{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,9]],"date-time":"2026-01-09T23:24:38Z","timestamp":1768001078713,"version":"3.49.0"},"reference-count":52,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2021,6,1]],"date-time":"2021-06-01T00:00:00Z","timestamp":1622505600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002858","name":"China Postdoctoral Science Foundation","doi-asserted-by":"publisher","award":["2019M662128"],"award-info":[{"award-number":["2019M662128"]}],"id":[{"id":"10.13039\/501100002858","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007928","name":"Ningbo Science and Technology Bureau","doi-asserted-by":"publisher","award":["2018B10073, 2019B10034, 2019A610089, 2020Z082"],"award-info":[{"award-number":["2018B10073, 2019B10034, 2019A610089, 2020Z082"]}],"id":[{"id":"10.13039\/501100007928","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100008990","name":"Zhejiang Provincial Department of Science and Technology","doi-asserted-by":"publisher","award":["2019C03090,LQ20F030003,LQ19F030002"],"award-info":[{"award-number":["2019C03090,LQ20F030003,LQ19F030002"]}],"id":[{"id":"10.13039\/501100008990","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Sensors"],"abstract":"<jats:p>In this paper, we present a novel muscle synergy extraction method based on multivariate curve resolution\u2013alternating least squares (MCR-ALS) to overcome the limitation of the nonnegative matrix factorization (NMF) method for extracting non-sparse muscle synergy, and we study its potential application for evaluating motor function of stroke survivors. Nonnegative matrix factorization (NMF) is the most widely used method for muscle synergy extraction. However, NMF is susceptible to components\u2019 sparseness and usually provides inferior reliability, which significantly limits the promotion of muscle synergy. In this study, MCR-ALS was employed to extract muscle synergy from electromyography (EMG) data. Its performance was compared with two other matrix factorization algorithms, NMF and self-modeling mixture analysis (SMMA). Simulated data sets were utilized to explore the influences of the sparseness and noise on the extracted synergies. As a result, the synergies estimated by MCR-ALS were the most similar to true synergies as compared with SMMA and NMF. MCR-ALS was used to analyze the muscle synergy characteristics of upper limb movements performed by healthy (n = 11) and stroke (n = 5) subjects. The repeatability and intra-subject consistency were used to evaluate the performance of MCR-ALS. As a result, MCR-ALS provided much higher repeatability and intra-subject consistency as compared with NMF, which were important for the reliability of the motor function evaluation. The stroke subjects had lower intra-subject consistency and seemingly had more synergies as compared with the healthy subjects. Thus, MCR-ALS is a promising muscle synergy analysis method for motor function evaluation of stroke patients.<\/jats:p>","DOI":"10.3390\/s21113833","type":"journal-article","created":{"date-parts":[[2021,6,1]],"date-time":"2021-06-01T23:07:03Z","timestamp":1622588823000},"page":"3833","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["A Novel Muscle Synergy Extraction Method Used for Motor Function Evaluation of Stroke Patients: A Pilot Study"],"prefix":"10.3390","volume":"21","author":[{"given":"Yehao","family":"Ma","sequence":"first","affiliation":[{"name":"Cixi Institute of Biomedical Engineering, Ningbo Institute of Materials Technology and Engineering, Chinese Academy of Sciences, Ningbo 315300, China"},{"name":"Zhejiang Engineering Research Center for Biomedical Materials, Ningbo Institute of Materials Technology and Engineering, Chinese Academy of Sciences, Ningbo 315300, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8879-4794","authenticated-orcid":false,"given":"Changcheng","family":"Shi","sequence":"additional","affiliation":[{"name":"Cixi Institute of Biomedical Engineering, Ningbo Institute of Materials Technology and Engineering, Chinese Academy of Sciences, Ningbo 315300, China"},{"name":"Zhejiang Engineering Research Center for Biomedical Materials, Ningbo Institute of Materials Technology and Engineering, Chinese Academy of Sciences, Ningbo 315300, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jialin","family":"Xu","sequence":"additional","affiliation":[{"name":"Cixi Institute of Biomedical Engineering, Ningbo Institute of Materials Technology and Engineering, Chinese Academy of Sciences, Ningbo 315300, China"},{"name":"Zhejiang Engineering Research Center for Biomedical Materials, Ningbo Institute of Materials Technology and Engineering, Chinese Academy of Sciences, Ningbo 315300, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sijia","family":"Ye","sequence":"additional","affiliation":[{"name":"Cixi Institute of Biomedical Engineering, Ningbo Institute of Materials Technology and Engineering, Chinese Academy of Sciences, Ningbo 315300, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Huilin","family":"Zhou","sequence":"additional","affiliation":[{"name":"Cixi Institute of Biomedical Engineering, Ningbo Institute of Materials Technology and Engineering, Chinese Academy of Sciences, Ningbo 315300, China"},{"name":"Zhejiang Engineering Research Center for Biomedical Materials, Ningbo Institute of Materials Technology and Engineering, Chinese Academy of Sciences, Ningbo 315300, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2499-7397","authenticated-orcid":false,"given":"Guokun","family":"Zuo","sequence":"additional","affiliation":[{"name":"Cixi Institute of Biomedical Engineering, Ningbo Institute of Materials Technology and Engineering, Chinese Academy of Sciences, Ningbo 315300, China"},{"name":"Zhejiang Engineering Research Center for Biomedical Materials, Ningbo Institute of Materials Technology and Engineering, Chinese Academy of Sciences, Ningbo 315300, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,6,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1310\/sci1701-16","article-title":"Muscle synergies: Implications for clinical evaluation and rehabilitation of movement","volume":"17","author":"Safavynia","year":"2011","journal-title":"Top. Spinal Cord Inj. Rehabil."},{"key":"ref_2","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_3","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/S0165-0173(02)00189-3","article-title":"Coordination and localization in spinal motor systems","volume":"39","author":"Tresch","year":"2002","journal-title":"Brain Res. Rev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1050","DOI":"10.3389\/fnins.2018.01050","article-title":"Muscle synergy alteration of human during walking with lower limb exoskeleton","volume":"12","author":"Li","year":"2019","journal-title":"Front. Neurosci."},{"key":"ref_5","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_6","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1152\/jn.00435.2016","article-title":"On identifying kinematic and muscle synergies: A comparison of matrix factorization methods using experimental data from the healthy population","volume":"117","year":"2017","journal-title":"J. Neurophysiol."},{"key":"ref_7","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_8","doi-asserted-by":"crossref","first-page":"57","DOI":"10.3389\/fnbot.2018.00057","article-title":"Muscle synergy analysis of a hand-grasp dataset: A limited subset of motor modules may underlie a large variety of grasps","volume":"12","author":"Scano","year":"2018","journal-title":"Front. Neurorobot."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","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":"ref_10","doi-asserted-by":"crossref","first-page":"69","DOI":"10.3389\/fncom.2018.00069","article-title":"Alterations of muscle synergies during voluntary arm reaching movement in subacute stroke survivors at different levels of impairment","volume":"12","author":"Pan","year":"2018","journal-title":"Front. Comput. Neurosci."},{"key":"ref_11","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. Acad. Natl. Sci. USA"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"844","DOI":"10.1152\/jn.00825.2009","article-title":"Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity poststroke","volume":"103","author":"Clark","year":"2010","journal-title":"J. Neurophysiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"337","DOI":"10.3389\/fneur.2017.00337","article-title":"Evaluation of functional correlation of task-specific muscle synergies with motor performance in patients postsroke","volume":"8","author":"Li","year":"2017","journal-title":"Front. Neurol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1301","DOI":"10.1152\/jn.00038.2013","article-title":"Absence of postural muscle synergies for balance after spinal cord transection","volume":"110","author":"Chvatal","year":"2013","journal-title":"J. Neurophysiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2024","DOI":"10.1016\/j.clinph.2014.02.001","article-title":"Neuromuscular constraints on muscle coordination during overground walking in persons with chronic incomplete spinal cord injury","volume":"125","author":"Hayes","year":"2014","journal-title":"Clin. Neurophysiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"130","DOI":"10.3389\/fnhum.2017.00130","article-title":"Assessment of upper limb motor dysfunction for children with cerebral palsy based on muscle synergy analysis","volume":"11","author":"Tang","year":"2017","journal-title":"Front. Hum. Neurosci."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Mileti, I., Zampogna, A., Santuz, A., Asci, F., Prete, Z.D., Arampatzis, A., Palermo, E., and Suppa, A. (2020). Muscle synergies in Parkinson\u2019s disease. Sensors, 20.","DOI":"10.3390\/s20113209"},{"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":"123","DOI":"10.3233\/THC-161256","article-title":"Muscle synergy extraction during arm reaching movements at different speeds","volume":"25","author":"Sabzevari","year":"2017","journal-title":"Technol. Health Care"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Ghislieri, M., Agostini, V., and Knaflitz, M. (2019, January 23\u201327). How to improve robustness in muscle synergy extraction. Proceedings of the 41st Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Berlin, Germany.","DOI":"10.1109\/EMBC.2019.8856438"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2180","DOI":"10.1152\/jn.00472.2019","article-title":"When 90% of the variance is not enough: Residual EMG from muscle synergy extraction influences task performance","volume":"93","author":"Barradas","year":"2020","journal-title":"J. Neurophysiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1109\/TNSRE.2018.2810859","article-title":"How are muscle synergies affected by electromyography pre-processing?","volume":"26","author":"Kieliba","year":"2018","journal-title":"IEEE Trans. Neural Syst. Rehabilit. Eng."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/j.humov.2014.11.010","article-title":"Coordination among thigh muscles including the vastus intermedius and adductor magnus at different cycling intensities","volume":"40","author":"Saito","year":"2015","journal-title":"Hum. Mov. Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"11255","DOI":"10.1523\/JNEUROSCI.23-35-11255.2003","article-title":"Early skill learning is expressed through selection and tuning of cortically represented muscle synergies","volume":"23","author":"Kargo","year":"2003","journal-title":"J. Neurosci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"52","DOI":"10.3389\/fncom.2013.00052","article-title":"Distinguishing synchronous and time-varying synergies using point process interval statistics: Motor primitives in frog and rat","volume":"7","author":"Hart","year":"2013","journal-title":"Front. Comput. Neurosci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1152\/jn.00681.2004","article-title":"A limited set of muscle synergies for force control during a postural task","volume":"93","author":"Ting","year":"2005","journal-title":"J. Neurophysiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2243","DOI":"10.1007\/s00221-017-4971-y","article-title":"Motor equivalence and structure of variance: Multi-muscle postural synergies in Parkinson\u2019s disease","volume":"235","author":"Falaki","year":"2017","journal-title":"Exp. Brain Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"8266","DOI":"10.1038\/s41598-020-65257-w","article-title":"Non-negative matrix factorisation is the most appropriate method for extraction of muscle synergies in walking and running","volume":"10","author":"Rabbi","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1128","DOI":"10.1162\/NECO_a_00576","article-title":"On nonnegative matrix factorization algorithms for signal-dependent noise with application to electromyography data","volume":"26","author":"Devarajan","year":"2014","journal-title":"Neural Comput."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1750007","DOI":"10.1142\/S0129065717500071","article-title":"On the methodological implications of extracting muscle synergies from human locomotion","volume":"27","author":"Santuz","year":"2017","journal-title":"Int. J. Neural Syst."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"3629347","DOI":"10.1155\/2018\/3629347","article-title":"Comparison of initialization techniques for the accurate extraction of muscle synergies from myoelectric signals via nonnegative matrix factorization","volume":"2018","author":"Soomro","year":"2018","journal-title":"Appl. Bionics Biomech."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"27257","DOI":"10.1109\/ACCESS.2019.2902122","article-title":"Muscle activity analysis using higher-order tensor decomposition: Application to muscle synergy extraction","volume":"7","author":"Ebied","year":"2019","journal-title":"IEEE Access"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.medengphy.2018.04.003","article-title":"Evaluation of matrix factorisation approaches for muscle synergy extraction","volume":"57","author":"Ebied","year":"2018","journal-title":"Med. Eng. Phys."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1177\/1545968313517751","article-title":"Reducing abnormal muscle coactivation after stroke using a myoelectric-computer interface: A pilot study","volume":"28","author":"Wright","year":"2014","journal-title":"Neurorehabilit. Neural Repair"},{"key":"ref_35","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_36","unstructured":"Lee, D.D., and Seung, H.S. (December, January 27). Algorithms for non-negative matrix factorization. Proceedings of the 14th Annual Neural Information Processing Systems Conference, Denver, CO, USA."},{"key":"ref_37","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_38","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1038\/29528","article-title":"Signal-dependent noise determines motor planning","volume":"394","author":"Harris","year":"1998","journal-title":"Nature"},{"key":"ref_39","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_40","first-page":"1457","article-title":"Non-negative matrix factorization with sparseness constraints","volume":"5","author":"Hoyer","year":"2004","journal-title":"J. Mach. Learn. Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2118","DOI":"10.1109\/TNSRE.2019.2939193","article-title":"Temporal features of muscle synergies in sit-to-stand motion reflect the motor impairment of post-stroke patients","volume":"27","author":"Yang","year":"2019","journal-title":"IEEE Trans. Neural Syst. Rehabilit. Eng."},{"key":"ref_42","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_43","doi-asserted-by":"crossref","first-page":"6459","DOI":"10.1007\/s00216-020-02628-2","article-title":"Discrimination of grass pollen of different species by FTIR spectroscopy of individual pollen grains","volume":"412","author":"Diehn","year":"2020","journal-title":"Anal. Bioanal. Chem."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1631\/FITEE.1600028","article-title":"Non-negativematrix factorization based unmixing for principal component transformed hyperspectral data","volume":"17","author":"Geng","year":"2016","journal-title":"Front. Inform. Technol. Electron. Eng."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1425","DOI":"10.1021\/ac00014a016","article-title":"Interactive self-modeling mixture analysis","volume":"63","author":"Windig","year":"1991","journal-title":"Anal. Chem."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"2633","DOI":"10.1016\/S1386-1425(02)00010-0","article-title":"Self-modelling analysis applied to nanosecond transient absorption spectroscopy of flavone: An aid to elucidate and characterise reaction intermediates","volume":"58","author":"Vrielynck","year":"2002","journal-title":"Spectrochim. Acta A"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"118929","DOI":"10.1016\/j.saa.2020.118929","article-title":"Investigation of the binding properties between levamlodipine and HSA based on MCR-ALS and computer modeling","volume":"245","author":"Liu","year":"2021","journal-title":"Spectrochim. Acta A"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"3223","DOI":"10.1021\/acs.jnatprod.0c00214","article-title":"Detection of penicillin G produced by penicillium chrysogenum with raman microspectroscopy and multivariate curve resolution-alternating least-squares methods","volume":"83","author":"Horii","year":"2020","journal-title":"J. Nat. Prod."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1002\/env.3170050203","article-title":"Positive matrix factorization: A non-negative factor model with optimal utilization of error estimates of data values","volume":"5","author":"Paatero","year":"1994","journal-title":"Environmetrics"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"19563","DOI":"10.1073\/pnas.0910114106","article-title":"Stability of muscle synergies for voluntary actions after cortical stroke in humans","volume":"106","author":"Cheung","year":"2009","journal-title":"Proc. Acad. Natl. Sci. USA"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"11","DOI":"10.3389\/fncom.2013.00011","article-title":"Investigating reduction of dimensionality during single-joint elbow movements: A case study on muscle synergies","volume":"7","author":"Chiovetto","year":"2013","journal-title":"Front. Comput. Neurosci."},{"key":"ref_52","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."}],"container-title":["Sensors"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1424-8220\/21\/11\/3833\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:09:49Z","timestamp":1760162989000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1424-8220\/21\/11\/3833"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,1]]},"references-count":52,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2021,6]]}},"alternative-id":["s21113833"],"URL":"https:\/\/doi.org\/10.3390\/s21113833","relation":{},"ISSN":["1424-8220"],"issn-type":[{"value":"1424-8220","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,1]]}}}