{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T00:07:54Z","timestamp":1785283674997,"version":"3.55.0"},"reference-count":58,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,3,1]],"date-time":"2023-03-01T00:00:00Z","timestamp":1677628800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100020959","name":"JST-Mirai Program","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100020959","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Bioeng. Biotechnol."],"abstract":"<jats:p>Adaptive locomotion is an essential behavior for animals to survive. The central pattern generator in the spinal cord is responsible for the basic rhythm of locomotion through sensory feedback coordination, resulting in energy-efficient locomotor patterns. Individuals with symmetrical body proportions exhibit an energy-efficient symmetrical gait on flat ground. In contrast, individuals with lower limb amputation, who have morphologically asymmetrical body proportions, exhibit asymmetrical gait patterns. However, it remains unclear how the nervous system adjusts the control of the lower limbs. Thus, in this study, we investigated how individuals with unilateral transtibial amputation control their left and right lower limbs during locomotion using a two-dimensional neuromusculoskeletal model. The model included a musculoskeletal model with 7 segments and 18 muscles, as well as a neural model with a central pattern generator and sensory feedback systems. Specifically, we examined whether individuals with unilateral transtibial amputation acquire prosthetic gait through a symmetric or asymmetric feedback control for the left and right lower limbs. After acquiring locomotion, the metabolic costs of transport and the symmetry of the spatiotemporal gait factors were evaluated. Regarding the metabolic costs of transportation, the symmetric control model showed values approximately twice those of the asymmetric control model, whereas both scenarios showed asymmetry of spatiotemporal gait patterns. Our results suggest that individuals with unilateral transtibial amputation can reacquire locomotion by modifying sensory feedback parameters. In particular, the model reacquired reasonable locomotion for activities of daily living by re-searching asymmetric feedback parameters for each lower limb. These results could provide insight into effective gait assessment and rehabilitation methods to reacquire locomotion in individuals with unilateral transtibial amputation.<\/jats:p>","DOI":"10.3389\/fbioe.2023.1130353","type":"journal-article","created":{"date-parts":[[2023,3,1]],"date-time":"2023-03-01T05:33:23Z","timestamp":1677648803000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":4,"title":["Acquisition of bipedal locomotion in a neuromusculoskeletal model with unilateral transtibial amputation"],"prefix":"10.3389","volume":"11","author":[{"given":"Daisuke","family":"Ichimura","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hiroaki","family":"Hobara","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Genki","family":"Hisano","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tsubasa","family":"Maruyama","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mitsunori","family":"Tada","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,3,1]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"4793","DOI":"10.1038\/s41598-021-84357-9","article-title":"Inter-limb weight transfer strategy during walking after unilateral transfemoral amputation","volume":"11","author":"Amma","year":"2021","journal-title":"Sci. Rep."},{"key":"B2","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1007\/s00422-010-0373-y","article-title":"Evaluating functional roles of phase resetting in generation of adaptive human bipedal walking with a physiologically based model of the spinal pattern generator","volume":"102","author":"Aoi","year":"2010","journal-title":"Biol. Cybern."},{"key":"B3","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1038\/s41598-018-37460-3","article-title":"Neuromusculoskeletal model that walks and runs across a speed range with a few motor control parameter changes based on the muscle synergy hypothesis","volume":"9","author":"Aoi","year":"2019","journal-title":"Sci. Rep."},{"key":"B4","doi-asserted-by":"publisher","first-page":"e43587","DOI":"10.7554\/eLife.43587","article-title":"Computational modeling of brainstem circuits controlling locomotor frequency and gait","volume":"8","author":"Ausborn","year":"2019","journal-title":"Elife"},{"key":"B5","doi-asserted-by":"publisher","first-page":"1245","DOI":"10.1523\/JNEUROSCI.3834-03.2004","article-title":"Efficacy of rehabilitative experience declines with time after focal ischemic brain injury","volume":"24","author":"Biernaskie","year":"2004","journal-title":"J. Neurosci."},{"key":"B6","doi-asserted-by":"publisher","first-page":"464","DOI":"10.1016\/j.gaitpost.2010.07.002","article-title":"Gait symmetry improves in childhood\u2014A 4-year follow-up of foot loading data","volume":"32","author":"Bosch","year":"2010","journal-title":"Gait Posture"},{"key":"B7","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1016\/j.gaitpost.2010.08.009","article-title":"A multiple-task gait analysis approach: Kinematic, kinetic and EMG reference data for healthy young and adult subjects","volume":"33","author":"Bovi","year":"2011","journal-title":"Gait Posture"},{"key":"B8","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1113\/jphysiol.1914.sp001646","article-title":"On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system","volume":"48","author":"Brown","year":"1914","journal-title":"J. Physiol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"2691","DOI":"10.1113\/JP282609","article-title":"Investigation of neural and biomechanical impairments leading to pathological toe and heel gaits using neuromusculoskeletal modelling","volume":"600","author":"Bruel","year":"2022","journal-title":"J. Physiol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"3443","DOI":"10.1523\/JNEUROSCI.18-09-03443.1998","article-title":"Mechanisms of cortical reorganization in lower-limb amputees","volume":"18","author":"Chen","year":"1998","journal-title":"J. Neurosci."},{"key":"B11","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1016\/j.gaitpost.2019.03.033","article-title":"Hip extension power and abduction power asymmetry as independent predictors of walking speed in individuals with unilateral lower-limb amputation","volume":"70","author":"Crozara","year":"2019","journal-title":"Gait Posture"},{"key":"B12","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1186\/s12984-018-0403-x","article-title":"Reference values for gait temporal and loading symmetry of lower-limb amputees can help in refocusing rehabilitation targets","volume":"15","author":"Cutti","year":"2018","journal-title":"J. Neuroeng. Rehabil."},{"key":"B13","doi-asserted-by":"publisher","first-page":"e0181120","DOI":"10.1371\/journal.pone.0181120","article-title":"Locomotor adaptability in persons with unilateral transtibial amputation","volume":"12","author":"Darter","year":"2017","journal-title":"PLoS One"},{"key":"B14","doi-asserted-by":"publisher","first-page":"9956","DOI":"10.1038\/s41598-019-45602-4","article-title":"The metabolic cost of walking in healthy young and older adults \u2013 a systematic review and meta analysis","volume":"9","author":"Das Gupta","year":"2019","journal-title":"Sci. Rep."},{"key":"B15","doi-asserted-by":"publisher","first-page":"360","DOI":"10.1111\/j.1749-6632.1998.tb09062.x","article-title":"Evidence for a spinal central pattern generator in humansa","volume":"860","author":"Dimitrijevic","year":"1998","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"B16","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1097\/JPO.0b013e3181cca79c","article-title":"K3 PromoterTM prosthetic foot reduces the metabolic cost of walking for unilateral transtibial amputees","volume":"22","author":"Grabowski","year":"2010","journal-title":"J. Prosthet. Orthot."},{"key":"B17","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1016\/0006-8993(75)90401-1","article-title":"How detailed is the central pattern generation for locomotion","volume":"88","author":"Grillner","year":"1975","journal-title":"Brain Res."},{"key":"B18","doi-asserted-by":"publisher","first-page":"1773","DOI":"10.1109\/TNSRE.2018.2858204","article-title":"Energy-optimal human walking with feedback-controlled robotic prostheses: A computational study","volume":"26","author":"Handford","year":"2018","journal-title":"IEEE Trans. Neural Syst. Rehabil. Eng."},{"key":"B19","doi-asserted-by":"publisher","first-page":"19983","DOI":"10.1038\/srep19983","article-title":"Robotic lower limb prosthesis design through simultaneous computer optimizations of human and prosthesis costs","volume":"6","author":"Handford","year":"2016","journal-title":"Sci. Rep."},{"key":"B20","doi-asserted-by":"publisher","first-page":"1040","DOI":"10.1299\/jsmec.45.1040","article-title":"Computer simulation study of human locomotion with a three-dimensional entire-body neuro-musculo-skeletal model. I. Acquisition of normal walking","volume":"45","author":"Hase","year":"2002","journal-title":"JSME Int. J. Ser. C Mech. Syst. Mach. Elem. Manuf."},{"key":"B21","doi-asserted-by":"publisher","first-page":"883","DOI":"10.1016\/j.gaitpost.2013.04.008","article-title":"Stride length-cadence relationship is disrupted in below-knee prosthesis users","volume":"38","author":"Howard","year":"2013","journal-title":"Gait Posture"},{"key":"B22","doi-asserted-by":"publisher","first-page":"250","DOI":"10.1016\/j.gaitpost.2006.04.013","article-title":"Control of lateral balance in walking","volume":"25","author":"Hof","year":"2007","journal-title":"Gait Posture"},{"key":"B23","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1038\/292239a0","article-title":"Gait and the energetics of locomotion in horses","volume":"292","author":"Hoyt","year":"1981","journal-title":"Nature"},{"key":"B24","doi-asserted-by":"publisher","first-page":"e0279593","DOI":"10.1371\/journal.pone.0279593","article-title":"Spatiotemporal gait patterns in individuals with unilateral transfemoral amputation: A hierarchical cluster analysis","volume":"17","author":"Ichimura","year":"2022","journal-title":"PLoS One"},{"key":"B25","doi-asserted-by":"publisher","first-page":"79","DOI":"10.3389\/fnbot.2019.00079","article-title":"A pathological condition affects motor modules in a bipedal locomotion model","volume":"13","author":"Ichimura","year":"2019","journal-title":"Front. Neurorobot."},{"key":"B26","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1007\/s00422-006-0126-0","article-title":"A model of cerebrocerebello-spinomuscular interaction in the sagittal control of human walking","volume":"96","author":"Jo","year":"2007","journal-title":"Biol. Cybern."},{"key":"B27","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1113\/jphysiol.2007.133413","article-title":"Locomotor rhythmogenesis in the isolated rat spinal cord: A phase-coupled set of symmetrical flexion extension oscillators","volume":"583","author":"Juvin","year":"2007","journal-title":"J. Physiol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"464","DOI":"10.1080\/17453674.2020.1756101","article-title":"SwedeAmp-the Swedish amputation and prosthetics registry: 8-year data on 5762 patients with lower limb amputation show sex differences in amputation level and in patient-reported outcome","volume":"91","author":"Kamrad","year":"2020","journal-title":"Acta Orthop."},{"key":"B29","doi-asserted-by":"publisher","first-page":"825149","DOI":"10.3389\/fbioe.2022.825149","article-title":"Contribution of afferent feedback to adaptive hindlimb walking in cats: A neuromusculoskeletal modeling study","volume":"10","author":"Kim","year":"2022","journal-title":"Front. Bioeng. Biotechnol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"e0222037","DOI":"10.1371\/journal.pone.0222037","article-title":"Metabolic cost calculations of gait using musculoskeletal energy models, a comparison study","volume":"14","author":"Koelewijn","year":"2019","journal-title":"PLoS One"},{"key":"B31","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1007\/BF00449593","article-title":"Sustained oscillations generated by mutually inhibiting neurons with adaptation","volume":"52","author":"Matsuoka","year":"1985","journal-title":"Biol. Cybern."},{"key":"B32","doi-asserted-by":"publisher","first-page":"446","DOI":"10.1177\/0309364616683818","article-title":"The effect of a supervised community-based exercise program on balance, balance confidence, and gait in individuals with lower limb amputation","volume":"41","author":"Miller","year":"2017","journal-title":"Prosthet. Orthot. Int."},{"key":"B33","doi-asserted-by":"publisher","first-page":"e11960","DOI":"10.7717\/peerj.11960","article-title":"Transtibial limb loss does not increase metabolic cost in three-dimensional computer simulations of human walking","volume":"9","author":"Miller","year":"2021","journal-title":"PeerJ"},{"key":"B34","doi-asserted-by":"publisher","first-page":"467","DOI":"10.1006\/jtbi.1997.0407","article-title":"A theory of metabolic costs for bipedal gaits","volume":"186","author":"Minetti","year":"1997","journal-title":"J. Theor. Biol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"9107","DOI":"10.1523\/JNEUROSCI.2622-06.2006","article-title":"Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking","volume":"26","author":"Morton","year":"2006","journal-title":"J. Neurosci."},{"key":"B36","doi-asserted-by":"publisher","first-page":"773","DOI":"10.1152\/jn.01001.2007","article-title":"Effects of motor training on the recovery of manual dexterity after primary motor cortex lesion in macaque monkeys","volume":"99","author":"Murata","year":"2008","journal-title":"J. Neurophysiol."},{"key":"B37","doi-asserted-by":"publisher","first-page":"118","DOI":"10.1249\/JES.0000000000000288","article-title":"Brain reorganization and neural plasticity in elite athletes with physical impairments","volume":"50","author":"Nakazawa","year":"2022","journal-title":"Exerc. Sport Sci. Rev."},{"key":"B38","doi-asserted-by":"publisher","first-page":"241","DOI":"10.2340\/16501977-0921","article-title":"A training programme to improve hip strength in persons with lower limb amputation","volume":"44","author":"Nolan","year":"2012","journal-title":"J. Rehabil. Med."},{"key":"B39","doi-asserted-by":"publisher","first-page":"142","DOI":"10.1016\/s0966-6362(02)00066-8","article-title":"Adjustments in gait symmetry with walking speed in trans-femoral and trans-tibial amputees","volume":"17","author":"Nolan","year":"2003","journal-title":"Gait Posture"},{"key":"B40","doi-asserted-by":"publisher","first-page":"487","DOI":"10.1016\/j.apmr.2004.04.034","article-title":"The prevalence of knee pain and symptomatic knee osteoarthritis among veteran traumatic amputees and nonamputees","volume":"86","author":"Norvell","year":"2005","journal-title":"Arch. Phys. Med. Rehabil."},{"key":"B41","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/PL00007977","article-title":"Generation of human bipedal locomotion by a bio-mimetic neuro-musculo-skeletal model","volume":"84","author":"Ogihara","year":"2001","journal-title":"Biol. Cybern."},{"key":"B42","doi-asserted-by":"publisher","first-page":"308","DOI":"10.1038\/s42003-021-01831-w","article-title":"Forward dynamic simulation of Japanese macaque bipedal locomotion demonstrates better energetic economy in a virtualised plantigrade posture","volume":"4","author":"Oku","year":"2021","journal-title":"Commun. Biol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"786","DOI":"10.1016\/0959-4388(95)80107-3","article-title":"Proprioceptive regulation of locomotion","volume":"5","author":"Pearson","year":"1995","journal-title":"Curr. Opin. Neurobiol."},{"key":"B44","volume-title":"Gait analysis: Normal and pathological function","author":"Perry","year":"2010"},{"key":"B45","doi-asserted-by":"publisher","first-page":"3452","DOI":"10.1016\/j.jbiomech.2016.09.015","article-title":"Increasing ankle push-off work with a powered prosthesis does not necessarily reduce metabolic rate for transtibial amputees","volume":"49","author":"Quesada","year":"2016","journal-title":"J. Biomech."},{"key":"B46","doi-asserted-by":"publisher","first-page":"2403","DOI":"10.1152\/jn.00089.2005","article-title":"Interlimb coordination during locomotion: What can be adapted and stored","volume":"94","author":"Reisman","year":"2005","journal-title":"J. Neurophysiol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"830278","DOI":"10.3389\/fspor.2022.830278","article-title":"Gait and neuromuscular changes are evident in some masters club level runners 24-h after interval training run","volume":"4","author":"Riazati","year":"2022","journal-title":"Front. Sports Act. Living"},{"key":"B48","doi-asserted-by":"publisher","first-page":"446","DOI":"10.1016\/j.gaitpost.2011.11.005","article-title":"Evaluating asymmetry in prosthetic gait with step-length asymmetry alone is flawed","volume":"35","author":"Roerdink","year":"2012","journal-title":"Gait Posture"},{"key":"B49","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1152\/physrev.00028.2005","article-title":"Dynamic sensorimotor interactions in locomotion","volume":"86","author":"Rossignol","year":"2006","journal-title":"Physiol. Rev."},{"key":"B50","doi-asserted-by":"publisher","first-page":"e0191310","DOI":"10.1371\/journal.pone.0191310","article-title":"Maintenance of muscle strength retains a normal metabolic cost in simulated walking after transtibial limb loss","volume":"13","author":"Russell Esposito","year":"2018","journal-title":"PLoS One"},{"key":"B51","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1016\/S0966-6362(97)01112-0","article-title":"Lower extremity kinematic and kinetic adaptations in unilateral below-knee amputees during walking","volume":"6","author":"Sanderson","year":"1997","journal-title":"Gait Posture"},{"key":"B52","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1016\/j.gaitpost.2004.01.016","article-title":"Centre of pressure displacements in trans-femoral amputees during gait","volume":"21","author":"Schmid","year":"2005","journal-title":"Gait Posture"},{"key":"B53","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1016\/j.gaitpost.2021.08.027","article-title":"The associations between asymmetries in quadriceps strength and gait in individuals with unilateral transtibial amputation","volume":"90","author":"Sibley","year":"2021","journal-title":"Gait Posture"},{"key":"B54","doi-asserted-by":"publisher","first-page":"3493","DOI":"10.1113\/JP270228","article-title":"A neural circuitry that emphasizes spinal feedback generates diverse behaviours of human locomotion","volume":"593","author":"Song","year":"2015","journal-title":"J. Physiol."},{"key":"B55","doi-asserted-by":"publisher","first-page":"4063","DOI":"10.1113\/JP279195","article-title":"Step time asymmetry but not step length asymmetry is adapted to optimize energy cost of split-belt treadmill walking","volume":"598","author":"Stenum","year":"2020","journal-title":"J. Physiol."},{"key":"B56","doi-asserted-by":"publisher","first-page":"2853","DOI":"10.1152\/jn.00814.2012","article-title":"Effects of early versus late rehabilitative training on manual dexterity after corticospinal tract lesion in macaque monkeys","volume":"109","author":"Sugiyama","year":"2013","journal-title":"J. Neurophysiol."},{"key":"B57","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1007\/BF00198086","article-title":"Self-organized control of bipedal locomotion by neural oscillators in unpredictable environment","volume":"65","author":"Taga","year":"1991","journal-title":"Biol. Cybern."},{"key":"B58","doi-asserted-by":"publisher","first-page":"105632","DOI":"10.1016\/j.clinbiomech.2022.105632","article-title":"Metabolic cost of transport and stance time asymmetry in individuals with unilateral transtibial amputation using a passive prostheses while walking","volume":"94","author":"Wedge","year":"2022","journal-title":"Clin. Biomech. (Bristol, Avon)"}],"container-title":["Frontiers in Bioengineering and Biotechnology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fbioe.2023.1130353\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,3,1]],"date-time":"2023-03-01T05:33:28Z","timestamp":1677648808000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fbioe.2023.1130353\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,1]]},"references-count":58,"alternative-id":["10.3389\/fbioe.2023.1130353"],"URL":"https:\/\/doi.org\/10.3389\/fbioe.2023.1130353","relation":{},"ISSN":["2296-4185"],"issn-type":[{"value":"2296-4185","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,3,1]]},"article-number":"1130353"}}