Activity-dependent spinal cord neuromodulation rapidly restores trunk and leg motor functions after complete paralysis

Article Article scientifique Article Activity-dependent spinal cord neuromodulation rapidly restores trunk and leg motor functions after complete paralysis eng 2022-02-07 2022-02-07 author Rowald Andreas author Komi Salif author Demesmaeker Robin 0000-0003-0856-0929 author Baaklini Edeny 0000-0003-0942-0768 935767 author Hernandez-Charpak Sergio Daniel 0000-0003-0477-8138 author Paoles Edoardo author Montanaro Hazael 0000-0002-5373-1646 author Cassara Antonino author Becce Fabio 0000-0001-8444-8504 author Lloyd Bryn author Newton Taylor author Ravier Jimmy author Kinany Nawal 873306 Département de radiologie et informatique médicale (RADIO) author D’Ercole Marina author Paley Aurélie author Hankov Nicolas author Varescon Camille author McCracken Laura author Vat Molywan author Caban Miroslav author Watrin Anne author Jacquet Charlotte author Bole-Feysot Léa author Harte Cathal author Lorach Henri author Galvez Andrea author Tschopp Manon author Herrmann Natacha author Wacker Moïra author Geernaert Lionel author Fodor Isabelle author Radevich Valentin author Van Den Keybus Katrien author Eberle Grégoire author Pralong Etienne author Roulet Maxime author Ledoux Jean-Baptiste author Fornari Eleonora author Mandija Stefano 0000-0002-4612-5509 author Mattera Loan 974895 author Martuzzi Roberto 0000-0003-3811-0961 909644 author Nazarian Bruno author Benkler Stefan author Callegari Simone 0000-0001-7598-1809 author Greiner Nathan author Fuhrer Benjamin 0000-0001-7626-3876 author Froeling Martijn 0000-0003-3841-0497 author Buse Nik author Denison Tim author Buschman Rik author Wende Christian author Ganty Damien author Bakker Jurriaan author Delattre Vincent author Lambert Hendrik author Minassian Karen 0000-0003-4197-6141 author van den Berg Cornelis A. T. author Kavounoudias Anne 0000-0002-2712-8739 author Micera Silvestro 0000-0003-4396-8217 author Van De Ville Dimitri 0000-0002-2879-3861 638484 Département de radiologie et informatique médicale (RADIO) author Barraud Quentin 0000-0003-0894-1959 author Kurt Erkan author Kuster Niels author Neufeld Esra 0000-0001-5528-6147 author Capogrosso Marco author Asboth Leonie 0000-0003-2414-9574 author Wagner Fabien B. 0000-0002-9582-6109 author Bloch Jocelyne 0000-0002-6405-1590 author Courtine Grégoire 0000-0002-5744-4142 260-271 10.1038/s41591-021-01663-5 35132264 1078-8956 https://www.nature.com/articles/s41591-021-01663-5 Epidural electrical stimulation (EES) targeting the dorsal roots of lumbosacral segments restores walking in people with spinal cord injury (SCI). However, EES is delivered with multielectrode paddle leads that were originally designed to target the dorsal column of the spinal cord. Here, we hypothesized that an arrangement of electrodes targeting the ensemble of dorsal roots involved in leg and trunk movements would result in superior efficacy, restoring more diverse motor activities after the most severe SCI. To test this hypothesis, we established a computational framework that informed the optimal arrangement of electrodes on a new paddle lead and guided its neurosurgical positioning. We also developed software supporting the rapid configuration of activity-specific stimulation programs that reproduced the natural activation of motor neurons underlying each activity. We tested these neurotechnologies in three individuals with complete sensorimotor paralysis as part of an ongoing clinical trial ( www.clinicaltrials.gov identifier <a href="http://clinicaltrials.gov/show/NCT02936453" rel="noopener noreferrer" target="_blank">NCT02936453</a>). Within a single day, activity-specific stimulation programs enabled these three individuals to stand, walk, cycle, swim and control trunk movements. Neurorehabilitation mediated sufficient improvement to restore these activities in community settings, opening a realistic path to support everyday mobility with EES in people with SCI. Humans Leg Paralysis / rehabilitation Spinal Cord / physiology Spinal Cord Injuries / rehabilitation Spinal Cord Stimulation Walking / physiology Dewey 616.0757 European Commission Human Brain Project Specific Grant Agreement 2 785907 HBP SGA2 EU H2020 European Commission Mechanisms of recovery after severe spinal cord injury 682999 HOW2WALKAGAIN EU H2020 European Commission Experienced Researchers Incoming Fellowship Programme at the Ecole Polytechnique Fédérale de Lausanne 665667 EPFL Fellows EU H2020 62 Département de radiologie et informatique médicale 227 false 552 Traitement d'images médicales 893 https://doi.org/10.5281/zenodo.5614586 https://static-content.springer.com/esm/art%3A10.1038%2Fs41591-021-01663-5/MediaObjects/41591_2021_1663_MOESM3_ESM.mp4 https://static-content.springer.com/esm/art%3A10.1038%2Fs41591-021-01663-5/MediaObjects/41591_2021_1663_MOESM4_ESM.mp4 https://static-content.springer.com/esm/art%3A10.1038%2Fs41591-021-01663-5/MediaObjects/41591_2021_1663_MOESM5_ESM.mp4 https://static-content.springer.com/esm/art%3A10.1038%2Fs41591-021-01663-5/MediaObjects/41591_2021_1663_MOESM6_ESM.mp4 Nature medicine 28 2 03589961-754d-424b-b9b6-13625ad3c599 Article (Published version) Restricted Article-scientifique-from-crossref.pdf 28922395 application/pdf e1a269ef66610a8338c4fac08eab823108740234073c46a1f74bed82752cedb8 534e5b7d-5226-4de3-87fe-9520a88fb3da Article (Accepted version) Public Rowald_et_al_2022_Activity_dependen.pdf 24413838 application/pdf Restricted 2022-08-08 4dd4b70296cd6eabd8b7aee31d7074efe84e44b9d19ba37a60fd682f981f201a 2b6a71dc-c1ff-49d2-a48b-685d5650c36c Appendix Restricted 41591_2021_1663_MOESM1_ESM.pdf 2893351 application/pdf Supplementary Figures 1 and 2, Table 1 and methods. 6f59e31532cd94c24a076de7ee189311733ecbdd8c3bef9a846435afeccf463e 76164774-6fee-4b10-9835-0d8314182a5e Appendix Restricted 41591_2021_1663_MOESM2_ESM.pdf 3140220 application/pdf Reporting Summary d674c5c817c6a83dcd3b00d8a0b0c9d4e1afabd71ea9569a69d3183acd26e1b7 333c8207-518b-4c09-aa2e-44ba41ec9779 Supplemental data Restricted 41591_2021_1663_MOESM7_ESM.xlsx 44895 application/vnd.openxmlformats-officedocument.spreadsheetml.sheet Source Data Fig. 1: Spinal cord segment length and width (b), and raw recruitment curves data (g). f25f904cb02bf1736e5dc7fb8ec586293a305cd4426c4d6e069cb5e8f850f887 a3f5e6c6-21f9-49da-9dcd-c17d95b7b1f5 Supplemental data Restricted 41591_2021_1663_MOESM8_ESM.rtf 2561 application/rtf Source Data Fig. 2 : Text file with link to repository of computational spinal cord models. 647915da7b5f8f4aa3c52855c481ee0b98381ab96313370f52352a5cfa273d71 1b0136b0-3dc8-44b3-82cf-bbc2a50576d8 Supplemental data Restricted 41591_2021_1663_MOESM9_ESM.xlsx 10787 application/vnd.openxmlformats-officedocument.spreadsheetml.sheet Source Data Fig. 3 : Statistical source data. 916f32cd3a81fca325012de05242058eef8b1fe27421d35a74ce2ad3be7d493f 916c7e7c-eb32-4db1-a561-11c8cb28ac7f Supplemental data Restricted 41591_2021_1663_MOESM10_ESM.mat 51206 application/octet-stream Source Data Fig. 5b : Motor responses to trunk stimulation (Fig. 5b). baa34b77f9bfda40a8ac64c70af60015d9a27d51946c997b6a53158d727c2f4c 4f8e96b4-62f3-4a4f-ba70-1dfc8a0bf370 Supplemental data Restricted 41591_2021_1663_MOESM11_ESM.xlsx 40760 application/vnd.openxmlformats-officedocument.spreadsheetml.sheet Source Data Fig. 6 : Statistical source data. aeb70038f4a6e379bf78b2412d6570365ae76942957f82f9bf21f1a4702a0dfd openAccess Faculté de médecine / Section de médecine clinique / Département de radiologie et informatique médicale

Title	Published in	Year	Views	Downloads

Electrical spinal cord stimulation protocols to restore trunk and respiratory functions after spinal cord injury		2023	426	0
Activity-dependent spinal cord neuromodulation rapidly restores trunk and leg motor functions after complete paralysis	Nature medicine	2022	269	2,384

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