{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,28]],"date-time":"2026-02-28T04:30:11Z","timestamp":1772253011493,"version":"3.50.1"},"reference-count":65,"publisher":"MDPI AG","issue":"18","license":[{"start":{"date-parts":[[2021,9,15]],"date-time":"2021-09-15T00:00:00Z","timestamp":1631664000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Sensors"],"abstract":"<jats:p>The extent to which muscle synergies represent the neural control of human behavior remains unknown. Here, we tested whether certain sets of muscle synergies that are fundamentally necessary across behaviors exist. We measured the electromyographic activities of 26 muscles, including bilateral trunk and lower limb muscles, during 24 locomotion, dynamic and static stability tasks, and we extracted the muscle synergies using non-negative matrix factorization. Our results show that 13 muscle synergies that may have unique functional roles accounted for almost all 24 tasks by combinations of single and\/or merging of synergies. Therefore, our results may support the notion of the low dimensionality in motor outputs, in which the central nervous system flexibly recruits fundamental muscle synergies to execute diverse human behaviors. Further studies are required to validate the neural representation of the fundamental components of muscle synergies.<\/jats:p>","DOI":"10.3390\/s21186186","type":"journal-article","created":{"date-parts":[[2021,9,15]],"date-time":"2021-09-15T12:00:44Z","timestamp":1631707244000},"page":"6186","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":26,"title":["Flexible Recruitments of Fundamental Muscle Synergies in the Trunk and Lower Limbs for Highly Variable Movements and Postures"],"prefix":"10.3390","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6790-1549","authenticated-orcid":false,"given":"Hiroki","family":"Saito","sequence":"first","affiliation":[{"name":"Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro, Tokyo 153-8902, Japan"},{"name":"Department of Physical Therapy, Tokyo University of Technology, Ota, Tokyo 144-8535, Japan"}]},{"given":"Hikaru","family":"Yokoyama","sequence":"additional","affiliation":[{"name":"Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro, Tokyo 153-8902, Japan"}]},{"given":"Atsushi","family":"Sasaki","sequence":"additional","affiliation":[{"name":"Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro, Tokyo 153-8902, Japan"},{"name":"Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda, Tokyo 102-0083, Japan"}]},{"given":"Tatsuya","family":"Kato","sequence":"additional","affiliation":[{"name":"Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro, Tokyo 153-8902, Japan"},{"name":"Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda, Tokyo 102-0083, Japan"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5483-8659","authenticated-orcid":false,"given":"Kimitaka","family":"Nakazawa","sequence":"additional","affiliation":[{"name":"Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro, Tokyo 153-8902, Japan"}]}],"member":"1968","published-online":{"date-parts":[[2021,9,15]]},"reference":[{"key":"ref_1","unstructured":"Bernstein, N.A. (1967). The Co-Ordination and Regulation of Movements, Pergamon Press."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/j.brainresrev.2007.08.004","article-title":"Combining modules for movement","volume":"57","author":"Bizzi","year":"2008","journal-title":"Brain Res. Rev."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1016\/j.conb.2009.09.002","article-title":"The case for and against muscle synergies","volume":"19","author":"Tresch","year":"2009","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Kutch, J.J., and Valero-Cuevas, F.J. (2012). Challenges and New Approaches to Proving the Existence of Muscle Synergies of Neural Origin. PLOS Comput. Biol., 8.","DOI":"10.1371\/journal.pcbi.1002434"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2013","DOI":"10.3389\/fncom.2013.00051","article-title":"The neural origin of muscle synergies","volume":"7","author":"Bizzi","year":"2013","journal-title":"Front. Comput. Neurosci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"77","DOI":"10.3389\/fbioe.2016.00077","article-title":"Muscle Synergies Facilitate Computational Prediction of {Subject-Specific} Walking Motions","volume":"4","author":"Meyer","year":"2016","journal-title":"Front. Bioeng. Biotechnol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"3426","DOI":"10.1152\/jn.00081.2006","article-title":"Motor Patterns in Human Walking and Running","volume":"95","author":"Cappellini","year":"2006","journal-title":"J. Neurophysiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"36275","DOI":"10.1038\/srep36275","article-title":"Distinct sets of locomotor modules control the speed and modes of human locomotion","volume":"6","author":"Yokoyama","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1113\/jphysiol.2003.057174","article-title":"Five basic muscle activation patterns account for muscle activity during human locomotion","volume":"556","author":"Ivanenko","year":"2004","journal-title":"J. Physiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1231","DOI":"10.3389\/fphys.2019.01231","article-title":"A Comprehensive Spatial Mapping of Muscle Synergies in Highly Variable {Upper-Limb} Movements of Healthy Subjects","volume":"10","author":"Scano","year":"2019","journal-title":"Front. Physiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1433","DOI":"10.1152\/jn.01377.2007","article-title":"Modulation of phasic and tonic muscle synergies with reaching direction and speed","volume":"100","author":"Fernandez","year":"2008","journal-title":"J. Neurophysiol."},{"key":"ref_12","first-page":"980","article-title":"Muscle synergies during incremental rowing {VO2max} test of collegiate rowers and untrained subjects","volume":"56","author":"Shaharudin","year":"2016","journal-title":"J. Sports Med. Phys. Fit."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.jelekin.2016.06.004","article-title":"Muscle synergies during bench press are reliable across days","volume":"30","author":"Kristiansen","year":"2016","journal-title":"J. Electromyogr. Kinesiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1941","DOI":"10.1080\/02640414.2016.1143109","article-title":"Muscle coordination during breaststroke swimming: Comparison between elite swimmers and beginners","volume":"34","author":"Vaz","year":"2016","journal-title":"J. Sports Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"40","DOI":"10.3389\/fnhum.2017.00040","article-title":"Shared and {Task-Specific} Muscle Synergies during Normal Walking and Slipping","volume":"11","author":"Nazifi","year":"2017","journal-title":"Front. Hum. Neurosci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2740","DOI":"10.1038\/s41598-018-21018-4","article-title":"Challenging human locomotion: Stability and modular organisation in unsteady conditions","volume":"8","author":"Santuz","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"12025","DOI":"10.1073\/pnas.1821455116","article-title":"Motor primitives are determined in early development and are then robustly conserved into adulthood","volume":"116","author":"Yang","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"4356","DOI":"10.1038\/s41467-020-18210-4","article-title":"Plasticity of muscle synergies through fractionation and merging during development and training of human runners","volume":"11","author":"Cheung","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"48","DOI":"10.3389\/fncom.2013.00048","article-title":"Common muscle synergies for balance and walking","volume":"7","author":"Chvatal","year":"2013","journal-title":"Front. Comput. Neurosci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2867","DOI":"10.1152\/jn.00029.2015","article-title":"Neuromuscular adjustments of gait associated with unstable conditions","volume":"114","author":"Martino","year":"2015","journal-title":"J. Neurophysiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3076","DOI":"10.1073\/pnas.0500199102","article-title":"Shared and specific muscle synergies in natural motor behaviors","volume":"102","author":"Bizzi","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1152\/jn.00109.2014","article-title":"The flexible recruitment of muscle synergies depends on the required force-generating capability","volume":"112","author":"Hagio","year":"2014","journal-title":"J. Neurophysiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1984","DOI":"10.1152\/jn.00220.2014","article-title":"Shared muscle synergies in human walking and cycling","volume":"112","author":"Barroso","year":"2014","journal-title":"J. Neurophysiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"79","DOI":"10.3389\/fncom.2013.00079","article-title":"A musculoskeletal model of human locomotion driven by a low dimensional set of impulsive excitation primitives","volume":"7","author":"Sartori","year":"2013","journal-title":"Front. Comput. Neurosci."},{"key":"ref_25","unstructured":"David, L., Gallahue, O., Goodway, J.C., and Jacqueline, D. (2011). Understanding Motor Development: Infants, Children, Adolescents, Adults, McGraw-Hill."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"210161","DOI":"10.1098\/rsos.210161","article-title":"Common kinematic synergies of various human locomotor behaviours","volume":"8","author":"Huang","year":"2021","journal-title":"R. Soc. Open Sci."},{"key":"ref_27","first-page":"549","article-title":"Functional movement screening: The use of fundamental movements as an assessment of function\u2014Part 2","volume":"9","author":"Cook","year":"2014","journal-title":"Int. J. Sports Phys. Ther."},{"key":"ref_28","first-page":"396","article-title":"Functional movement screening: The use of fundamental movements as an assessment of function\u2014Part 1","volume":"9","author":"Cook","year":"2014","journal-title":"Int. J. Sports Phys. Ther."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jelekin.2010.08.009","article-title":"Can muscle coordination be precisely studied by surface electromyography?","volume":"21","author":"Hug","year":"2011","journal-title":"J. Electromyogr. Kinesiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jelekin.2018.06.001","article-title":"An automatic, adaptive, information-based algorithm for the extraction of the {sEMG} envelope","volume":"42","author":"Ranaldi","year":"2018","journal-title":"J. Electromyogr. Kinesiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1186\/s12984-019-0616-7","article-title":"Modular motor control of the sound limb in gait of people with trans-femoral amputation","volume":"16","author":"Ranaldi","year":"2019","journal-title":"J. Neuroeng. Rehabil."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"026015","DOI":"10.1088\/1741-2552\/ab7c1a","article-title":"Modulation of muscle synergies for multiple forearm movements under variant force and arm position constraints","volume":"17","author":"Geng","year":"2020","journal-title":"J. Neural Eng."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2199","DOI":"10.1152\/jn.00222.2005","article-title":"Matrix factorization algorithms for the identification of muscle synergies: Evaluation on simulated and experimental data sets","volume":"95","author":"Tresch","year":"2006","journal-title":"J. Neurophysiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"788","DOI":"10.1038\/44565","article-title":"Learning the parts of objects by non-negative matrix factorization","volume":"401","author":"Lee","year":"1999","journal-title":"Nature"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"999","DOI":"10.1152\/jn.00549.2010","article-title":"Common muscle synergies for control of center of mass and force in nonstepping and stepping postural behaviors","volume":"106","author":"Chvatal","year":"2011","journal-title":"J. Neurophysiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1530","DOI":"10.1152\/jn.00810.2005","article-title":"Muscle synergy organization is robust across a variety of postural perturbations","volume":"96","author":"Macpherson","year":"2006","journal-title":"J. Neurophysiol."},{"key":"ref_37","unstructured":"Zar, J.H. (1999). Biostatistical Analysis, Pearson Education."},{"key":"ref_38","first-page":"99","article-title":"Between-subject variability of muscle synergies during a complex motor skill","volume":"6","author":"Hug","year":"2012","journal-title":"Front. Comput. Neurosci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"8391","DOI":"10.1038\/s41598-018-26780-z","article-title":"Deciphering the functional role of spatial and temporal muscle synergies in whole-body movements","volume":"8","author":"Delis","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1111\/1467-9868.00293","article-title":"Estimating the number of clusters in a data set via the gap statistic","volume":"63","author":"Tibshirani","year":"2001","journal-title":"J. R. Stat. Soc. Ser. B Stat. Methodol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"14652","DOI":"10.1073\/pnas.1212056109","article-title":"Muscle synergy patterns as physiological markers of motor cortical damage","volume":"109","author":"Cheung","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"48","DOI":"10.3389\/fnhum.2015.00048","article-title":"Identification of muscle synergies associated with gait transition in humans","volume":"9","author":"Hagio","year":"2015","journal-title":"Front. Hum. Neurosci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"8643","DOI":"10.1073\/pnas.1704328114","article-title":"Neural basis for hand muscle synergies in the primate spinal cord","volume":"114","author":"Takei","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1016\/j.neuron.2012.10.018","article-title":"Microstimulation Activates a Handful of Muscle Synergies","volume":"76","author":"Overduin","year":"2012","journal-title":"Neuron"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1580","DOI":"10.1152\/jn.00625.2019","article-title":"Approaches to Revealing the Neural Basis of Muscle Synergies: A Review and A Critique","volume":"125","author":"Cheung","year":"2021","journal-title":"J. Neurophysiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1093\/ptj\/77.2.132","article-title":"Contraction of the Abdominal Muscles Associated With Movement of the Lower Limb","volume":"77","author":"Hodges","year":"1997","journal-title":"Phys. Ther."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.neuron.2015.02.042","article-title":"Neuromechanical principles underlying movement modularity and their implications for rehabilitation","volume":"86","author":"Ting","year":"2015","journal-title":"Neuron"},{"key":"ref_48","unstructured":"Jacquelin Perry, J.M.B. (2010). Gait Analysis: Normal and Pathological Function, SLACK Incorporated. [2nd ed.]."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1016\/j.brainresrev.2007.08.006","article-title":"Organization of mammalian locomotor rhythm and pattern generation","volume":"57","author":"McCrea","year":"2008","journal-title":"Brain Res. Rev."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Liew, B.X.W., Del Vecchio, A., and Falla, D. (2018). The influence of musculoskeletal pain disorders on muscle synergies\u2014A systematic review. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0206885"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"632","DOI":"10.3389\/fphys.2020.00632","article-title":"Muscle Synergies During Walking in Children With Cerebral Palsy: A Systematic Review","volume":"11","author":"Bekius","year":"2020","journal-title":"Front. Physiol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2836","DOI":"10.1080\/09638288.2019.1578421","article-title":"Lower limb muscle synergies during walking after stroke: A systematic review","volume":"42","author":"Vermeulen","year":"2020","journal-title":"Disabil. Rehabil."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"3934698","DOI":"10.1155\/2018\/3934698","article-title":"Feasibility of muscle synergy outcomes in clinics, robotics, and sports: A systematic review","volume":"2018","author":"Taborri","year":"2018","journal-title":"Appl. Bionics Biomech."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"046061","DOI":"10.1088\/1741-2552\/abe244","article-title":"Functional synergy recruitment index as a reliable biomarker of motor function and recovery in chronic stroke patients","volume":"18","author":"Birbaumer","year":"2021","journal-title":"J. Neural Eng."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12984-019-0614-9","article-title":"Pathway-specific modulatory effects of neuromuscular electrical stimulation during pedaling in chronic stroke survivors","volume":"16","author":"Bao","year":"2019","journal-title":"J. NeuroEng. Rehabil."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1109\/TNSRE.2019.2891004","article-title":"Synergy-Based FES for Post-Stroke Rehabilitation of Upper-Limb Motor Functions","volume":"27","author":"Niu","year":"2019","journal-title":"IEEE Trans. Neural Syst. Rehabil. Eng."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1186\/s12984-020-00662-w","article-title":"Changes in leg cycling muscle synergies after training augmented by functional electrical stimulation in subacute stroke survivors: A pilot study","volume":"17","author":"Ambrosini","year":"2020","journal-title":"J. Neuroeng. Rehabil."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Niu, C., Bao, Y., Zhuang, C., Li, S., Wang, T., Zhang, X., Ma, Y., Xuan, Z., Gu, L., and Lan, N. (2018). Effectiveness of short-term training with a synergy-based FES paradigm on motor function recovery post-stroke. Ann. Phys. Rehabil. Med., 61.","DOI":"10.1016\/j.rehab.2018.05.072"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1093\/ptj\/pzx042","article-title":"Complex Skill Training Transfers to Improved Performance and Control of Simpler Tasks After Stroke","volume":"97","author":"Kantak","year":"2017","journal-title":"Phys. Ther."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"12657","DOI":"10.1038\/s41598-018-31174-2","article-title":"Consistent visuomotor adaptations and generalizations can be achieved through different rotations of robust motor modules","volume":"8","author":"Zych","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"105","DOI":"10.3389\/fncom.2013.00105","article-title":"The number and choice of muscles impact the results of muscle synergy analyses","volume":"7","author":"Steele","year":"2013","journal-title":"Front. Comput. Neurosci."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1235","DOI":"10.1152\/jn.01387.2007","article-title":"Adjustments of motor pattern for load compensation via modulated activations of muscle synergies during natural behaviors","volume":"101","author":"Cheung","year":"2009","journal-title":"J. Neurophysiol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1007\/s00421-021-04604-9","article-title":"How to improve the muscle synergy analysis methodology?","volume":"121","author":"Turpin","year":"2021","journal-title":"Eur. J. Appl. Physiol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1109\/7333.918272","article-title":"Modulation and vectorial summation of the spinalized frog\u2019s hindlimb end-point force produced by intraspinal electrical stimulation of the cord","volume":"9","author":"Lemay","year":"2001","journal-title":"IEEE Trans. Neural Syst. Rehabil. Eng."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"27655","DOI":"10.1073\/pnas.1919253117","article-title":"Forelimb force direction and magnitude independently controlled by spinal modules in the macaque","volume":"117","author":"Yaron","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"}],"container-title":["Sensors"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1424-8220\/21\/18\/6186\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:00:17Z","timestamp":1760166017000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1424-8220\/21\/18\/6186"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,9,15]]},"references-count":65,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2021,9]]}},"alternative-id":["s21186186"],"URL":"https:\/\/doi.org\/10.3390\/s21186186","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2021.08.03.455001","asserted-by":"object"}]},"ISSN":["1424-8220"],"issn-type":[{"value":"1424-8220","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,15]]}}}