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Neuromodulation of lumbosacral spinal networks enables independent stepping after complete paraplegia
Abstract
Spinal sensorimotor networks that are functionally disconnected from the brain because of spinal cord injury (SCI) can be facilitated via epidural electrical stimulation (EES) to restore robust, coordinated motor activity in humans with paralysis 1-3. Previously, we reported a clinical case of complete sensorimotor paralysis of the lower extremities in which EES restored the ability to stand and the ability to control step-like activity while side-lying or suspended vertically in a body-weight support system (BWS)4. Since then, dynamic task-specific training in the presence of EES, termed multimodal rehabilitation (MMR), was performed for 43 weeks and resulted in bilateral stepping on a treadmill, independent from trainer assistance or BWS. Additionally, MMR enabled independent stepping over ground while using a front-wheeled walker with trainer assistance at the hips to maintain balance. Furthermore, MMR engaged sensorimotor networks to achieve dynamic performance of standing and stepping. To our knowledge, this is the first report of independent stepping enabled by task-specific training in the presence of EES by a human with complete loss of lower extremity sensorimotor function due to SCI.
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“This recovery has been documented in various independent studies, including in participants with complete sensorimotor paralysis5,6,30–34.”
From Walking naturally after spinal cord injury using a brain–spine interface (2023) · cites this paper as [33]
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“The delivery of epidural electrical stimulation over the lumbar spinal cord has enabled many individuals with spinal cord injury to regain adaptive control over the activity of otherwise paralysed muscles.”
From Walking naturally after spinal cord injury using a brain–spine interface (2023) · cites this paper as [33]
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Advances in Spinal Cord Stimulation
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Neuromusculoskeletal Modeling-Based Prostheses for Recovery After Spinal Cord Injury
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A review of emerging neuroprotective and neuroregenerative therapies in traumatic spinal cord injury
Hejrati, N., & Fehlings, M. G. (2021) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2021.08.009 · Cited by 61
Electrical Stimulation as a Tool to Promote Plasticity of the Injured Spinal Cord
Jack, A. S., Hurd, C., Martin, J. H., & Fouad, K. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2020.7033 · Cited by 58
Zhou, K., Wei, W., Yang, D., Zhang, H., Yang, W., Zhang, Y., Nie, Y., Hao, M., Wang, P., Ruan, H., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-44898-9 · Cited by 58
Seáñez, I., & Capogrosso, M. (2021) · Bioelectronic Medicine · doi:10.1186/s42234-021-00077-5 · Cited by 58
“In 2018, three independent groups demonstrated, for the first time, that participants with chronic motor-complete SCI could achieve overground walking with SCS (Angeli et al. 2018; Gill et al. 2018; Wagner et al. 2018).”
BackgroundInfluentialTargeting Sensory and Motor Integration for Recovery of Movement After CNS Injury
Asan, A. S., McIntosh, J. R., & Carmel, J. B. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.791824 · Cited by 71
Izzy, S. (2024) · CONTINUUM Lifelong Learning in Neurology · doi:10.1212/con.0000000000001392 · Cited by 55
Wang, X., Zhou, T., Maynard, G. D., Terse, P., Cafferty, W. B. J., Kocsis, J. D., & Strittmatter, S. M. (2020) · Brain · doi:10.1093/brain/awaa116 · Cited by 54
“This point is highlighted by the ability of caudal stimulation to support limited voluntary movement recovery in otherwise clinically complete SCI cases (Angeli et al., 2018; Gill et al., 2018; Wagner et al., 2018).”
BackgroundEpidural Spinal Cord Stimulation for Spinal Cord Injury in Humans: A Systematic Review
Chalif, J. I., Chavarro, V. S., Mensah, E. O., Johnston, B. R., Fields, D. P., Chalif, E. J., Chiang, M., Sutton, O. M., Yong, R. J., Trumbower, R. D., et al. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13041090 · Cited by 60
“Although several of the studies reported results from trials registered on Clinical-trials.gov [39–41, 43, 45, Finally, most articles utilized qualitative assessments as the primary outcomes (Table 3).”
BackgroundResultInfluentialPaired corticospinal-motoneuronal stimulation and exercise after spinal cord injury
Jo, H. J., Richardson, M. S. A., Oudega, M., & Pérez, M. A. (2021) · Journal of Spinal Cord Medicine · doi:10.1080/10790268.2021.1970908 · Cited by 52
Herrity, A. N., Aslan, S. C., Ugiliweneza, B., Mohamed, A., Hubscher, C. H., & Harkema, S. J. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2020.614691 · Cited by 53
A Review of Functional Restoration From Spinal Cord Stimulation in Patients With Spinal Cord Injury
Lin, A., Shaaya, E. A., Calvert, J. S., Parker, S. R., Borton, D. A., & Fridley, J. (2022) · Neurospine · doi:10.14245/ns.2244652.326 · Cited by 52
Self-citationComplications of epidural spinal stimulation: lessons from the past and alternatives for the future
Taccola, G., Barber, S. M., Horner, P. J., Bazo, H. A. C., & Sayenko, D. G. (2020) · Spinal Cord · doi:10.1038/s41393-020-0505-8 · Cited by 53
“Although transcutaneous SCS can augment and enable stepping movements [98–102, 118] and postural control during sitting [104] and standing [105], the fine and selective voluntary activation of specific agonists (with minimum co-contraction of antagonists) below spinal lesion after clinically diagnosed motor “complete”…”
BackgroundSelf-citationClinical guidelines for neurorestorative therapies in spinal cord injury (2021 China version)
Guo, X., Feng, Y., Sun, T., Feng, S., Tang, J., Chen, L., Cao, X., Lin, H., He, X., Li, M.-H., et al. (2021) · Journal of Neurorestoratology · doi:10.26599/jnr.2021.9040003 · Cited by 50
Mendez, A., Islam, R., Latypov, T. H., Basa, P., Joseph, O. J., Knudsen, B. E., Siddiqui, A. M., Summer, P., Staehnke, L. J., Grahn, P. J., et al. (2021) · Mayo Clinic Proceedings · doi:10.1016/j.mayocp.2020.07.039 · Cited by 51
Self-citationMechanisms of Stem Cell Therapy in Spinal Cord Injuries
Shinozaki, M., Nagoshi, N., Nakamura, M., & Okano, H. (2021) · Cells · doi:10.3390/cells10102676 · Cited by 58
Liu, G., An, Z., Lu, Y., Wu, Y., Shi, Z., Li, X., Li, X., Wen, H., Peng, Z., Han, R. P. S., et al. (2023) · Nano Energy · doi:10.1016/j.nanoen.2023.109098 · Cited by 51
Transspinal stimulation increases motoneuron output of multiple segments in human spinal cord injury
Murray, L. M., & Knikou, M. (2019) · PLoS ONE · doi:10.1371/journal.pone.0213696 · Cited by 48
Spinal motor mapping by epidural stimulation of lumbosacral posterior roots in humans
Hofstoetter, U. S., Perret, I., Bayart, A., Lackner, P., Binder, H., Freundl, B., & Minassian, K. (2020) · iScience · doi:10.1016/j.isci.2020.101930 · Cited by 47
Angeli, C., Rejc, E., Boakye, M., Herrity, A. N., Mesbah, S., Hubscher, C. H., Forrest, G. F., & Harkema, S. J. (2023) · Neuromodulation Technology at the Neural Interface · doi:10.1016/j.neurom.2023.03.014 · Cited by 47
Woodington, B. J., Jiang, L., Carnicer‐Lombarte, A., Güemes, A., Naegele, T. E., Hilton, S., Hadwe, S. E., Trivedi, R. A., Malliaras, G. G., & Barone, D. G. (2024) · Science Advances · doi:10.1126/sciadv.adl1230 · Cited by 49
Posteroanterior cervical transcutaneous spinal stimulation targets ventral and dorsal nerve roots
Wu, Y., Levine, J. M., Wecht, J. R., Maher, M. T., LiMonta, J. M., Saeed, S., Santiago, T. M., Bailey, E., Kastuar, S., Guber, K. S., et al. (2019) · Clinical Neurophysiology · doi:10.1016/j.clinph.2019.11.056 · Cited by 47
“Targeted stimulation of the spinal cord, as demonstrated with lumbar epidural stimulation (Harkema et al. 2011; Angeli et al. 2014, 2018; Gill et al. 2018; Wagner et al. 2018), may recruit endogenous circuitry that leads to re-expression of natural movement synergies (Giszter 2015; Wenger et al.”
Barss, T. S., Parhizi, B., Porter, J., & Mushahwar, V. K. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11030639 · Cited by 45
“Most recently, eSCS applied to the lumbar spinal cord, in conjunction with intensive locomotor training, enabled persons with clinically motor-complete SCI to walk over ground for short distances [4,13,18].”
MethodMultisite Hebbian Plasticity Restores Function in Humans with Spinal Cord Injury
Jo, H. J., Kizziar, E., Sangari, S., Chen, D., Kessler, A., Kim, K., Anschel, A. S., Heinemann, A. W., Mensh, B. D., Awadalla, S., et al. (2023) · Annals of Neurology · doi:10.1002/ana.26622 · Cited by 48
“walking with assistive devices during epidural stimulation with an implanted stimulator after 278 or 113 stimulation sessions combined with exercise training.(5,6) In another study, three participants with incomplete SCI regained voluntary control over previously paralyzed muscles and could walk or cycle in outdoor se…”
MethodCalvert, J. S., Manson, G. A., Grahn, P. J., & Sayenko, D. G. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00454.2019 · Cited by 46
Self-citationMesbah, S., Ball, T., Angeli, C., Rejc, E., Dietz, N. E., Ugiliweneza, B., Harkema, S. J., & Boakye, M. (2020) · Brain · doi:10.1093/brain/awaa423 · Cited by 45
Spinal Cord Injury: Animal Models, Imaging Tools and the Treatment Strategies
Cizkova, D., Murgoci, A., Cubinkova, V., Humeník, F., Mojzisova, Z., Maloveská, M., Čížek, M., Fournier, I., & Salzet, M. (2019) · Neurochemical Research · doi:10.1007/s11064-019-02800-w · Cited by 43
Optimization of Spinal Cord Stimulation Using Bayesian Preference Learning and Its Validation
Zhao, Z., Ahmadi, A., Hoover, C., Grado, L. L., Peterson, N., Wang, X., Freeman, D., Murray, T. A., Lamperski, A., Darrow, D., et al. (2021) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2021.3113636 · Cited by 39
Using a high-frequency carrier does not improve comfort of transcutaneous spinal cord stimulation
Dalrymple, A. N., Hooper, C. A., Kuriakose, M. G., Capogrosso, M., & Weber, D. J. (2022) · Journal of Neural Engineering · doi:10.1088/1741-2552/acabe8 · Cited by 42
Romeni, S., Losanno, E., Emedoli, D., Albano, L., Agnesi, F., Mandelli, C., Barzaghi, L. R., Pompeo, E., Mura, C., Alemanno, F., et al. (2025) · Science Translational Medicine · doi:10.1126/scitranslmed.adp9607 · Cited by 45
Metadata
- Authors
- Gill, M. L., Grahn, P. J., Calvert, J. S., Linde, M. B., Lavrov, I. A., Strommen, J. A., Beck, L. A., Sayenko, D. G., Van Straaten, M. G., Drubach, D. I., Veith, D. D., Thoreson, A. R., Lopez, C., Gerasimenko, Y. P., Edgerton, V. R., Lee, K. H., & Zhao, K. D.
- Affiliations
- Mayo Clinic (US)
- Houston Methodist (US)
- Russian Academy of Sciences (RU)
- University of California, Los Angeles (US)
- Corresponding author
- Lee, Kendall H.
- Zhao, Kristin D.
- ORCID
- Venue
- Nature Medicine
- Published
- 2018-09-24
- Volume
- 24
- Issue
- 11
- Pages
- 1677-1682
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- OpenAlex
- W2892074957
- Cited by
- 574
- References
- 43
- Citations by year
- 2026: 51 · 2025: 63 · 2024: 58 · 2023: 81 · 2022: 87 · 2021: 94 · 2020: 72 · 2019: 50 · 2018: 16
- FWCI
- 44.13
- Type
- journal article
- Language
- en
- Update notices
- correction (2018-10-23)
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Nature
- Topics
- Health Sciences › Medicine › Clinical Neurology › Spinal Cord Injury Research
- Health Sciences › Medicine › Rehabilitation › Stroke Rehabilitation and Recovery
- Physical Sciences › Engineering › Biomedical Engineering › Prosthetics and Rehabilitation Robotics
- Keywords
- spinal cord injury, complete paraplegia, epidural stimulation, multimodal rehabilitation, task-oriented training, body weight support, standing, paraplegia
- MeSH terms
- Adult, Electric Stimulation, Transcutaneous Electric Nerve Stimulation, Electromyography, Humans, Male, Motor Activity, Nerve Net, Paralysis, Paraplegia, Spinal Cord Injuries, Muscle, Skeletal
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