{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T05:07:27Z","timestamp":1787029647876,"version":"build-2736575974"},"reference-count":52,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2024,4,28]],"date-time":"2024-04-28T00:00:00Z","timestamp":1714262400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Research Grants Council of the Hong Kong Special Administrative Region, China","award":["R4022-18"],"award-info":[{"award-number":["R4022-18"]}]},{"name":"Research Grants Council of the Hong Kong Special Administrative Region, China","award":["N_CUHK456\/21"],"award-info":[{"award-number":["N_CUHK456\/21"]}]},{"name":"Research Grants Council of the Hong Kong Special Administrative Region, China","award":["14114721"],"award-info":[{"award-number":["14114721"]}]},{"name":"Research Grants Council of the Hong Kong Special Administrative Region, China","award":["14119022"],"award-info":[{"award-number":["14119022"]}]},{"name":"Research Grants Council of the Hong Kong Special Administrative Region, China","award":["CityU 11217019"],"award-info":[{"award-number":["CityU 11217019"]}]},{"name":"Research Grants Council of the Hong Kong Special Administrative Region, China","award":["7005641"],"award-info":[{"award-number":["7005641"]}]},{"name":"Research Grants Council of the Hong Kong Special Administrative Region, China","award":["7005857"],"award-info":[{"award-number":["7005857"]}]},{"name":"City University of Hong Kong","award":["R4022-18"],"award-info":[{"award-number":["R4022-18"]}]},{"name":"City University of Hong Kong","award":["N_CUHK456\/21"],"award-info":[{"award-number":["N_CUHK456\/21"]}]},{"name":"City University of Hong Kong","award":["14114721"],"award-info":[{"award-number":["14114721"]}]},{"name":"City University of Hong Kong","award":["14119022"],"award-info":[{"award-number":["14119022"]}]},{"name":"City University of Hong Kong","award":["CityU 11217019"],"award-info":[{"award-number":["CityU 11217019"]}]},{"name":"City University of Hong Kong","award":["7005641"],"award-info":[{"award-number":["7005641"]}]},{"name":"City University of Hong Kong","award":["7005857"],"award-info":[{"award-number":["7005857"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Sensors"],"abstract":"<jats:p>Muscle synergy has been widely acknowledged as a possible strategy of neuromotor control, but current research has ignored the potential inhibitory components in muscle synergies. Our study aims to identify and characterize the inhibitory components within motor modules derived from electromyography (EMG), investigate the impact of aging and motor expertise on these components, and better understand the nervous system\u2019s adaptions to varying task demands. We utilized a rectified latent variable model (RLVM) to factorize motor modules with inhibitory components from EMG signals recorded from ten expert pianists when they played scales and pieces at different tempo\u2013force combinations. We found that older participants showed a higher proportion of inhibitory components compared with the younger group. Senior experts had a higher proportion of inhibitory components on the left hand, and most inhibitory components became less negative with increased tempo or decreased force. Our results demonstrated that the inhibitory components in muscle synergies could be shaped by aging and expertise, and also took part in motor control for adapting to different conditions in complex tasks.<\/jats:p>","DOI":"10.3390\/s24092820","type":"journal-article","created":{"date-parts":[[2024,4,29]],"date-time":"2024-04-29T08:49:24Z","timestamp":1714380564000},"page":"2820","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Rectified Latent Variable Model-Based EMG Factorization of Inhibitory Muscle Synergy Components Related to Aging, Expertise and Force\u2013Tempo Variations"],"prefix":"10.3390","volume":"24","author":[{"given":"Subing","family":"Huang","sequence":"first","affiliation":[{"name":"Department of Electrical Engineering, City University of Hong Kong, Hong Kong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoyu","family":"Guo","sequence":"additional","affiliation":[{"name":"Department of Electrical Engineering, City University of Hong Kong, Hong Kong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0863-1010","authenticated-orcid":false,"given":"Jodie J.","family":"Xie","sequence":"additional","affiliation":[{"name":"School of Biomedical Sciences, The Chinese University of Hong Kong, Hong Kong, China"},{"name":"Gerald Choa Neuroscience Institute, The Chinese University of Hong Kong, Hong Kong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3083-479X","authenticated-orcid":false,"given":"Kelvin Y. S.","family":"Lau","sequence":"additional","affiliation":[{"name":"School of Biomedical Sciences, The Chinese University of Hong Kong, Hong Kong, China"},{"name":"Gerald Choa Neuroscience Institute, The Chinese University of Hong Kong, Hong Kong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Electrical Engineering, City University of Hong Kong, Hong Kong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arthur D. P.","family":"Mak","sequence":"additional","affiliation":[{"name":"Department of Psychiatry, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong, China"},{"name":"Cambridgeshire and Peterborough NHS Foundation Trust, Fulbourn Hospital, Cambridge CB21 5EF, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6031-7320","authenticated-orcid":false,"given":"Vincent C. K.","family":"Cheung","sequence":"additional","affiliation":[{"name":"School of Biomedical Sciences, The Chinese University of Hong Kong, Hong Kong, China"},{"name":"Gerald Choa Neuroscience Institute, The Chinese University of Hong Kong, Hong Kong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4808-2490","authenticated-orcid":false,"given":"Rosa H. M.","family":"Chan","sequence":"additional","affiliation":[{"name":"Department of Electrical Engineering, City University of Hong Kong, Hong Kong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,4,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"51","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_2","doi-asserted-by":"crossref","first-page":"1686","DOI":"10.1152\/jn.00776.2013","article-title":"Can modular strategies simplify neural control of multidirectional human locomotion?","volume":"111","author":"Zelik","year":"2014","journal-title":"J. Neurophysiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"958","DOI":"10.1152\/jn.00499.2021","article-title":"Evidence for basic units of upper limb muscle synergies underlying a variety of complex human manipulations","volume":"127","author":"Saito","year":"2022","journal-title":"J. Neurophysiol."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Oliveira, A.S., Gizzi, L., Ketabi, S., Farina, D., and Kersting, U.G. (2016). Modular control of treadmill vs overground running. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0153307"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"912440","DOI":"10.3389\/fnhum.2022.912440","article-title":"Muscle activation patterns and muscle synergies reflect different modes of coordination during upper extremity movement","volume":"16","author":"Chen","year":"2023","journal-title":"Front. Hum. Neurosci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1282","DOI":"10.1016\/j.jbiomech.2009.03.009","article-title":"Modular control of human walking: A simulation study","volume":"42","author":"Neptune","year":"2009","journal-title":"J. Biomech."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2157","DOI":"10.1016\/j.jbiomech.2012.05.037","article-title":"Three-dimensional modular control of human walking","volume":"45","author":"Allen","year":"2012","journal-title":"J. Biomech."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1038\/nn1010","article-title":"Combinations of muscle synergies in the construction of a natural motor behavior","volume":"6","author":"Saltiel","year":"2003","journal-title":"Nat. Neurosci."},{"key":"ref_9","first-page":"126","article-title":"Modularity in motor control: From muscle synergies to cognitive action representation","volume":"9","author":"Giese","year":"2015","journal-title":"Front. Comput. Neurosci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"479352","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","first-page":"561","article-title":"Inter-muscular coordination during running on grass, concrete and treadmill","volume":"123","author":"Yaserifar","year":"2023","journal-title":"Eur. J. Appl. Physiol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Pale, U., Atzori, M., M\u00fcller, H., and Scano, A. (2020). Variability of muscle synergies in hand grasps: Analysis of intra-and inter-session data. Sensors, 20.","DOI":"10.3390\/s20154297"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1016\/j.gaitpost.2023.03.010","article-title":"Characteristics of muscle synergy and anticipatory synergy adjustments strategy when cutting in different angles","volume":"107","author":"Pan","year":"2024","journal-title":"Gait Posture"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1080\/17461391.2021.2014573","article-title":"Muscle coordination during archery shooting: A comparison of archers with different skill levels","volume":"23","author":"Baifa","year":"2023","journal-title":"Eur. J. Sport Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"e16202","DOI":"10.1016\/j.heliyon.2023.e16202","article-title":"Muscle synergies for evaluating upper limb in clinical applications: A systematic review","volume":"9","author":"Zhao","year":"2023","journal-title":"Heliyon"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"6997","DOI":"10.1038\/s41598-023-34151-6","article-title":"Muscle synergies in Parkinson\u2019s disease before and after the deep brain stimulation of the bilateral subthalamic nucleus","volume":"13","author":"Ghislieri","year":"2023","journal-title":"Sci. Rep."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1109\/OJEMB.2023.3263123","article-title":"Optimal identification of muscle synergies from typical sit-to-stand clinical tests","volume":"4","author":"Ranaldi","year":"2023","journal-title":"IEEE Open J. Eng. Med. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1109\/OJEMB.2019.2963666","article-title":"Modulating the structure of motor variability for skill learning through specific muscle synergies in elderlies and young adults","volume":"1","author":"Cheung","year":"2020","journal-title":"IEEE Open J. Eng. Med. Biol."},{"key":"ref_19","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_20","doi-asserted-by":"crossref","unstructured":"Luo, X., Wu, X., Chen, L., Zhao, Y., Zhang, L., Li, G., and Hou, W. (2019). Synergistic myoelectrical activities of forearm muscles improving robust recognition of multi-fingered gestures. Sensors, 19.","DOI":"10.3390\/s19030610"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Mileti, I., Zampogna, A., Santuz, A., Asci, F., Del Prete, Z., Arampatzis, A., Palermo, E., and Suppa, A. (2020). Muscle synergies in Parkinson\u2019s disease. Sensors, 20.","DOI":"10.3390\/s20113209"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1152\/jn.2001.85.2.605","article-title":"Muscle synergies encoded within the spinal cord: Evidence from focal intraspinal NMDA iontophoresis in the frog","volume":"85","author":"Saltiel","year":"2001","journal-title":"J. Neurophysiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1363","DOI":"10.1152\/jn.00842.2010","article-title":"Modules in the brain stem and spinal cord underlying motor behaviors","volume":"106","author":"Roh","year":"2011","journal-title":"J. Neurophysiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"604","DOI":"10.24272\/j.issn.2095-8137.2022.276","article-title":"Gradient descent decomposition of force-field motor primitives optogenetically elicited for motor mapping of the murine lumbosacral spinal cord","volume":"44","author":"Salmas","year":"2023","journal-title":"Zool. Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"17041","DOI":"10.1523\/JNEUROSCI.4297-10.2010","article-title":"Spinal interneurons facilitate coactivation of hand muscles during a precision grip task in monkeys","volume":"30","author":"Takei","year":"2010","journal-title":"J. Neurosci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"40","DOI":"10.3389\/fncom.2013.00040","article-title":"Synaptic and functional linkages between spinal premotor interneurons and hand-muscle activity during precision grip","volume":"7","author":"Takei","year":"2013","journal-title":"Front. Comput. Neurosci."},{"key":"ref_27","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_28","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."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"8850","DOI":"10.1523\/JNEUROSCI.4032-12.2013","article-title":"Spinal premotor interneurons mediate dynamic and static motor commands for precision grip in monkeys","volume":"33","author":"Takei","year":"2013","journal-title":"J. Neurosci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1152\/jn.1980.44.4.751","article-title":"Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells","volume":"44","author":"Fetz","year":"1980","journal-title":"J. Neurophysiol."},{"key":"ref_31","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_32","doi-asserted-by":"crossref","first-page":"e168448","DOI":"10.1172\/jci.insight.168448","article-title":"Aging alters mechanisms underlying voluntary movements in spinal motor neurons of mice, primates, and humans","volume":"8","author":"Castro","year":"2023","journal-title":"JCI Insight"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"111050","DOI":"10.1016\/j.exger.2020.111050","article-title":"Older adults reduce the complexity and efficiency of neuromuscular control to preserve walking balance","volume":"140","author":"Moraes","year":"2020","journal-title":"Exp. Gerontol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"102946","DOI":"10.1016\/j.humov.2022.102946","article-title":"Muscle synergies are modified with improved task performance in skill learning","volume":"83","author":"Park","year":"2022","journal-title":"Hum. Mov. Sci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1123\/mc.2020-0008","article-title":"Effects of varying Overground walking speeds on lower-extremity muscle synergies in healthy individuals","volume":"25","author":"Escalona","year":"2021","journal-title":"Mot. Control"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"535096","DOI":"10.3389\/fphys.2020.00751","article-title":"Muscle synergies and coherence networks reflect different modes of coordination during walking","volume":"11","author":"Kerkman","year":"2020","journal-title":"Front. Physiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"6220","DOI":"10.1523\/JNEUROSCI.6289-11.2012","article-title":"The control of locomotor frequency by excitation and inhibition","volume":"32","author":"Li","year":"2012","journal-title":"J. Neurosci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1152\/jn.00698.2016","article-title":"Revealing unobserved factors underlying cortical activity with a rectified latent variable model applied to neural population recordings","volume":"117","author":"Whiteway","year":"2017","journal-title":"J. Neurophysiol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Whiteway, M.R., Socha, K., Bonin, V., and Butts, D.A. (2019). Characterizing the nonlinear structure of shared variability in cortical neuron populations using latent variable models. Neurons Behav. Data Anal. Theory, 3, Available online: https:\/\/www.ncbi.nlm.nih.gov\/pmc\/articles\/PMC6779168\/.","DOI":"10.1101\/407858"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"75741","DOI":"10.1109\/ACCESS.2021.3081118","article-title":"Latent Variable Models Reconstruct Diversity of Neuronal Response to Drifting Gratings in Murine Visual Cortex","volume":"9","author":"Palmerston","year":"2021","journal-title":"IEEE Access"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"872","DOI":"10.1016\/j.celrep.2019.03.069","article-title":"Parallel processing of sound dynamics across mouse auditory cortex via spatially patterned thalamic inputs and distinct areal intracortical circuits","volume":"27","author":"Liu","year":"2019","journal-title":"Cell Rep."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"026017","DOI":"10.1088\/1741-2560\/11\/2\/026017","article-title":"A fast, robust algorithm for power line interference cancellation in neural recording","volume":"11","author":"Keshtkaran","year":"2014","journal-title":"J. Neural Eng."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2495","DOI":"10.1152\/jn.1998.80.5.2495","article-title":"Response patterns and force relations of monkey spinal interneurons during active wrist movement","volume":"80","author":"Maier","year":"1998","journal-title":"J. Neurophysiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.neuroscience.2023.07.010","article-title":"Age, Cognitive Task, and Arm Position Differently Affect Muscle Synergy Recruitment but have Similar Effects on Walking Balance","volume":"527","author":"Sawers","year":"2023","journal-title":"Neuroscience"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2700","DOI":"10.1109\/TNSRE.2022.3206887","article-title":"Age-related modifications of muscle synergies and their temporal activations for overground walking","volume":"30","author":"Guo","year":"2022","journal-title":"IEEE Trans. Neural Syst. Rehabil. Eng."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1152\/jn.00513.2022","article-title":"Motor patterns of patients with spinal muscular atrophy suggestive of sensory and corticospinal contributions to the development of locomotor muscle synergies","volume":"131","author":"Cheung","year":"2024","journal-title":"J. Neurophysiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1152\/jn.00425.2022","article-title":"Evolution of muscle coordination and mechanical output throughout four weeks of arm cranking submaximal training","volume":"129","author":"Cartier","year":"2023","journal-title":"J. Neurophysiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2632","DOI":"10.1016\/j.cub.2014.09.026","article-title":"A group of segmental premotor interneurons regulates the speed of axial locomotion in Drosophila larvae","volume":"24","author":"Kohsaka","year":"2014","journal-title":"Curr. Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1230","DOI":"10.1109\/TNSRE.2023.3242911","article-title":"Surface electromyography-based analysis of the lower limb muscle network and muscle synergies at various gait speeds","volume":"31","author":"Liang","year":"2023","journal-title":"IEEE Trans. Neural Syst. Rehabil. Eng."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1266","DOI":"10.1152\/japplphysiol.00128.2015","article-title":"In vivo behavior of the human soleus muscle with increasing walking and running speeds","volume":"118","author":"Lai","year":"2015","journal-title":"J. Appl. Physiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1002\/1097-0029(20000915)50:6<500::AID-JEMT7>3.0.CO;2-7","article-title":"Myosin isoforms, muscle fiber types, and transitions","volume":"50","author":"Pette","year":"2000","journal-title":"Microsc. Res. Tech."},{"key":"ref_52","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."}],"container-title":["Sensors"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1424-8220\/24\/9\/2820\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:35:33Z","timestamp":1760106933000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1424-8220\/24\/9\/2820"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,28]]},"references-count":52,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2024,5]]}},"alternative-id":["s24092820"],"URL":"https:\/\/doi.org\/10.3390\/s24092820","relation":{},"ISSN":["1424-8220"],"issn-type":[{"value":"1424-8220","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4,28]]}}}