Electrical spinal cord stimulation must preserve proprioception to enable locomotion in humans with spinal cord injury
Open accessAbstract
Epidural electrical stimulation (EES) of the spinal cord restores locomotion in animal models of spinal cord injury but is less effective in humans. Here we hypothesized that this interspecies discrepancy is due to interference between EES and proprioceptive information in humans. Computational simulations and preclinical and clinical experiments reveal that EES blocks a significant amount of proprioceptive input in humans, but not in rats. This transient deafferentation prevents modulation of reciprocal inhibitory networks involved in locomotion and reduces or abolishes the conscious perception of leg position. Consequently, continuous EES can only facilitate locomotion within a narrow range of stimulation parameters and is unable to provide meaningful locomotor improvements in humans without rehabilitation. Simulations showed that burst stimulation and spatiotemporal stimulation profiles mitigate the cancellation of proprioceptive information, enabling robust control over motor neuron activity. This demonstrates the importance of stimulation protocols that preserve proprioceptive information to facilitate walking with EES.
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EES is known to enable walking through the recruitment of large-diameter afferents.
“EES is known to enable walking through the recruitment of large-diameter afferents37,38.”
From The neurons that restore walking after paralysis (2022) · cites this paper as [38]
A validated finite element model of epidural electrical stimulation of the lumbar spinal cord was used to estimate the proportion of afferent and efferent fibres recruited at a given stimulation amplitude.
“A validated finite element model of EES of the lumbar spinal cord37,38 was used to estimate the proportion of afferent and efferent fibres recruited at a given stimulation amplitude.”
From The neurons that restore walking after paralysis (2022) · cites this paper as [38]
Computer simulations were performed on a previously validated spiking neural network model reproducing proprioceptive feedback circuits associated with a pair of antagonist muscles in the lumbar spinal cord of rodents.
“We performed computer simulations on a previously validated spiking neural network model37,38, reproducing the proprioceptive feedback circuits associated with a pair of antagonist muscles in the lumbar spinal cord of rodents.”
From The neurons that restore walking after paralysis (2022) · cites this paper as [38]
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- Authors
- Formento, E., Minassian, K., Wagner, F., Mignardot, J. B., Le Goff-Mignardot, C. G., Rowald, A., Bloch, J., Micera, S., Capogrosso, M., & Courtine, G.
- Affiliations
- École Polytechnique Fédérale de Lausanne (CH)
- University of Fribourg (CH)
- Centre Hospitalier Universitaire Vaudois (CH)
- Scuola Superiore Sant'Anna (IT)
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2018-10-31
- Volume
- 21
- Issue
- 12
- Pages
- 1728-1741
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC6268129
- OpenAlex
- W2898777639
- Cited by
- 370
- References
- 72
- Citations by year
- 2026: 43 · 2025: 46 · 2024: 44 · 2023: 42 · 2022: 55 · 2021: 66 · 2020: 36 · 2019: 29 · 2018: 9
- FWCI
- 26.47
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- SERVAL (Université de Lausanne) (acceptedVersion, other-oa)
- IRIS (submittedVersion)
- HAL (submittedVersion)
- RERO DOC (Universität Bern) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- CINECA IRIS Institutional Research Information System (Sant'Anna School of Advanced Studies) (submittedVersion)
- Funders
- National Science Foundation (720270, 785907)
- European Commission (ERC-2015-CoG, 25761, 682999, 720270, HORIZON2020, 785907)
- École Polytechnique Fédérale de Lausanne
- International Foundation for Research in Paraplegia
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (720270, 25761)
- Innosuisse - Schweizerische Agentur für Innovationsförderung
- Horizon 2020 Framework Programme (720270, 785907)
- Eurostars
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Spinal Cord Injury Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neural Engineering
- Health Sciences › Medicine › Rehabilitation › Stroke Rehabilitation and Recovery
- Keywords
- epidural stimulation, spinal cord injury, proprioception, locomotion, deafferentation, reciprocal inhibition, burst stimulation, motor neuron activity, species differences, rat model, computer simulation
- MeSH terms
- Animals, Biomechanical Phenomena, Computer Simulation, Female, Humans, Locomotion, Models, Biological, Proprioception, Spinal Cord, Spinal Cord Injuries, Walking, Muscle, Skeletal, Feedback, Physiological, Rats, Spinal Cord Stimulation
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