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A Computational Model for Epidural Electrical Stimulation of Spinal Sensorimotor Circuits
Open accessAbstract
Epidural electrical stimulation (EES) of lumbosacral segments can restore a range of movements after spinal cord injury. However, the mechanisms and neural structures through which EES facilitates movement execution remain unclear. Here, we designed a computational model and performed in vivo experiments to investigate the type of fibers, neurons, and circuits recruited in response to EES. We first developed a realistic finite element computer model of rat lumbosacral segments to identify the currents generated by EES. To evaluate the impact of these currents on sensorimotor circuits, we coupled this model with an anatomically realistic axon-cable model of motoneurons, interneurons, and myelinated afferent fibers for antagonistic ankle muscles. Comparisons between computer simulations and experiments revealed the ability of the model to predict EES-evoked motor responses over multiple intensities and locations. Analysis of the recruited neural structures revealed the lack of direct influence of EES on motoneurons and interneurons. Simulations and pharmacological experiments demonstrated that EES engages spinal circuits trans-synaptically through the recruitment of myelinated afferent fibers. The model also predicted the capacity of spatially distinct EES to modulate side-specific limb movements and, to a lesser extent, extension versus flexion. These predictions were confirmed during standing and walking enabled by EES in spinal rats. These combined results provide a mechanistic framework for the design of spinal neuroprosthetic systems to improve standing and walking after neurological disorders.
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“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 [9]
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“In turn, optimized configurations of anodes and cathodes can steer electric fields towards specific subsets of dorsal root entry zones to modulate well-defined ensembles of motor neuron pools5,9,25.”
From Walking naturally after spinal cord injury using a brain–spine interface (2023) · cites this paper as [9]
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“Epidural electrical stimulation of the spinal cord can modulate specific ensembles of motor pools through the recruitment of the dorsal root entry zones projecting to the spinal cord regions wherein these motor pools reside9,25.”
From Walking naturally after spinal cord injury using a brain–spine interface (2023) · cites this paper as [9]
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“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 [37]
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“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 [37]
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“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 [37]
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A Virtual Inner Ear Model Selects Ramped Pulse Shapes for Vestibular Afferent Stimulation
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Towards a high efficiency implantable electric simulator for programmable biomedical stimulations
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BackgroundTheoretical model of external spinal cord stimulation
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High-density spinal cord stimulation selectively activates lower urinary tract afferentsPreprint
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“…or adjacent to the spine to activate primary afferent neurons in the spinal roots, particularly the large diameter afferent fibers, similar to SCS (Capogrosso et al., 2013; Hofstoetter et al., 2018). tSCS is a more accessible neuromodulation therapy that could potentially reach people without…”
BackgroundSelf-citationSpIC3D imaging: Spinal In-situ Contrast 3D imagingPreprint
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BackgroundRewiring the Nervous System, Without Wires
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“Firstly, the tissue should not be considered as purely resistive[5-9], as recent indirect[10][11][12] and direct[13] evidence suggests that the extracellular medium consists of non-resistive components.”
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“Studies have shown that parameters such as electrode structure, the position of spinal cord stimulation, frequency and amplitude of stimulation signal are key factors determining the motor output [7-9], and adjusting the frequency, amplitude and pulse width of micro-stimulation signals in the spinal cord can change th…”
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Cervical Epidural Electrical Stimulation Restores Voluntary Arm Control In Paralyzed MonkeysPreprint
Capogrosso, M., Barra, B., Conti, S., Perich, M. G., Zhuang, K., Schiavone, G., Fallegger, F., Galan, K., James, N. D., Barraud, Q., et al. (2020) · doi:10.21203/rs.3.rs-123709/v1
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Optimizing Neuroprosthetic Therapies via Autonomous Learning AgentsPreprint
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Stimulation of the Spinal Cord of Decerebrated Rat with Double Pulses
Lyakhovetskii, V. A., Shkorbatova, P. Y., Gorsky, O. V., Pavlova, N. V., Bazhenova, E. Y., Евгеньевич, М. П., & Merkulyeva, N. S. (2024) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093024020054
“Significant selectivity in the sensory compo(cid:2) nents of TA and GM responses was shown only during ES of the L2 segment in acute experiments on narcotized rats [16].”
InfluentialRen, Z., Wang, J., Guo, L., Ye, X., Xu, C., & Ma, Y. (2024) · Research Square · doi:10.21203/rs.3.rs-4490905/v1
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A NEW POSTURAL MOTOR RESPONSE TO SPINAL CORD STIMULATION: POST-STIMULATION REBOUND EXTENSIONPreprint
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“However, stimulation effectiveness was location-dependent as it undoubtedly recruits sensory axons in the vicinity of the stimulation electrode (Capogrosso et al., 2013).”
BackgroundCovert actions of epidural stimulation on spinal locomotor circuitsPreprint
Garcia-Ramirez, D. L., McGrath, J. R., Ha, N. T., Wheel, J. H., Atoche, S. J., Yao, L., Stachowski, N. J., Giszter, S. F., & Dougherty, K. J. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.06.18.599598
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“Another explanation for the linearity observed here is that muscle and spinal stimulation might have recruited non-overlapping neural substrates.”
BackgroundResultStimulation of the spinal cord of decerebrated rat with double pulses
Lyakhovetskii, V. A., Shkorbatova, P. Y., Gorsky, O. V., Pavlova, N. V., Bazhenova, E. Y., Евгеньевич, М. П., & Merkulyeva, N. S. (2024) · Журнал эволюционной биохимии и физиологии · doi:10.31857/s0044452924020051
Riera, C. M., de Oliveira, D. S., Borutta, M. C., Regensburger, M., Zhao, Y., Brenner, S., Vecchio, A. D., & Kinfe, T. M. (2024) · Pain and Therapy · doi:10.1007/s40122-024-00670-x
Metadata
- Authors
- Capogrosso, M., Wenger, N., Raspopovic, S., Musienko, P., Beauparlant, J., Bassi Luciani, L., Courtine, G., & Micera, S.
- Affiliations
- Scuola Superiore Sant'Anna (IT)
- École Polytechnique Fédérale de Lausanne (CH)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2013-12-04
- Volume
- 33
- Issue
- 49
- Pages
- 19326-19340
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6618777
- OpenAlex
- W2127033470
- Cited by
- 435
- References
- 62
- Citations by year
- 2026: 36 · 2025: 56 · 2024: 45 · 2023: 44 · 2022: 47 · 2021: 57 · 2020: 40 · 2019: 24 · 2018: 28 · 2017: 20 · 2016: 13 · 2015: 16 · 2014: 9
- FWCI
- 9.47
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (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
- European Commission (258654)
- École Polytechnique Fédérale de Lausanne
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- FP7 Ideas: European Research Council (261247)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Spinal Cord Injury Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neural Engineering
- Health Sciences › Medicine › Anesthesiology and Pain Medicine › Pain Management and Treatment
- Keywords
- epidural stimulation, spinal cord injury, lumbosacral spinal cord, sensorimotor circuits, motor neurons, interneurons, ankle muscles, standing and walking, rat model
- MeSH terms
- Algorithms, Animals, Computer Simulation, Electric Stimulation, Electrodes, Implanted, Epidural Space, Female, Interneurons, Models, Neurological, Motor Neurons, Nerve Fibers, Rats, Inbred Lew, Sensory Receptor Cells, Recruitment, Neurophysiological, Spinal Cord, Walking, Finite Element Analysis, Rats, Electrophysiological Phenomena
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