{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,25]],"date-time":"2026-04-25T15:44:56Z","timestamp":1777131896061,"version":"3.51.4"},"reference-count":43,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2025,11,27]],"date-time":"2025-11-27T00:00:00Z","timestamp":1764201600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,12,30]],"date-time":"2025-12-30T00:00:00Z","timestamp":1767052800000},"content-version":"vor","delay-in-days":33,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100000738","name":"Department of Veterans Affairs","doi-asserted-by":"crossref","award":["I21RX003757"],"award-info":[{"award-number":["I21RX003757"]}],"id":[{"id":"10.13039\/100000738","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Functional electrical stimulation (FES) bicycle training is a physical rehabilitation technique used to promote muscle recovery and\/or cardiorespiratory health in persons with lower extremity impairment due to neurologic injury. FES cycling may also increase bone mineral density (BMD) in such populations, although no consensus exists that supports FES-induced skeletal improvement, in-part due to the extended 9\u201312\u2009+\u2009month duration necessary to detect BMD gain in humans and the multitude of FES parameter permutations that require optimization to improve bone strength and\/or reduce fracture risk, which may differ from those needed to improve muscle or cardiovascular fitness. Rodent models have been used in FES studies because musculoskeletal changes are phenotypically like humans but occur over an accelerated time course that permits more rapid identification of potentially efficacious FES parameters. To gain accelerated understanding of FES-cycling in humans, we performed a kinematic analysis of the rat hindlimb with a fixed hip location and variable foot location as the pedal of the bicycle rotated about the crank. Based on this analysis, an FES pattern was developed for the femoral and sciatic nerves to produce forward (clockwise) or reverse (counterclockwise) motion of the crank. These modeled FES patterns were validated in nine experiments that used 743 unique stimulation trials conducted in anesthetized male and female rodents. Such insights represent initial steps to facilitate closed-loop FES control of cycling in rats, which will help to refine rehabilitation strategies to promote bone and muscle recovery in rodent models and ultimately people.<\/jats:p>","DOI":"10.1038\/s41598-025-29285-8","type":"journal-article","created":{"date-parts":[[2025,11,27]],"date-time":"2025-11-27T11:05:55Z","timestamp":1764241555000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Development and validation of a kinematic hindlimb cycling model for rats"],"prefix":"10.1038","volume":"15","author":[{"given":"Hannah M.","family":"Sweatland","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eric","family":"Pettit","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Heet","family":"Patel","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Neeley","family":"de la Mata","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christine F.","family":"Conover","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Emily J.","family":"Griffis","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Joshua F.","family":"Yarrow","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Matthew A.","family":"Schiefer","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Warren E.","family":"Dixon","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2025,11,27]]},"reference":[{"key":"29285_CR1","doi-asserted-by":"crossref","unstructured":"Sutor, T. W., Kura, J., Mattingly, A. J., Otzel, D. M. & Yarrow, J. F. The effects of exercise and Activity-Based physical therapy on bone after spinal cord injury. Int. J. Mol. Sci. 23 (2022).","DOI":"10.3390\/ijms23020608"},{"key":"29285_CR2","doi-asserted-by":"publisher","first-page":"1005","DOI":"10.1007\/s00198-013-2557-5","volume":"25","author":"WB Edwards","year":"2014","unstructured":"Edwards, W. B., Schnitzer, T. J. & Troy, K. L. Bone mineral and stiffness loss at the distal femur and proximal tibia in acute spinal cord injury. Osteoporos. Int. 25, 1005\u20131015 (2014).","journal-title":"Osteoporos. Int."},{"key":"29285_CR3","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1080\/10790268.1997.11719458","volume":"20","author":"JH Frisbie","year":"1997","unstructured":"Frisbie, J. H. Fractures after myelopathy: the risk quantified. J. Spinal Cord Med. 20, 66\u201369 (1997).","journal-title":"J. Spinal Cord Med."},{"key":"29285_CR4","doi-asserted-by":"publisher","first-page":"2261","DOI":"10.1007\/s00198-013-2295-8","volume":"24","author":"LD Carbone","year":"2013","unstructured":"Carbone, L. D. et al. Morbidity following lower extremity fractures in men with spinal cord injury. Osteoporos. Int. 24, 2261\u20132267 (2013).","journal-title":"Osteoporos. Int."},{"key":"29285_CR5","doi-asserted-by":"publisher","unstructured":"Carraro, U. et al. Recovery from muscle weakness by exercise and FES: Lessons from masters, active or sedentary seniors and SCI patients. Aging Clin. Exp. Res. 29, 579\u2013590   (2017). https:\/\/doi.org\/10.1007\/s40520-016-0619-1 (preprint).","DOI":"10.1007\/s40520-016-0619-1"},{"key":"29285_CR6","doi-asserted-by":"publisher","first-page":"Preprintathttps","DOI":"10.3389\/fneur.2020.00607","volume":"11","author":"L Duffell","year":"2020","unstructured":"Duffell, L. & N. de N. Donaldson, D. A comparison of FES and SCS for neuroplastic recovery after SCI: historical perspectives and future directions. Front. Neurol. 11, Preprintathttpsdoiorg103389fneur202000607 (2020).","journal-title":"Front. Neurol."},{"key":"29285_CR7","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1002\/mus.10408","volume":"28","author":"T Marqueste","year":"2003","unstructured":"Marqueste, T., Hug, F., Decherchi, P. & Jammes, Y. Changes in neuromuscular function after training by functional electrical stimulation. Muscle Nerve. 28, 181\u2013188 (2003).","journal-title":"Muscle Nerve"},{"key":"29285_CR8","doi-asserted-by":"publisher","first-page":"282","DOI":"10.2340\/16501977-0321","volume":"41","author":"A Frotzler","year":"2009","unstructured":"Frotzler, A. et al. Effect of detraining on bone and muscle tissue in subjects with chronic spinal cord injury after a period of electrically-stimulated cycling: A small cohort study. J. Rehabil Med. 41, 282\u2013285 (2009).","journal-title":"J. Rehabil Med."},{"key":"29285_CR9","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1016\/j.bone.2008.03.004","volume":"43","author":"A Frotzler","year":"2008","unstructured":"Frotzler, A. et al. High-volume FES-cycling partially reverses bone loss in people with chronic spinal cord injury. Bone 43, 169\u2013176 (2008).","journal-title":"Bone"},{"key":"29285_CR10","doi-asserted-by":"crossref","unstructured":"Mohr, T. et al. Increased Bone Mineral Density After Prolonged Electrically Induced Cycle Training of Paralyzed Limbs in Spinal Cord Injured Man. (1997).","DOI":"10.1007\/s002239900286"},{"key":"29285_CR11","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1097\/00002060-199601000-00008","volume":"75","author":"K BeDell","year":"1669","unstructured":"BeDell, K., Scremin, A., Perell, K. & Kunkel, C. Effects of functional electrical stimulation-induced lower extremity cycling on bone density of spinal cord-injured patients. Am. J. Phys. Med. Rehabil. 75, 29\u201334 (1669).","journal-title":"Am. J. Phys. Med. Rehabil"},{"key":"29285_CR12","doi-asserted-by":"crossref","unstructured":"Johnston, T. E. et al.  Musculoskeletal effects of 2 functional electrical stimulation cycling paradigms conducted at different cadences for people with spinal cord injury: A pilot study.  Arch. Phys. Med. Rehabil. 97, 1413\u20131422 (W.B. Saunders, 2016).","DOI":"10.1016\/j.apmr.2015.11.014"},{"key":"29285_CR13","doi-asserted-by":"publisher","first-page":"412","DOI":"10.1046\/j.1365-2362.2003.01156.x","volume":"33","author":"P Eser","year":"2003","unstructured":"Eser, P. et al. Effect of electrical stimulation-induced cycling on bone mineral density in spinal cord-injured patients. Eur. J. Clin. Invest. 33, 412\u2013419 (2003).","journal-title":"Eur. J. Clin. Invest."},{"key":"29285_CR14","doi-asserted-by":"publisher","first-page":"Preprintathttps","DOI":"10.1038\/s41413-022-00219-8","volume":"10","author":"S Bolamperti","year":"2022","unstructured":"Bolamperti, S., Villa, I. & Rubinacci, A. Bone remodeling: an operational process ensuring survival and bone mechanical competence. Bone Res. 10, Preprintathttpsdoiorg101038s41413\u2013Preprintathttpsdoiorg101038s41022 (2022).","journal-title":"Bone Res."},{"key":"29285_CR15","doi-asserted-by":"publisher","unstructured":"Fraz\u00e3o, M., de Figueiredo, T. & Cipriano, G. G. Should we use the functional electrical stimulation-cycling exercise in clinical practice? Physiological and clinical effects systematic review with meta-analysis. Arch. Phys. Med. Rehabil. 106, 404\u2013423 (2025) (preprint). https:\/\/doi.org\/10.1016\/j.apmr.2024.06.003","DOI":"10.1016\/j.apmr.2024.06.003"},{"key":"29285_CR16","doi-asserted-by":"publisher","first-page":"493","DOI":"10.1210\/endrev\/bnae004","volume":"45","author":"NYY Koh","year":"2024","unstructured":"Koh, N. Y. Y., Miszkiewicz, J. J., Fac, M. L., Wee, N. K. Y. & Sims, N. A. Preclinical rodent models for human bone disease, including a focus on cortical bone. Endocr. Rev. 45, 493\u2013520 (2024).","journal-title":"Endocr. Rev."},{"key":"29285_CR17","doi-asserted-by":"publisher","unstructured":"Sharif-Alhoseini, M. et al. Animal models of spinal cord injury: A systematic review. Spinal Cord 55, 714\u2013721   (2017). https:\/\/doi.org\/10.1038\/sc.2016.187 (preprint).","DOI":"10.1038\/sc.2016.187"},{"key":"29285_CR18","doi-asserted-by":"publisher","first-page":"1288","DOI":"10.1152\/japplphysiol.00444.2021","volume":"131","author":"JF Yarrow","year":"2021","unstructured":"Yarrow, J. F. et al. Bone loss after severe spinal cord injury coincides with reduced bone formation and precedes bone blood flow deficits. J. Appl. Physiol. 131, 1288\u20131299 (2021).","journal-title":"J. Appl. Physiol."},{"key":"29285_CR19","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1007\/s00223-018-0471-8","volume":"104","author":"DM Otzel","year":"2019","unstructured":"Otzel, D. M. et al. Longitudinal examination of bone loss in male rats after moderate\u2013severe contusion spinal cord injury. Calcif Tissue Int. 104, 79\u201391 (2019).","journal-title":"Calcif Tissue Int."},{"key":"29285_CR20","first-page":"255","volume":"14","author":"JF Yarrow","year":"2014","unstructured":"Yarrow, J. F. et al. Bone loss in a new rodent model combining spinal cord injury and cast immobilization. J. Musculoskelet. Neuronal Interact. 14, 255\u2013266 (2014).","journal-title":"J. Musculoskelet. Neuronal Interact."},{"key":"29285_CR21","doi-asserted-by":"publisher","first-page":"643","DOI":"10.1007\/s12975-011-0118-9","volume":"2","author":"LR Morse","year":"2011","unstructured":"Morse, L. R. et al. Severe spinal cord injury causes immediate Multi-cellular dysfunction at the Chondro-Osseous junction. Transl Stroke Res. 2, 643\u2013650 (2011).","journal-title":"Transl Stroke Res."},{"key":"29285_CR22","doi-asserted-by":"publisher","first-page":"1676","DOI":"10.1089\/neu.2011.2037","volume":"29","author":"MJ Voor","year":"2012","unstructured":"Voor, M. J. et al. Bone loss following spinal cord injury in a rat model. J. Neurotrauma. 29, 1676\u20131682 (2012).","journal-title":"J. Neurotrauma"},{"key":"29285_CR23","doi-asserted-by":"crossref","unstructured":"Lin, T. et al. A comprehensive study of long-term skeletal changes after spinal cord injury in adult rats. Bone Res. 3, 15028 (2015).","DOI":"10.1038\/boneres.2015.28"},{"key":"29285_CR24","doi-asserted-by":"crossref","unstructured":"Yarrow, J. F. & Cardozo, C. P. Effects of spinal cord injury and related conditions. In Encyclopedia Bone Biology. 429\u2013448 (2020).","DOI":"10.1016\/B978-0-12-801238-3.11219-X"},{"key":"29285_CR25","doi-asserted-by":"publisher","first-page":"180","DOI":"10.1007\/s00198-003-1529-6","volume":"15","author":"Y Zehnder","year":"2004","unstructured":"Zehnder, Y. et al. Long-term changes in bone metabolism, bone mineral density, quantitative ultrasound parameters, and fracture incidence after spinal cord injury: A cross-sectional observational study in 100 paraplegic men. Osteoporos. Int. 15, 180\u2013189 (2004).","journal-title":"Osteoporos. Int."},{"key":"29285_CR26","first-page":"141","volume":"9","author":"PK Bose","year":"2016","unstructured":"Bose, P. K. & Thompson, F. J. Systems and methods for promoting locomotion and facilitating exercise. U S Patent No. 9, 421,141 (2016).","journal-title":"U S Patent No"},{"key":"29285_CR27","doi-asserted-by":"crossref","unstructured":"Bose, P. K., Hou, J., Parmer, R., Reier, P. J. & Thompson, F. J. Altered patterns of reflex excitability, balance, and locomotion following spinal cord injury and locomotor training. Front. Physiol.  (2012).","DOI":"10.3389\/fphys.2012.00258"},{"key":"29285_CR28","doi-asserted-by":"publisher","first-page":"813","DOI":"10.1249\/MSS.0000000000003101","volume":"55","author":"JF Yarrow","year":"2023","unstructured":"Yarrow, J. F. et al. Passive cycle training promotes bone recovery after spinal cord injury without altering resting-state bone perfusion. Med. Sci. Sports Exerc. 55, 813\u2013823 (2023).","journal-title":"Med. Sci. Sports Exerc."},{"key":"29285_CR29","doi-asserted-by":"publisher","DOI":"10.1152\/japplphysiol.00299.2024","author":"JR Kura","year":"2024","unstructured":"Kura, J. R. et al. Passive bicycle training stimulates epiphyseal bone formation and restores bone integrity independent of locomotor recovery in a rat spinal cord injury model. J. Appl. Physiol. https:\/\/doi.org\/10.1152\/japplphysiol.00299.2024 (2024).","journal-title":"J. Appl. Physiol."},{"key":"29285_CR30","doi-asserted-by":"publisher","first-page":"77","DOI":"10.46292\/sci23-00048","volume":"31","author":"SK Couper","year":"2025","unstructured":"Couper, S. K. & Smith, M. The effects of functional electrical stimulation cycling on muscle spasticity in individuals with spinal cord injury: A systematic review. Top. Spinal Cord Inj Rehabil. 31, 77\u201399 (2025).","journal-title":"Top. Spinal Cord Inj Rehabil"},{"key":"29285_CR31","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1007\/978-981-13-1435-3_26","volume":"1088","author":"M Rabelo","year":"2018","unstructured":"Rabelo, M. et al. Overview of FES-Assisted cycling approaches and their benefits on functional rehabilitation and muscle atrophy. Adv. Exp. Med. Biol. 1088, 561\u2013583 (2018).","journal-title":"Adv. Exp. Med. Biol."},{"key":"29285_CR32","doi-asserted-by":"publisher","first-page":"641","DOI":"10.1016\/S0146-2806(98)80003-0","volume":"23","author":"WT Phillips","year":"1998","unstructured":"Phillips, W. T. et al. Effect of spinal cord injury on the heart and cardiovascular fitness. Curr. Probl. Cardiol. 23, 641\u2013716 (1998).","journal-title":"Curr. Probl. Cardiol."},{"key":"29285_CR33","doi-asserted-by":"publisher","first-page":"1225","DOI":"10.1109\/TASE.2016.2527716","volume":"14","author":"MJ Bellman","year":"2017","unstructured":"Bellman, M. J., Downey, R. J., Parikh, A. & Dixon, W. E. Automatic control of cycling induced by functional electrical stimulation with electric motor assistance. IEEE Trans. Autom. Sci. Eng. 14, 1225\u20131234 (2017).","journal-title":"IEEE Trans. Autom. Sci. Eng."},{"key":"29285_CR34","doi-asserted-by":"crossref","unstructured":"Bellman, M. J. Control of Cycling Induced by Functional Electrical Stimulation: A Switched Systems Theory Approach. (2015).","DOI":"10.1109\/ACC.2014.6859346"},{"key":"29285_CR35","doi-asserted-by":"crossref","unstructured":"Dienes, J. et al. Comprehensive dynamic and kinematic analysis of the rodent hindlimb during over ground walking. Sci. Rep. 12 (2022).","DOI":"10.1038\/s41598-022-20288-3"},{"key":"29285_CR36","doi-asserted-by":"crossref","unstructured":"Duysens, J., Van De Crommert, H. W. A. A., Smits-Engelsman, B. C. M. & Van Der Helm F. C. T. A walking robot called human: Lessons to be learned from neural control of locomotion. J. Biomech. 35 (2002).","DOI":"10.1016\/S0021-9290(01)00187-7"},{"key":"29285_CR37","unstructured":"Crane, C. D. & Duffy, J. Kinematic Analysis of Robot Manipulators (Cambridge University Press, 1998)."},{"key":"29285_CR38","unstructured":"Ids\u00f8, E. S. Development of a Mathematical Model of a Rider-Tricycle System. (2002)."},{"key":"29285_CR39","unstructured":"Carda, S., Cisari, C. & Invernizzi, M. Sarcopenia or muscle modifications in neurologic diseases: A lexical or patophysiological difference? Eur. J. Phys. Rehabil. Med.  (2013). https:\/\/www.researchgate.net\/publication\/236156743."},{"key":"29285_CR40","doi-asserted-by":"publisher","first-page":"119","DOI":"10.14740\/jocmr6070","volume":"17","author":"I Saleh","year":"2025","unstructured":"Saleh, I., Akbar, A., Hasan, H. S., Yulisa, N. D. & Aprilya, D. Clinical characteristics and bone mineral density score in post-stroke neuromuscular deficit. J. Clin. Med. Res. 17, 119\u2013124 (2025).","journal-title":"J. Clin. Med. Res."},{"key":"29285_CR41","doi-asserted-by":"publisher","unstructured":"Barrows, D. & Goldstein, B. Virtual care in the veterans affairs spinal cord injuries and disorders system of care during the COVID-19 National Public Health Emergency. Phys. Med. Rehabil. Clin. N. Am. 32, 207\u2013221   (2021). https:\/\/doi.org\/10.1016\/j.pmr.2021.01.007 (preprint)","DOI":"10.1016\/j.pmr.2021.01.007"},{"key":"29285_CR42","unstructured":"National Spinal Cord Injury Statistical Center. Traumatic Spinal Cord Injury Facts and Figures at a Glance 2025 SCI Data Sheet. (2025)."},{"key":"29285_CR43","doi-asserted-by":"publisher","first-page":"1309","DOI":"10.1002\/jcsm.13476","volume":"15","author":"HJ Kok","year":"2024","unstructured":"Kok, H. J. et al. Transcriptomics reveals transient and dynamic muscle fibrosis and atrophy differences following spinal cord injury in rats. J. Cachexia Sarcopenia Muscle. 15, 1309\u20131323 (2024).","journal-title":"J. Cachexia Sarcopenia Muscle"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-29285-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-29285-8","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-29285-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,25]],"date-time":"2026-04-25T15:10:24Z","timestamp":1777129824000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-29285-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,11,27]]},"references-count":43,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["29285"],"URL":"https:\/\/doi.org\/10.1038\/s41598-025-29285-8","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,11,27]]},"assertion":[{"value":"7 April 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 November 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"27 November 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"45444"}}