Upper Limbs Muscle Co-contraction Changes Correlated With the Impairment of the Corticospinal Tract in Stroke Survivors: Preliminary Evidence From Electromyography and Motor-Evoked Potential

I hate research with motor evoked potentials. It tells us nothing about how to get to actual recovery.

Upper Limbs Muscle Co-contraction Changes Correlated With the Impairment of the Corticospinal Tract in Stroke Survivors: Preliminary Evidence From Electromyography and Motor-Evoked Potential

Wenfei Sheng^1†, Shijue Li^1†, Jiangli Zhao¹, Yujia Wang², Zichong Luo², Wai Leung Ambrose Lo¹, Minghui Ding¹, Chuhuai Wang^1* and Le Li^3*

• ¹Department of Rehabilitation Medicine, The First Affiliated Hospital of Sun Yat-sen University, Guangzhou, China
• ²Faculty of Science and Technology, University of Macau, Taipa, Macao SAR, China
• ³Institute of Medical Research, Northwestern Polytechnical University, Xi’an, China

Objective: Increased muscle co-contraction of the agonist and antagonist muscles during voluntary movement is commonly observed in the upper limbs of stroke survivors. Much remain to be understood about the underlying mechanism. The aim of the study is to investigate the correlation between increased muscle co-contraction and the function of the corticospinal tract (CST).

Methods: Nine stroke survivors and nine age-matched healthy individuals were recruited. All the participants were instructed to perform isometric maximal voluntary contraction (MVC) and horizontal task which consist of sponge grasp, horizontal transportation, and sponge release. We recorded electromyography (EMG) activities from four muscle groups during the MVC test and horizontal task in the upper limbs of stroke survivors. The muscle groups consist of extensor digitorum (ED), flexor digitorum (FD), triceps brachii (TRI), and biceps brachii (BIC). The root mean square (RMS) of EMG was applied to assess the muscle activation during horizontal task. We adopted a co-contraction index (CI) to evaluate the degree of muscle co-contraction. CST function was evaluated by the motor-evoked potential (MEP) parameters, including resting motor threshold, amplitude, latency, and central motor conduction time. We employed correlation analysis to probe the association between CI and MEP parameters.

Results: The RMS, CI, and MEP parameters on the affected side showed significant difference compared with the unaffected side of stroke survivors and the healthy group. The result of correlation analysis showed that CI was significantly correlated with MEP parameters in stroke survivors.

Conclusion: There existed increased muscle co-contraction and impairment in CST functionality on the affected side of stroke survivors. The increased muscle co-contraction was correlated with the impairment of the CST. Intervention that could improve the excitability of the CST may contribute to the recovery of muscle discoordination in the upper limbs of stroke survivors.

Introduction

Stroke is the major disease that leads to mortality and disability worldwide GBD 2016 Stroke Collaborators (2019). The most common impairment of stroke survivors is motor impairment, which affects an individual’s ability to perform everyday activities and participate in social life (Langhorne et al., 2009). Hemiparesis is the most common symptom in stroke survivors (Bourbonnais et al., 1989; Nakayama et al., 1994; Wolfe, 2000; Roger et al., 2012), with abnormal muscle activation patterns being commonly observed (Bourbonnais et al., 1989). In many stroke survivors, motor impairment originates primarily in abnormal muscle coactivation (Dewald et al., 2001). Muscle co-contraction refers to the simultaneous activity of the agonist and antagonist muscles across the same joint (Banks et al., 2017; Souissi et al., 2018). Surface electromyography (EMG) can detect the muscle activities of the agonist and antagonist muscles (Campanini et al., 2020), and it can be used to identify abnormal muscular coordination in stroke survivors (Bourbonnais et al., 1989; Safavynia et al., 2011). The co-contraction between agonist and antagonist muscles can be evaluated quantitatively using the co-contraction index (CI) (Frost et al., 1997; Song and Tong, 2013; Banks et al., 2017; Li et al., 2020). Song and Tong (2013) found that there was an increased co-contraction between agonist and antagonist muscles of elbow during voluntary movement on the affected side compared with the unaffected side in stroke survivors. Increased muscle co-contraction indicates that the muscles could not contract independently (Hu et al., 2013). Hammond et al. (1988) found that the agonist and antagonist muscles of the wrist joint have a higher co-contraction ratio during voluntary isometric contraction on the affected side compared with the healthy control group. Kamper and Rymer (2001) found that stroke survivors had excessive co-contraction of hand muscles compared with the healthy control group. Increased muscle co-contraction leads to impairment in the upper limb motor function in stroke survivors. Previous studies reported that increased muscle co-contraction had a negative effect on voluntary movement (Chae et al., 2002; Chalard et al., 2019). It could bring about increased duration of the movement, muscle discoordination, and decreased range of movement (Arene and Hidler, 2009; Gross et al., 2015; Sarcher et al., 2015). Several studies applied the CI to evaluate muscular coactivation pattern changes during stroke recovery (Hammond et al., 1988; Chae et al., 2002; Hu et al., 2009; Nam et al., 2017; Qian et al., 2017; Rong et al., 2017). Chae et al. (2002) found that the co-contraction between the agonist and antagonist muscles of the wrist showed a negative relationship to motor function of the upper limbs, evaluated by Fugl-Meyer scales and arm motor ability test. Previous studies assessed the structural and functional muscle alternation after stroke by ultrasonography (Kim et al., 2021), muscle biopsy (Dalise et al., 2020), sEMG (Hu et al., 2015), high-density-surface (HD-sEMG) (Tanzarella et al., 2020), and dual-energy X-ray absorptiometry (Choi et al., 2021). There are studies that applied sEMG, kinematic parameters, and clinical scales to evaluate the upper-limb motor function in stroke survivors (Donoso Brown et al., 2014; Pan et al., 2021). But these studies focused only on the changes in the properties of muscles. For better stroke rehabilitation, it is necessary to assess the peripheral muscle changes and alternation in descending motor pathway at the same time (Azzollini et al., 2021).

The corticospinal tract (CST) is the principal neural pathway of the voluntary drive to the upper limb where muscle synergy is modulated (Lemon, 2008; McMorland et al., 2015; Van Wittenberghe and Peterson, 2021). The assessment of CST includes the transcranial magnetic stimulation (TMS) and diffusion tensor imaging (DTI) (Jang, 2013; Potter-Baker et al., 2016). Motor-evoked potential (MEP), elicited by TMS, provides quantitative method for evaluating the functional integrity of the CST (Groppa et al., 2012; Bestmann and Krakauer, 2015; Okamoto et al., 2021). TMS could induce rapidly changing magnetic field that stimulates cortical neurons and generates induced current. The induced current then depolarizes cortical axons and triggers MEP at suprathreshold stimulus intensities. The MEP is transmitted to the peripheral muscle through a descending path such as CST and corticobulbar motor pathways (Groppa et al., 2012). MEP provides insight into the mechanisms of motor output control (Bestmann and Krakauer, 2015) and can be applied to monitor the clinical progression stroke recovery (Cakar et al., 2016). Longer latency, smaller amplitude, and higher thresholds of MEP were observed on the affected side compared with the unaffected side in stroke survivors (Turton et al., 1996; Pennisi et al., 2002). During the recovery from stroke, the MEP of the paresis side changes toward the healthy state (Barker et al., 2012). Byrnes et al. (1999) showed that the MEP had a broad relationship with motor deficit as assessed by the Motor Assessment Scale and British Medical Research Council Scale (Brouwer and Schryburt-Brown, 2006). Bowden et al. (2014) showed that muscle weakness of the upper limb in stroke survivors resulted from the impairment of the descending corticospinal connections. Madhavan et al. (2011) investigated the correlation between the CST integrity and muscle strength by TMS, DTI, and dynamometer. There are few studies combining the assessment of muscle activation with the evaluation of the CST. Although there are many studies using MEP to assess the motor function of the stroke survivors (Turton et al., 1996; Traversa et al., 1998; Hendricks et al., 2003), only a limited number of studies investigated the correlation between MEP and muscle discoordination in stroke survivors.

Hortobágyi and Devita (2006) found that there was increased muscle co-contraction in the agonist and antagonist muscles in older adults. The age-associated change in the muscle co-contraction might result from the cortical component. The increased coactivation between the ankle and knee extensors in the paretic leg of stroke survivors was correlated with alterations in propriospinal pathways (Dyer et al., 2011). Chalard et al. (2020) conducted an EEG study, which found that an increased co-contraction was correlated with cortical movement-related beta oscillation alterations. Increased recurrent Renshaw inhibition is considered to be related to the increased co-contraction of the agonist and antagonist muscles (Katz and Pierrot-Deseilligny, 1982), Another physiological mechanism associated with increased muscle co-contraction of the agonist and antagonist includes the decrease in the Ia reciprocal inhibition, presynaptic inhibition, and Ib inhibition (Morita et al., 2006; Crone et al., 2007; Baude et al., 2019). The decrease in reciprocal inhibition was associated with the impairment of the CST (Crone et al., 2004). Much remains to be understood about the correlation between the impairment of the CST and increased muscle co-contraction of the upper limbs of stroke survivors. The impaired motor function is not only the result of the dysfunction of central motor control system but the result of the alternation in muscle activation (Azzollini et al., 2021). MEP evoked by TMS could reflect the function of the CST. The sEMG data provided the information of the peripheral muscle activity. The correlation between sEMG and MEP from TMS could lead to a better understanding about the mechanism of the abnormal muscle contraction pattern in stroke survivors. Especially, these findings provided insights into the mechanism of increased muscle co-contraction in stroke survivors. Therefore, the study aimed to probe the possible correlation between MEP and CI of the agonist and antagonist muscles during voluntary movement of the upper limbs of stroke survivors. We attempted to investigate whether the abnormal muscle coordination was associated with the impairment of the CST in stroke survivors.

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