The DOI matches its Crossref record; 56 of the 56 references it cites were found in a registry or an index.
Mechanisms Underlying the Neuromodulation of Spinal Circuits for Correcting Gait and Balance Deficits after Spinal Cord Injury
Open accessAbstract
Epidural electrical stimulation of lumbar segments facilitates standing and walking in animal models and humans with spinal cord injury. However, the mechanisms through which this neuromodulation therapy engages spinal circuits remain enigmatic. Using computer simulations and behavioral experiments, we provide evidence that epidural electrical stimulation interacts with muscle spindle feedback circuits to modulate muscle activity during locomotion. Hypothesis-driven strategies emerging from simulations steered the design of stimulation protocols that adjust bilateral hindlimb kinematics throughout gait execution. These stimulation strategies corrected subject-specific gait and balance deficits in rats with incomplete and complete spinal cord injury. The conservation of muscle spindle feedback circuits across mammals suggests that the same mechanisms may facilitate motor control in humans. These results provide a conceptual framework to improve stimulation protocols for clinical applications.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“We previously showed that epidural electrical stimulation targeting the individual dorsal root entry zones of the lumbosacral spinal cord enables the modulation of specific leg motor pools9–12.”
From Walking naturally after spinal cord injury using a brain–spine interface (2023) · cites this paper as [12]
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
OpenSim: Open-Source Software to Create and Analyze Dynamic Simulations of Movement
Delp, S. L., Anderson, F. C., Arnold, A. S., Loan, P., Habib, A., John, C. T., Guendelman, E., & Thelen, D. G. (2007) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2007.901024 · Cited by 4,951
The NEURON Simulation Environment
Hines, M. L., & Carnevale, N. T. (1997) · Neural Computation · doi:10.1162/neco.1997.9.6.1179 · Cited by 2,630
Flexion‐reflex of the limb, crossed extension‐reflex, and reflex stepping and standing
Sherrington, C. (1910) · The Journal of Physiology · doi:10.1113/jphysiol.1910.sp001362 · Cited by 1,336
Dynamic Sensorimotor Interactions in Locomotion
Rossignol, S., Dubuc, R., & Gossard, J.-P. (2006) · Physiological Reviews · doi:10.1152/physrev.00028.2005 · Cited by 1,096
Electronic dura mater for long-term multimodal neural interfaces
Minev, I. R., Musienko, P., Hirsch, A., Barraud, Q., Wenger, N., Moraud, E. M., Gandar, J., Capogrosso, M., Milekovic, T., Asboth, L., et al. (2015) · Science · doi:10.1126/science.1260318 · Cited by 1,082
Self-citationInterneuronal relay in spinal pathways from proprioceptors
Jankowska, E. (1992) · Progress in Neurobiology · doi:10.1016/0301-0082(92)90024-9 · Cited by 931
LOCOMOTOR CIRCUITS IN THE MAMMALIAN SPINAL CORD
Kiehn, O. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112910 · Cited by 868
Restoring Voluntary Control of Locomotion after Paralyzing Spinal Cord Injury
van den Brand, R., Heutschi, J., Barraud, Q., DiGiovanna, J., Bartholdi, K., Huerlimann, M., Friedli, L., Vollenweider, I., Moraud, E. M., Duis, S., et al. (2012) · Science · doi:10.1126/science.1217416 · Cited by 767
Self-citationMcIntyre, C. C., Richardson, A. G., & Grill, W. M. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00353.2001 · Cited by 764
Angeli, C. A., Edgerton, V. R., Gerasimenko, Y. P., & Harkema, S. J. (2014) · Brain · doi:10.1093/brain/awu038 · Cited by 750
Transformation of nonfunctional spinal circuits into functional states after the loss of brain input
Courtine, G., Gerasimenko, Y., van den Brand, R., Yew, A., Musienko, P., Zhong, H., Song, B., Ao, Y., Ichiyama, R. M., Lavrov, I., et al. (2009) · Nature Neuroscience · doi:10.1038/nn.2401 · Cited by 706
Self-citationCommon Principles of Motor Control in Vertebrates and Invertebrates
Pearson, K. G. (1993) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.16.030193.001405 · Cited by 567
Neuronal Control of Locomotion 'From Mollusc to Man '
Gn, O., Deliagina, T. G., & Grillner, S. (1999) · Medical Entomology and Zoology · Cited by 453
A Computational Model for Epidural Electrical Stimulation of Spinal Sensorimotor Circuits
Capogrosso, M., Wenger, N., Raspopovic, S., Musienko, P., Beauparlant, J., Bassi Luciani, L., Courtine, G., & Micera, S. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1688-13.2013 · Cited by 435
Self-citationMcIntyre, C. C., & Grill, W. M. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.4.1592 · Cited by 383
Motor Circuits in Action: Specification, Connectivity, and Function
Arber, S. (2012) · Neuron · doi:10.1016/j.neuron.2012.05.011 · Cited by 319
Edgerton, V. R., Courtine, G., Gerasimenko, Y., Lavrov, I. A., Ichiyama, R. M., Fong, A. J., Cai, L. L., Otoshi, C. K., Tillakaratne, N. J. K., Burdick, J. W., et al. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.09.002 · Cited by 316
Self-citationA neural circuitry that emphasizes spinal feedback generates diverse behaviours of human locomotion
Song, S., & Geyer, H. (2015) · The Journal of Physiology · doi:10.1113/jp270228 · Cited by 243
Rattay, F., Minassian, K., & Dimitrijevic, M. (2000) · Spinal Cord · doi:10.1038/sj.sc.3101039 · Cited by 226
Pratt, C. A., & Jordan, L. M. (1987) · Journal of Neurophysiology · doi:10.1152/jn.1987.57.1.56 · Cited by 224
Rybak, I. A., Stecina, K., Shevtsova, N. A., & McCrea, D. A. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.118711 · Cited by 222
Identification of a cellular node for motor control pathways
Levine, A. J., Hinckley, C. A., Hilde, K. L., Driscoll, S. P., Poon, T., Montgomery, J. M., & Pfaff, S. L. (2014) · Nature Neuroscience · doi:10.1038/nn.3675 · Cited by 216
Tapping into spinal circuits to restore motor function
Barbeau, H., McCrea, D. A., O'Donovan, M. J., Rossignol, S., Grill, W. M., & Lemay, M. A. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00008-9 · Cited by 211
Wenger, N., Moraud, E. M., Raspopovic, S., Bonizzato, M., DiGiovanna, J., Musienko, P., Morari, M., Micera, S., & Courtine, G. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3008325 · Cited by 209
Ekeberg, Ö., & Pearson, K. G. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00065.2005 · Cited by 206
Motor antagonism exposed by spatial segregation and timing of neurogenesis
Tripodi, M., Stepien, A. E., & Arber, S. (2011) · Nature · doi:10.1038/nature10538 · Cited by 203
Scott, J. G., & Mendell, L. M. (1976) · Journal of Neurophysiology · doi:10.1152/jn.1976.39.4.679 · Cited by 201
Friedli, L., Rosenzweig, E. S., Barraud, Q., Schubert, M. J. W., Dominici, N., Awai, L., Nielson, J. L., Евгеньевич, М. П., Nout‐Lomas, Y. S., Zhong, H., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aac5811 · Cited by 198
Self-citationThe special nature of human walking and its neural control
Capaday, C. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02173-2 · Cited by 196
Booth, V., Rinzel, J., & Kiehn, O. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.6.3371 · Cited by 192
Locomotor pattern in paraplegic patients: training effects and recovery of spinal cord function
Dietz, V., Wirz, M., Curt, A. E. P., & Colombo, G. (1998) · Spinal Cord · doi:10.1038/sj.sc.3100590 · Cited by 180
Ensemble firing of muscle afferents recorded during normal locomotion in cats
Prochazka, A., & Gorassini, M. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.293bu.x · Cited by 177
Carhart, M. R., He, J., Herman, R. M., D'Luzansky, S., & Willis, W. T. (2004) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2003.822763 · Cited by 177
Human spinal locomotor control is based on flexibly organized burst generators
Danner, S. M., Hofstoetter, U. S., Freundl, B., Binder, H., Mayr, W., Rattay, F., & Minassian, K. (2015) · Brain · doi:10.1093/brain/awu372 · Cited by 175
Models of ensemble firing of muscle spindle afferents recorded during normal locomotion in cats
Procházka, A., & Gorassini, M. A. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.277bu.x · Cited by 172
Borton, D., Micera, S., Millán, J. D. R., & Courtine, G. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005968 · Cited by 171
Self-citationSayenko, D. G., Angeli, C., Harkema, S. J., Edgerton, V. R., & Gerasimenko, Y. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00489.2013 · Cited by 169
Mechanisms and models of spinal cord stimulation for the treatment of neuropathic pain
Zhang, T. C., Janik, J. J., & Grill, W. M. (2014) · Brain Research · doi:10.1016/j.brainres.2014.04.039 · Cited by 163
Spinal cord reflexes induced by epidural spinal cord stimulation in normal awake rats
Gerasimenko, Y., Lavrov, I. A., Courtine, G., Ichiyama, R. M., Dy, C. J., Zhong, H., Roy, R. R., & Edgerton, V. R. (2006) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2006.05.004 · Cited by 162
Self-citationThe role of gravity in human walking: pendular energy exchange, external work and optimal speed
Cavagna, G., Willems, P. A., & Heglund, N. C. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.00657.x · Cited by 151
Harrison, P. J., & Taylor, A. (1981) · The Journal of Physiology · doi:10.1113/jphysiol.1981.sp013638 · Cited by 151
Development of human locomotion
Lacquaniti, F., Ivanenko, Y. P., & Zago, M. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.03.012 · Cited by 118
Central control components of a ‘simple’ stretch reflex
Clarac, F., Cattaert, D., & Ray, D. L. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01535-0 · Cited by 113
Segev, I., Fleshman, J. W., & Burke, R. E. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.64.2.648 · Cited by 109
Talpalar, A. E., Endo, T., Löw, P., Borgius, L., Hägglund, M., Dougherty, K. J., Ryge, J., Hnasko, T. S., & Kiehn, O. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.011 · Cited by 100
A three-dimensional model of the rat hindlimb: Musculoskeletal geometry and muscle moment arms
Johnson, W. L., Jindrich, D. L., Roy, R. R., & Edgerton, V. R. (2007) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2007.10.004 · Cited by 100
Supraspinal control of a short-latency cutaneous pathway to hindlimb motoneurons
Fleshman, J. W., Rudomin, P., & Burke, R. E. (1988) · Experimental Brain Research · doi:10.1007/bf00247299 · Cited by 90
Hofstoetter, U. S., Danner, S. M., Freundl, B., Binder, H., Mayr, W., Rattay, F., & Minassian, K. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00136.2015 · Cited by 75
Quevedo, J. N., Fedirchuk, B., Gosgnach, S., & McCrea, D. A. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.t01-1-00549.x · Cited by 65
Jones, K. E., & Bawa, P. N. S. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.1.405 · Cited by 56
Computational modeling of deep brain stimulation
McIntyre, C. C., & Foutz, T. J. (2013) · Handbook of clinical neurology · doi:10.1016/b978-0-444-53497-2.00005-x · Cited by 54
Analysis of reflex modulation with a biologically realistic neural network
Stienen, A. H. A., Schouten, A. C., Schuurmans, J., & van der Helm, F. C. T. (2007) · Journal of Computational Neuroscience · doi:10.1007/s10827-007-0037-7 · Cited by 53
Properties of single-fiber spindle group II EPSPs in triceps surae motoneurons
Munson, J. B., Fleshman, J. W., & Sypert, G. W. (1980) · Journal of Neurophysiology · doi:10.1152/jn.1980.44.4.713 · Cited by 49
Defining Ecological Strategies in Neuroprosthetics
Courtine, G., & Bloch, J. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.039 · Cited by 31
Self-citationPierrot-Deseilligny, E. (1989) · Progress in brain research · doi:10.1016/s0079-6123(08)62225-6 · Cited by 29
Johnson, W. L., Jindrich, D. L., Zhong, H., Roy, R. R., & Edgerton, V. R. (2011) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2011.2106784 · Cited by 25
Flagged first, then by citations
Cited by
Sorted by citations
Seth, A., Hicks, J. L., Uchida, T. K., Habib, A., Dembia, C. L., Dunne, J. J., Ong, C. F., DeMers, M. S., Rajagopal, A., Millard, M., et al. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006223 · Cited by 1,338
Targeted neurotechnology restores walking in humans with spinal cord injury
Wagner, F. B., Mignardot, J.-B., Le Goff-Mignardot, C. G., Demesmaeker, R., Komi, S., Capogrosso, M., Rowald, A., Seáñez, I., Caban, M., Pirondini, E., et al. (2018) · Nature · doi:10.1038/s41586-018-0649-2 · Cited by 1,087
Self-citationWalking 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
“We previously showed that epidural electrical stimulation targeting the individual dorsal root entry zones of the lumbosacral spinal cord enables the modulation of specific leg motor pools 9–12 .”
BackgroundSelf-citationA 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
Self-citationSpinal cord repair: advances in biology and technology
Courtine, G., & Sofroniew, M. V. (2019) · Nature Medicine · doi:10.1038/s41591-019-0475-6 · Cited by 508
Self-citation
Metadata
- Authors
- Moraud, E. M., Capogrosso, M., Formento, E., Wenger, N., DiGiovanna, J., Courtine, G., & Micera, S.
- Affiliations
- École Polytechnique Fédérale de Lausanne (CH)
- Scuola Superiore Sant'Anna (IT)
- Corresponding author
- Courtine, Grégoire
- Micera, Silvestro
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2016-02
- Volume
- 89
- Issue
- 4
- Pages
- 814-828
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2255557036
- Cited by
- 220
- References
- 56
- Citations by year
- 2026: 19 · 2025: 30 · 2024: 29 · 2023: 18 · 2022: 26 · 2021: 28 · 2020: 21 · 2019: 15 · 2018: 14 · 2017: 12 · 2016: 8
- FWCI
- 14.86
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- CINECA IRIS Institutional Research Information System (Sant'Anna School of Advanced Studies) (submittedVersion)
- Funders
- Fondation Bertarelli
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (269921)
- Berlin Institute of Health
- Topics
- Health Sciences › Medicine › Clinical Neurology › 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, gait rehabilitation, balance deficits, spinal cord circuits, locomotion, hindlimb kinematics, incomplete spinal cord injury, complete spinal cord injury
- MeSH terms
- Analysis of Variance, Animals, Biomechanical Phenomena, Computer Simulation, Electromyography, Electric Stimulation Therapy, Postural Balance, Female, Hindlimb, Locomotion, Models, Neurological, Motor Neurons, Nerve Net, Rats, Inbred Lew, Sensation Disorders, Spinal Cord Injuries, Gait Disorders, Neurologic, Feedback, Physiological, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review