Daniela Souza De Oliveira, Marco Carbonaro, Brent James Raiteri, Alberto Botter, Matthias Ponfick, Alessandro Del Vecchio
{"title":"The discharge characteristics of motor units innervating functionally paralyzed muscles.","authors":"Daniela Souza De Oliveira, Marco Carbonaro, Brent James Raiteri, Alberto Botter, Matthias Ponfick, Alessandro Del Vecchio","doi":"10.1152/jn.00389.2024","DOIUrl":null,"url":null,"abstract":"<p><p>For individuals with motor complete spinal cord injury (SCI), previous works have shown that spared motor neurons below the injury level can still be voluntarily controlled. In this study, we investigated the behavior of these neurons after SCI by analyzing neural and spatial properties of individual motor units using high-density surface electromyography (HDsEMG) and ultrasound imaging. The dataset for this study is based on motor unit data from our previous work (Oliveira et al. <i>Brain</i> 147: 3583-3595, 2024). Eight participants with chronic motor complete SCI and twelve uninjured controls attempted multiple hand movements, guided by a virtual hand, while we recorded forearm muscle activity. We analyzed the common synaptic input to motor neurons with a factorization method and found two dominant motor unit modes in both the SCI and control groups. Each mode was strongly correlated with the virtual hand's flexion or extension movements. The delay between flexion and extension movements and the motor unit modes was similar between groups, suggesting preserved common input to motor neurons after SCI. We classified motor units into task-modulated or nonmodulated (i.e., tonic or irregularly firing) based on their discharge patterns and phase difference with virtual hand kinematics and found a higher proportion of nonmodulated motor units in the SCI group. At the motor unit action potential level, we found larger motor unit territories after SCI. Finally, we observed distinct movements of paralyzed muscles with concurrent HDsEMG and ultrasound imaging, indicating the presence of highly functional motor units with distinct spared territories after SCI.<b>NEW & NOTEWORTHY</b> Here, we observed a similar pattern of motor unit activation during attempted hand movements in individuals with complete SCI, who cannot move their fingers, and in a control group, who performed the prescribed movements. Despite differences in individual motor unit behavior between these groups, such as a higher proportion of nonmodulated motor units in SCI, movement intention can still be decoded from paralyzed muscles.</p>","PeriodicalId":16563,"journal":{"name":"Journal of neurophysiology","volume":" ","pages":"343-357"},"PeriodicalIF":2.1000,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of neurophysiology","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1152/jn.00389.2024","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/12/20 0:00:00","PubModel":"Epub","JCR":"Q3","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
For individuals with motor complete spinal cord injury (SCI), previous works have shown that spared motor neurons below the injury level can still be voluntarily controlled. In this study, we investigated the behavior of these neurons after SCI by analyzing neural and spatial properties of individual motor units using high-density surface electromyography (HDsEMG) and ultrasound imaging. The dataset for this study is based on motor unit data from our previous work (Oliveira et al. Brain 147: 3583-3595, 2024). Eight participants with chronic motor complete SCI and twelve uninjured controls attempted multiple hand movements, guided by a virtual hand, while we recorded forearm muscle activity. We analyzed the common synaptic input to motor neurons with a factorization method and found two dominant motor unit modes in both the SCI and control groups. Each mode was strongly correlated with the virtual hand's flexion or extension movements. The delay between flexion and extension movements and the motor unit modes was similar between groups, suggesting preserved common input to motor neurons after SCI. We classified motor units into task-modulated or nonmodulated (i.e., tonic or irregularly firing) based on their discharge patterns and phase difference with virtual hand kinematics and found a higher proportion of nonmodulated motor units in the SCI group. At the motor unit action potential level, we found larger motor unit territories after SCI. Finally, we observed distinct movements of paralyzed muscles with concurrent HDsEMG and ultrasound imaging, indicating the presence of highly functional motor units with distinct spared territories after SCI.NEW & NOTEWORTHY Here, we observed a similar pattern of motor unit activation during attempted hand movements in individuals with complete SCI, who cannot move their fingers, and in a control group, who performed the prescribed movements. Despite differences in individual motor unit behavior between these groups, such as a higher proportion of nonmodulated motor units in SCI, movement intention can still be decoded from paralyzed muscles.
对于运动完全性脊髓损伤(SCI)的个体,以往的研究表明,损伤水平以下的备用运动神经元仍然可以被自愿控制。在这项研究中,我们通过高密度表面肌电图(HDsEMG)和超声成像分析单个运动单元的神经和空间特性来研究脊髓损伤后这些神经元的行为。本研究的数据集基于我们以前工作中的运动单元数据(Oliveira et al., 2024)。8名患有慢性运动性完全性脊髓损伤的参与者和12名未受伤的对照组在虚拟手的指导下进行了多次手部运动,同时我们记录了前臂肌肉的活动。我们用因式分解方法分析了运动神经元的共同突触输入,发现在脊髓损伤组和对照组中有两种主要的运动单元模式。每种模式都与虚拟手的屈伸运动密切相关。各组屈伸运动和运动单元模式之间的延迟相似,表明脊髓损伤后运动神经元保留了共同输入。我们根据放电模式和虚拟手运动学的相位差将运动单元分为任务调制或非调制(即强直或不规则放电),并发现SCI组中非调制运动单元的比例更高。在运动单元动作电位水平上,我们发现脊髓损伤后运动单元区域变大。最后,我们通过并发HDsEMG和超声成像观察到瘫痪肌肉的明显运动,表明脊髓损伤后存在具有明显保留区域的高功能运动单元。
期刊介绍:
The Journal of Neurophysiology publishes original articles on the function of the nervous system. All levels of function are included, from the membrane and cell to systems and behavior. Experimental approaches include molecular neurobiology, cell culture and slice preparations, membrane physiology, developmental neurobiology, functional neuroanatomy, neurochemistry, neuropharmacology, systems electrophysiology, imaging and mapping techniques, and behavioral analysis. Experimental preparations may be invertebrate or vertebrate species, including humans. Theoretical studies are acceptable if they are tied closely to the interpretation of experimental data and elucidate principles of broad interest.