Ang, B. T., Kuah, C. W. K., Wang, C., … Zhang, H. (2011). A large clinical study on the ability of stroke patients to use an EEG-based motor imagery brain-computer interface. Clinical EEG and Neuroscience, 42(4), 253–258. https://doi.org/10.1177/155005941104200411
Wang, C., Phua, K. S., Ang, K. K., Guan, C., Zhang, H., Rongsheng Lin, … Kuah, C. W. K. (2009). A feasibility study of non-invasive motor-imagery BCI-based robotic rehabilitation for stroke patients. In 2009 4th International IEEE/EMBS Conference on Neural Engineering (pp. 271–274). IEEE. https://doi.org/10.1109/NER.2009.5109285
Irimia, D. C., Cho, W., Ortner, R., Allison, B. Z., Ignat, B. E., Edlinger, G., & Guger, C. (2017). Brain-computer interfaces with Multi‐sensory feedback for stroke rehabilitation: A case study. Artificial Organs, 41(11). https://doi.org/10.1111/aor.13054
Arvaneh, M., Guan, C., Ang, K. K., Ward, T. E., Chua, K. S. G., Kuah, C. W. K., … Wang, C. (2017). Facilitating motor imagery-based brain–computer interface for stroke patients using passive movement. Neural Computing and Applications, 28(11), 3259–3272. https://doi.org/10.1007/s00521-016-2234-7
Barsotti, M., Leonardis, D., Loconsole, C., Solazzi, M., Sotgiu, E., Procopio, C., … Frisoli, A. (2015). A full upper limb robotic exoskeleton for reaching and grasping rehabilitation triggered by MI-BCI. In 2015 IEEE International Conference on Rehabilitation Robotics (ICORR) (pp. 49–54). IEEE. https://doi.org/10.1109/ICORR.2015.7281174
Nagarajan, A., Robinson, N., Ang, K. K., Chua, K. S. G., Chew, E., & Guan, C. (2024). Transferring a deep learning model from healthy subjects to stroke patients in a motor imagery brain–computer interface. Journal of Neural Engineering, 21(1), 016007. https://doi.org/10.1088/1741-2552/ad152f
Acknowledgements
Authors would like to acknowledge Consejo Nacional de Ciencia y Tecnología (CONACYT) for supporting this work with grant number SALUD-2018-02-B-S-45803. Authors would also like to thank Martín Emiliano Rodríguez-García for his assistance in programming some of the software used to assess BCI performance. Also, authors would like to thank Marlene A. Rodriguez Barragan, Claudia Hernandez-Arenas and Jimena Quinzaños-Fresnedo for their help in patients’ recruitment.
Funding
This work was supported by Consejo Nacional de Ciencia y Tecnología (CONACYT) (Grant number SALUD-2018-02-B-S-45803).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Jessica Cantillo-Negrete, Luis A. Franceschi-Jimenez, Paul Carrillo-Mora and Ruben I. Carino-Escobar. The first draft of the manuscript was written by Ruben I. Carino-Escobar and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.”
Corresponding author
Ethics declarations
Ethical Approval
This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics and Research Committees of the National Institute of Rehabilitation Luis Guillermo Ibarra Ibarra with approval numbers 36/15 and 25/19 AC.
Consent to Participate
Informed consent was obtained from all individual participants included in the study.
Competing Interests
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Carino-Escobar, R.I., Franceschi-Jimenez, L.A., Carrillo-Mora, P. et al. Subject-Specific Session-to-Session Transfer Learning Strategies for Increasing Brain-Computer Interface Performance during Upper Extremity Neurorehabilitation in Stroke. J. Med. Biol. Eng. 44, 596–606 (2024). https://doi.org/10.1007/s40846-024-00891-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40846-024-00891-7