An exoskeleton controlled by an epidural wireless brain–machine interface in a tetraplegic patient: a proof-of-concept demonstration
Open accessAbstract
BACKGROUND: Approximately 20% of traumatic cervical spinal cord injuries result in tetraplegia. Neuroprosthetics are being developed to manage this condition and thus improve the lives of patients. We aimed to test the feasibility of a semi-invasive technique that uses brain signals to drive an exoskeleton. METHODS: We recruited two participants at Clinatec research centre, associated with Grenoble University Hospital, Grenoble, France, into our ongoing clinical trial. Inclusion criteria were age 18-45 years, stability of neurological deficits, a need for additional mobility expressed by the patient, ambulatory or hospitalised monitoring, registration in the French social security system, and signed informed consent. The exclusion criteria were previous brain surgery, anticoagulant treatments, neuropsychological sequelae, depression, substance dependence or misuse, and contraindications to magnetoencephalography (MEG), EEG, or MRI. One participant was excluded because of a technical problem with the implants. The remaining participant was a 28-year-old man, who had tetraplegia following a C4-C5 spinal cord injury. Two bilateral wireless epidural recorders, each with 64 electrodes, were implanted over the upper limb sensorimotor areas of the brain. Epidural electrocorticographic (ECoG) signals were processed online by an adaptive decoding algorithm to send commands to effectors (virtual avatar or exoskeleton). Throughout the 24 months of the study, the patient did various mental tasks to progressively increase the number of degrees of freedom. FINDINGS: Between June 12, 2017, and July 21, 2019, the patient cortically controlled a programme that simulated walking and made bimanual, multi-joint, upper-limb movements with eight degrees of freedom during various reach-and-touch tasks and wrist rotations, using a virtual avatar at home (64·0% [SD 5·1] success) or an exoskeleton in the laboratory (70·9% [11·6] success). Compared with microelectrodes, epidural ECoG is semi-invasive and has similar efficiency. The decoding models were reusable for up to approximately 7 weeks without recalibration. INTERPRETATION: These results showed long-term (24-month) activation of a four-limb neuroprosthetic exoskeleton by a complete brain-machine interface system using continuous, online epidural ECoG to decode brain activity in a tetraplegic patient. Up to eight degrees of freedom could be simultaneously controlled using a unique model, which was reusable without recalibration for up to about 7 weeks. FUNDING: French Atomic Energy Commission, French Ministry of Health, Edmond J Safra Philanthropic Foundation, Fondation Motrice, Fondation Nanosciences, Institut Carnot, Fonds de Dotation Clinatec.
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A comparable robustness and stability of this computational and technological brain decoding framework has now been observed in two additional individuals with tetraplegia.
“Third, a comparable robustness and stability of this computational and technological brain decoding framework has now been observed in two additional individuals with tetraplegia3,26,29.”
From Walking naturally after spinal cord injury using a brain–spine interface (2023) · cites this paper as [3]
The Discussion reports stable decoding without recalibration for several weeks, but only for the study’s single evaluated participant. The Magnetic resonance imaging (MRI) section says the other implanted patient was excluded and three further patients were still being recruited; it does not support an observation in two additional individuals. Page numbers are unavailable in our copy. (LLM, conf=0.88)
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Cites
Reach and grasp by people with tetraplegia using a neurally controlled robotic arm
Hochberg, L. R., Bacher, D., Jarosiewicz, B., Masse, N. Y., Simeral, J. D., Vogel, J., Haddadin, S., Liu, J., Cash, S. S., van der Smagt, P., et al. (2012) · Nature · doi:10.1038/nature11076 · Cited by 2,719 · see citing works
Localization of the motor hand area to a knob on the precentral gyrus. A new landmark
Yousry, T. A. (1997) · Brain · doi:10.1093/brain/120.1.141 · Cited by 1,840 · see citing works
Direct Cortical Control of 3D Neuroprosthetic Devices
Taylor, D. M., Tillery, S. I. H., & Schwartz, A. B. (2002) · Science · doi:10.1126/science.1070291 · Cited by 1,542 · see citing works
Restoring cortical control of functional movement in a human with quadriplegia
Bouton, C. E., Shaikhouni, A., Annetta, N. V., Bockbrader, M. A., Friedenberg, D. A., Nielson, D. M., Sharma, G., Sederberg, P. B., Glenn, B. C., Mysiw, W. J., et al. (2016) · Nature · doi:10.1038/nature17435 · Cited by 924 · see citing works
Ajiboye, A. B., Willett, F. R., Young, D. R., Memberg, W. D., Murphy, B. A., Miller, J. P., Walter, B. L., Sweet, J. A., Hoyen, H. A., Keith, M. W., et al. (2017) · The Lancet · doi:10.1016/s0140-6736(17)30601-3 · Cited by 862 · see citing works
A brain–spine interface alleviating gait deficits after spinal cord injury in primates
Capogrosso, M., Milekovic, T., Borton, D., Wagner, F., Moraud, E. M., Mignardot, J.-B., Buse, N., Gandar, J., Barraud, Q., Xing, D., et al. (2016) · Nature · doi:10.1038/nature20118 · Cited by 635 · see citing works
Fully Implanted Brain–Computer Interface in a Locked-In Patient with ALS
Vansteensel, M. J., Pels, E. G. M., Bleichner, M. G., Branco, M. P., Denison, T., Freudenburg, Z. V., Gosselaar, P., Leinders, S., Ottens, T. H., Van Den Boom, M. A., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmoa1608085 · Cited by 578 · see citing works
Wodlinger, B., Downey, J. E., Tyler-Kabara, E. C., Schwartz, A. B., Boninger, M. L., & Collinger, J. L. (2015) · Journal of Neural Engineering · doi:10.1088/1741-2560/12/1/016011 · Cited by 536 · see citing works
Simeral, J. D., Kim, S.-P., Black, M. J., Donoghue, J. P., & Hochberg, L. R. (2011) · Journal of Neural Engineering · doi:10.1088/1741-2560/8/2/025027 · Cited by 496 · see citing works
Restoration of neural output from a paralyzed patient by a direct brain connection
Kennedy, P. R., & Bakay, R. A. E. (1998) · Neuroreport · doi:10.1097/00001756-199806010-00007 · Cited by 475 · see citing works
Brain oscillations control hand orthosis in a tetraplegic
Pfurtscheller, G., Guger, C., Müller, G., Krausz, G., & Neuper, C. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01471-3 · Cited by 472 · see citing works
Donati, A. R. C., Shokur, S., Morya, E., Campos, D. S. F., Moioli, R. C., Gitti, C. M., Augusto, P. B., Tripodi, S., Pires, C. G., Pereira, G. A., et al. (2016) · Scientific Reports · doi:10.1038/srep30383 · Cited by 428 · see citing works
Frolov, A., Mokienko, O. A., Lyukmanov, R. K., Biryukova, E., Kotov, S. V., Григорьевна, Т. Л., Nadareyshvily, G., & Bushkova, Y. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00400 · Cited by 412 · see citing works
An Electrocorticographic Brain Interface in an Individual with Tetraplegia
Wang, W., Collinger, J. L., Degenhart, A. D., Tyler‐Kabara, E. C., Schwartz, A. B., Moran, D. W., Weber, D. J., Wodlinger, B., Vinjamuri, R. K., Ashmore, R. C., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055344 · Cited by 396 · see citing works
Making brain–machine interfaces robust to future neural variability
Sussillo, D., Stavisky, S. D., Kao, J. C., Ryu, S. I., & Shenoy, K. V. (2016) · Nature Communications · doi:10.1038/ncomms13749 · Cited by 214 · see citing works
WIMAGINE: Wireless 64-Channel ECoG Recording Implant for Long Term Clinical Applications
Mestais, C. S., Charvet, G., Sauter-Starace, F., Foerster, M., Ratel, D., & Benabid, A. L. (2015) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2014.2333541 · Cited by 202 · see citing works
Self-citationHatsopoulos, N., & Suminski, A. J. (2011) · Neuron · doi:10.1016/j.neuron.2011.10.020 · Cited by 172 · see citing works
Felton, E. A., Wilson, J. A., Williams, J. C., & Garell, P. C. (2007) · Journal of neurosurgery · doi:10.3171/jns.2007.106.3.495 · Cited by 154 · see citing works
Stable long-term BCI-enabled communication in ALS and locked-in syndrome using LFP signals
Milekovic, T., Sarma, A. A., Bacher, D., Simeral, J. D., Saab, J., Pandarinath, C., Sorice, B. L., Blabe, C. H., Oakley, E. M., Tringale, K. R., et al. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00493.2017 · Cited by 142 · see citing works
First North American fossil monkey and early Miocene tropical biotic interchange
Bloch, J. I., Woodruff, E. D., Wood, A. R., Rincón, A. F., Harrington, A. R., Morgan, G. S., Foster, D. A., Montes, C., Jaramillo, C. A., Jud, N. A., et al. (2016) · Nature · doi:10.1038/nature17415 · Cited by 99 · see citing works
Cortical Areas Involved in Virtual Movement of Phantom Limbs: Comparison with Normal Subjects
Roux, F., Lotterie, J.-A., Cassol, E., Lazorthes, Y. R., Sol, J., & Berry, I. (2003) · Neurosurgery · doi:10.1227/01.neu.0000093424.71086.8f · Cited by 74 · see citing works
Eliseyev, A., Auboiroux, V., Costecalde, T., Langar, L., Charvet, G., Mestais, C., Aksenova, T., & Benabid, A.-L. (2017) · Scientific Reports · doi:10.1038/s41598-017-16579-9 · Cited by 42 · see citing works
Self-citationElnady, A. M., Zhang, X., Xiao, Z. G., Yong, X., Randhawa, B. K., Boyd, L. A., & Menon, C. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00168 · Cited by 40 · see citing works
The Time Course of Corticospinal Excitability during a Simple Reaction Time Task
Kennefick, M., Maslovat, D., & Carlsen, A. N. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113563 · Cited by 39 · see citing works
Long-Term Sheep Implantation of WIMAGINE®, a Wireless 64-Channel Electrocorticogram Recorder
Sauter-Starace, F., Ratel, D., Crétallaz, C., Foerster, M., Lambert, A., Gaude, C., Costecalde, T., Bonnet, S., Charvet, G., Aksenova, T., et al. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00847 · Cited by 30 · see citing works
Self-citationMorinière, B., Verney, A., Abroug, N., et al. (2015) · IEEE/RSJ International Conference on Intelligent Robots and Systems (IROS) · doi:10.1109/iros.2015.7354130 · Cited by 19 · see citing works
Self-citationSchaeffer, M.-C., & Aksenova, T. (2016) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2017.03.002 · Cited by 18 · see citing works
Self-citationEliseyev, A., Moro, C., Costecalde, T., Torres-Martinez, N., Gharbi, S., Mestais, C., Benabid, A. L., & Aksenova, T. (2011) · Journal of Neural Engineering · doi:10.1088/1741-2560/8/4/046012 · Cited by 17 · see citing works
Self-citationCould cortical signals control intraspinal stimulators? A theoretical evaluation
Mushahwar, V. K., Guevremont, L., & Saigal, R. (2006) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2006.875532 · Cited by 13 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Friggeri A. « Influence du type et du niveau de la lesion, du délai chirurgical et des complications respiratoires sur la récuperation clinique à un an » (French). 2006, MD Thesis, Amiens University, France.
- Rose J, Gamble JG. (2006). Human walking. ed. Philadelphia, PA: Lippincott Williams & Wilkins.
Cited by
Sorted by citations
Walking naturally after spinal cord injury using a brain–spine interface
Lorach, H., Galvez, A., Spagnolo, V., Martel, F., Karakas, S., Intering, N., Vat, M., Faivre, O., Harte, C., Komi, S., et al. (2023) · Nature · doi:10.1038/s41586-023-06094-5 · Cited by 631 · see citing works
“This brain–spine interface (BSI) consists of fully implanted recording and stimulation systems that establish a direct link between cortical signals 3 and the analogue modulation of epidural electrical stimulation targeting the spinal cord regions involved in the production of walking 4–6 .”
BackgroundMethodInfluentialSelf-citationRowald, A., Komi, S., Demesmaeker, R., Baaklini, E., Hernandez-Charpak, S. D., Paoles, E., Montanaro, H., Cassara, A., Becce, F., Lloyd, B., et al. (2022) · Nature Medicine · doi:10.1038/s41591-021-01663-5 · Cited by 455 · see citing works
Oxley, T. J., Yoo, P. E., Rind, G. S., Ronayne, S. M., Lee, C. M. S., Bird, C., Hampshire, V., Sharma, R. P., Morokoff, A., Williams, D. L., et al. (2021) · Journal of NeuroInterventional Surgery · doi:10.1136/neurintsurg-2020-016862 · Cited by 243 · see citing works
Simeral, J. D., Hosman, T., Saab, J., Flesher, S. N., Vilela, M., Franco, B., Kelemen, J. N., Brandman, D. M., Ciancibello, J. G., Rezaii, P. G., et al. (2021) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2021.3069119 · Cited by 165 · see citing works
Plug-and-play control of a brain–computer interface through neural map stabilization
Silversmith, D. B., Abiri, R., Hardy, N. F., Natraj, N., Tu-Chan, A., Chang, E. F., & Ganguly, K. (2021) · Nature Biotechnology · doi:10.1038/s41587-020-0662-5 · Cited by 126 · see citing works
Strategies and prospects of effective neural circuits reconstruction after spinal cord injury
Yang, B., Zhang, F., Cheng, F., Ying, L., Wang, C., Shi, K., Wang, J., Xia, K., Gong, Z., Huang, X., et al. (2020) · Cell Death & Disease · doi:10.1038/s41419-020-2620-z · Cited by 128 · see citing works
Brain-Computer Interface: Applications to Speech Decoding and Synthesis to Augment Communication
Luo, S., Rabbani, Q., & Crone, N. E. (2022) · Neurotherapeutics · doi:10.1007/s13311-022-01190-2 · Cited by 106 · see citing works
Luo, S., Angrick, M., Coogan, C., Candrea, D. N., Wyse‐Sookoo, K., Shah, S., Rabbani, Q., Milsap, G. W., Weiss, A. R., Anderson, W. S., et al. (2023) · Advanced Science · doi:10.1002/advs.202304853 · Cited by 90 · see citing works
Duffau, H. (2021) · Acta Neurochirurgica · doi:10.1007/s00701-021-04752-z · Cited by 69 · see citing works
Moly, A., Costecalde, T., Martel, F., Martin, M., Larzabal, C., Karakas, S., Verney, A., Charvet, G., Chabardes, S., Benabid, A. L., et al. (2022) · Journal of Neural Engineering · doi:10.1088/1741-2552/ac59a0 · Cited by 65 · see citing works
Self-citationLong-term stability of the chronic epidural wireless recorder WIMAGINE in tetraplegic patients
Larzabal, C., Bonnet, S., Costecalde, T., Auboiroux, V., Charvet, G., Chabardes, S., Aksenova, T., & Sauter-Starace, F. (2021) · Journal of Neural Engineering · doi:10.1088/1741-2552/ac2003 · Cited by 37 · see citing works
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Dabbour, A.-H., Tan, S., Kim, S. H., Guild, S.-J., Heppner, P., McCormick, D., Wright, B. E., Leung, D., Gallichan, R., Budgett, D., et al. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.796203 · Cited by 13 · see citing works
- Authors
- Benabid, A. L., Costecalde, T., Eliseyev, A., Charvet, G., Verney, A., Karakas, S., Foerster, M., Lambert, A., Morinière, B., Abroug, N., Schaeffer, M.-C., Moly, A., Sauter-Starace, F., Ratel, D., Moro, C., Torres-Martinez, N., Langar, L., Oddoux, M., Polosan, M., Pezzani, S., Auboiroux, V., Aksenova, T., Mestais, C., & Chabardes, S.
- Affiliations
- Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR)
- Centre Hospitalier Universitaire de Grenoble (FR)
- Corresponding author
- Benabid, Alim Louis
- ORCID
- Venue
- The Lancet Neurology
- Publisher
- Elsevier BV
- Published
- 2019-12
- Volume
- 18
- Issue
- 12
- Pages
- 1112-1122
- ISSN
- 1474-4422 (ISSN-L)
- OpenAlex
- W2978677644
- Cited by
- 404
- References
- 29
- Citations by year
- 2026: 34 · 2025: 64 · 2024: 58 · 2023: 63 · 2022: 51 · 2021: 83 · 2020: 40 · 2019: 11
- FWCI
- 26.88
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- The Lancet Neurology (acceptedVersion, other-oa)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by-nc)
- Funders
- French Ministry of Health (PHRC-15-15-0124)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › EEG and Brain-Computer Interfaces
- Health Sciences › Medicine › Pathology and Forensic Medicine › Spinal Cord Injury Research
- Physical Sciences › Engineering › Biomedical Engineering › Prosthetics and Rehabilitation Robotics
- Keywords
- brain-computer interface, tetraplegia, cervical spinal cord injury, upper limb motor control, adaptive decoding, avatars, bimanual movement, wrist rotation
- MeSH terms
- Exoskeleton Device, Proof of Concept Study, Adult, Cervical Vertebrae, Epidural Space, Humans, Magnetic Resonance Imaging, Male, Quadriplegia, Spinal Cord Injuries, Magnetoencephalography, Implantable Neurostimulators, Wireless Technology, Brain-Computer Interfaces, Sensorimotor Cortex
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