EDITORIAL

published: 18 December 2018

doi: 10.3389/fneur.2018.01122

Editorial: Electromyography (EMG)

Techniques for the Assessment and
Rehabilitation of Motor Impairment
Following Stroke
Cliff S. Klein 1*, Sheng Li 2*, Xiaogang Hu 3* and Xiaoyan Li 2*
1
Guangdong Work Injury Rehabilitation Center, Guangzhou, China, 2 University of Texas Health Science Center at Houston,
and TIRR Memorial Hermann Research Center, Houston, TX, United States, 3 Joint Department of Biomedical Engineering,
University of North Carolina at Chapel Hill and North Carolina State University, Raleigh, NC, United States

Keywords: electromyography, MUSC, motor, rehabilitation, stroke

Editorial on the Research Topic

Electromyography (EMG) Techniques for the Assessment and Rehabilitation of Motor

Impairment Following Stroke

The nineteen papers of the research topic Electromyography (EMG) Techniques for the Assessment
Edited and reviewed by:
Jean-Claude Baron,
and Rehabilitation of Motor Impairment Following Stroke highlight a variety of ways that
University of Cambridge, EMG may be used to better understand and treat stroke-induced brain damage. Seven papers
United Kingdom addressed the impact of weekly training on EMG properties and function post-stroke, and one
*Correspondence:
paper examined the effect of a robotic exoskeleton on gait during a single training session
Cliff S. Klein (Exercise/therapy interventions). Six of the seven training studies were concerned with upper
[email protected] limb function (one of which also assessed corticomuscular coupling), and one examined the effect
Sheng Li of foot drop stimulator training. The six upper limb studies used a variety of training modalities
[email protected] including Wii-based upper limb therapy (two papers from one group), EMG-driven robotic devices
Xiaogang Hu
with or without neuromuscular electrical stimulation (NMES) (three papers), and traditional
[email protected]
physical/occupational therapy (one paper).
Xiaoyan Li
[email protected] Another seven papers were focused on using EMG to examine motor impairment after stroke
(Mechanisms of motor impairment). These included one study that addressed coupling between
Specialty section: the index finger and thumb, whereas another addressed upper limb synergies during reaching. One
This article was submitted to paper examined EMG co-contraction during gait, and one addressed gait EMG during obstacle
Stroke, crossing. One group examined reticulospinal pathways during elbow flexor activity using startling
a section of the journal acoustic stimulation. Another studied masticatory muscle activity following brainstem stroke.
Frontiers in Neurology Finally, one group addressed coupling between the electroencephalogram (EEG) and EMG signals
Received: 30 November 2018 during upper limb movements.
Accepted: 06 December 2018 Four studies used novel EMG processing techniques to study motor control and
Published: 18 December 2018 impairment post-stroke (Novel EMG processing techniques). These included new approaches to
Citation: intramuscular EMG decomposition, coherence of motor unit firing patterns from surface EMG,
Klein CS, Li S, Hu X and Li X (2018) clustering index analysis of surface EMG, and pattern recognition from high density surface EMG.
Editorial: Electromyography (EMG)
Techniques for the Assessment and
Rehabilitation of Motor Impairment EXERCISE/THERAPY INTERVENTIONS
Following Stroke.
Front. Neurol. 9:1122. A number of studies examined the effects of an exercise/therapy program, or a single exercise
doi: 10.3389/fneur.2018.01122 session, on EMG and motor function. Some also addressed the associated cortical plasticity.

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Klein et al. EMG in Stroke Assessment/Rehabilitation

Upper Limb during gait over a 6 month period of community walking.

Many addressed the effect of exercise/therapy on upper limb A wavelet-based time-frequency analysis approach was used
muscle activation properties. Hesam-Shariati et al. examined to quantify activation changes of multiple ankle muscles in
changes in upper limb EMG activity resulting from the chronic stroke survivors. The findings suggest alterations in
standardized 14-day Wii-based Movement Therapy program motor unit recruitment strategies after foot drop stimulator use.
(i.e., Wii-tennis, golf, baseball) in chronic stroke survivors. They The outcomes establish the efficacy of a foot drop stimulator as a
found that training lead to different patterns of EMG changes rehabilitation intervention that may promote motor recovery in
that were related to the level of motor deficit. In their companion addition to reducing foot drop.
paper Hesam-Shariati et al. they quantified muscle synergies Quantitative and continuous monitoring of muscle activation
during therapy (Wii baseball swing) based on EMG activity of the is necessary to adjust training protocols in a timely manner.
affected arm muscles using a non-negative matrix factorization Androwis et al. used novel EMG analysis (Burst Duration
algorithm. They were able to identify differences in the number Similarity Index) to quantify the intensity and timing of muscle
of muscle synergies used by patients as a function of the level of activation during a single session of robotic gait therapy in acute
motor deficit. stroke survivors. The authors showed that a robotic exoskeleton
Device-assisted interventions offer a way to study and train can reduce the soleus and rectus femoris muscle activity in the
patients with more severe limb impairment. In a case study, Lu et affected limb during stance phase, and can also improve the
al. used forearm EMG signals to detect a stroke survivor’s motion timing of muscle activation in the affected limb.
intent, and then used the EMG to drive a hand exoskeleton to
assist with finger motion in real time. After 10-weeks of robot- Mechanisms of Motor Impairment
assisted hand therapy, the patient showed improved grip strength Surface EMG together with other signals recorded peripherally
and hand function. The results demonstrate the feasibility of or centrally provides a means to assess mechanisms of motor
robot-assisted training driven by myoelectric pattern recognition impairment. Jones and Kamper studied the coupling of the
in chronic stroke survivors. index finger and thumb during close-open pinching motions in
After a stroke, it is critically important to start rehabilitation chronic stroke survivors. A Cable-Actuated Finger Exoskeleton
early to take advantage of the highly plastic period of the neural was used to perturb joints of the index finger during pinching
system. In a pilot randomized control trial, Qian et al. evaluated motions, while finger/thumb muscle surface EMG and finger
the effects of 1 month (20 sessions) of EMG-driven NMES kinematics were recorded. They found that involuntary finger-
combined with robotic assistance, targeting the elbow, wrist, and thumb coupling was present during the dynamic pinching task,
fingers of subacute stroke survivors. EMG parameters, including with perturbation of the index finger impacting thumb activity.
the co-contraction index and the activation level of targeted This finding reveals a potential mechanism to improve hand
muscles were used to monitor the muscle coordination patterns. mobility following stroke. Li et al. analyzed motor synergies
They found that the NMES combined with robotic training could during arm reaching based on surface EMG recordings from
achieve higher motor outcomes at the distal joints and more multiple muscles and correlated with reaching kinematics. They
effective reduction in muscle tone than traditional therapy. were able to detect task-specific deficits in reaching movements
Some investigators also addressed training-related cortical after stroke
plasticity and corticomuscular coupling. Wilkins et al. found Ma et al. studied lower limb muscle activity during obstacle
EMG-driven NMES task-specific arm/hand training (7 weeks) crossing using surface EMG in chronic stroke survivors. EMG
improved hand opening and functional use in chronic stroke activity of the leading limb during the swing phase was larger
survivors with moderate to severe motor impairments. in all muscles in the stroke compared to the control group, and
Functional improvement was paralleled with functional TA activity increased with obstacle height in both groups. Co-
reorganization in the ipsilesional primary sensorimotor cortex. contraction between agonist-antagonist muscle pairs was larger
The neural plastic reorganization after functional improvement in the stroke group in the leading/ trailing limb during certain
was also seen with strengthened corticomuscular coupling. In a phases. The authors suggested that the greater muscle activation
case study of a subacute stroke subject, Zheng et al. evaluated during obstacle crossing following stroke may have a negative
corticomuscular coupling between EEG and EMG (biceps) impact on balance.
signals during elbow flexion before and after 1 month of regular It remains unclear whether co-contraction of agonist-
physical and occupational therapy. Corticomuscular coherence antagonist muscles is excessive and impacts gait significantly
was increased in the affected limb with functional improvement, following stroke. In chronic stroke survivors, Banks et al.
but not in the non-affected limb. These results exemplify that quantified surface EMG co-contraction of agonist-antagonist
stroke survivors with severe motor impairments may still muscle pairs in three ways (no normalization, normalized to
have the potential to improve hand function if appropriate the maximal EMG of the gait cycle, normalized to the M-
interventions are used to induce neural plasticity. wave) and determined their association with gait impairment
during treadmill walking. Co-contraction during the terminal
stance phase was not different between healthy controls and
Lower Limb the stroke subjects, regardless of the normalization method.
Pilkar et al. used different EMG-based indices to quantify Normalization also did not impact the ability to resolve group
the effects of a foot drop stimulator on muscle activation differences. Furthermore, the correlation between stance phase

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Klein et al. EMG in Stroke Assessment/Rehabilitation

co-contraction and walking speed was modest. Pathological subacute stroke survivors (88%) and 20 healthy control
co-contraction may not be a primary factor contributing to participants (94%).
impaired gait in most stroke survivors. The authors suggest other Dai et al. quantified the different types of connectivity in
approaches that account for timing and amplitude components the spinal networks and changes in their relative contributions
of the EMG (i.e., muscle synergy analysis) may better capture the after a stroke. By comparing the coherence of motor unit
relevant deficits. firing pattern across different isometric contractions, they
The coupling strength between the EEG and EMG signals identified significant changes in coherence in three frequency
during motion is instructive in assessing motor function. Gao bands: delta (1–4 Hz), alpha (8–12 Hz), and beta (15–30 Hz)
et al. studied subacute stroke patients completing tasks such as in the paretic hand muscles. These changes reflect increased
hand gripping and elbow bending. Stroke subjects demonstrated common synaptic inputs in the subcortical pathway and provide
greater strength in the bi-directional corticomuscular coupling evidence on different origins of impaired muscle activation in
between the EEG and EMG signals. Such changes suggest a stroke.
compensational strategy after the brain lesion. To further differentiate neurogenic and myopathic changes
It is difficult to assess activities of brainstem nuclei in vivo in the muscle, Tang et al. applied clustering index analysis to
even with the most advanced neuroimaging techniques. Startling examine surface EMG in the distal and proximal muscles of the
acoustic stimulation is known to stimulate the reticulospinal upper limb from 12 stroke survivors. They observed abnormally
pathways, thus allowing the opportunity to assess the role of high or low clustering index values in the paretic muscles
brainstem motor system indirectly. Li et al. analyzed changes compared to healthy controls. This finding may indicate that
in EMG and force in response to startling acoustic stimulation both neurogenic and myopathic changes may occur in paretic
during isometric elbow flexion in stroke survivors and healthy muscles.
controls. They reported that the sound-induced force and EMG Selection of appropriate features from surface EMG is
increase in stroke survivors was not significantly different from essential for development of highly effective pattern recognition
those in healthy controls. As such, there results suggest that algorithms in the EMG-controlled devices. Wang et al. developed
the reticulospinal projections do not increase their contributions a novel pattern recognition technique for precise discrimination
to muscle strength in stroke. Jian et al. analyzed surface EMG of 20 hand/upper limb functional movements in stroke survivors.
signals of bilateral masticatory muscles in stroke survivors after Specifically, they applied wavelet packet to extract the neural
brainstem stroke using multiple EMG parameters. In addition control features and used the Fisher’s class separability index
to expected differences between muscles and sides, they did not and the sequential feedforward selection analyses to select
observe the head position effect on muscle activation on both appropriate channels in high density surface EMG. Such
sides. These are valuable information as the results could advance implementation can facilitate use of surface EMG control in
the understanding whether head positions alter chewing and stroke rehabilitation.
swallowing activities in stroke survivors.

Novel EMG Processing Techniques AUTHOR CONTRIBUTIONS

Examining motor unit discharge and recruitment patterns
post-stroke can disclose valuable information pertaining All authors made an equal contribution to the work, and
to impaired spinal versus supraspinal motor control. EMG approved it for publication.
decomposition into constituent motor unit action potential
Conflict of Interest Statement: The authors declare that the research was
(MUAP) trains, however, is challenging with severe superposition conducted in the absence of any commercial or financial relationships that could
of multiple MUAPs. Ren et al. developed a new intramuscular be construed as a potential conflict of interest.
EMG decomposition technique to improve the accuracy
of EMG decomposition with interference patterns. The Copyright © 2018 Klein, Li, Hu and Li. This is an open-access article distributed
technique was implemented by using six stages of analysis under the terms of the Creative Commons Attribution License (CC BY). The use,
distribution or reproduction in other forums is permitted, provided the original
including feature extraction, clustering, refinement of the author(s) and the copyright owner(s) are credited and that the original publication
classification, and splitting of the superimposed MUAPs. in this journal is cited, in accordance with accepted academic practice. No use,
A high accuracy of MUAP detection was reported in 8 distribution or reproduction is permitted which does not comply with these terms.

Frontiers in Neurology | www.frontiersin.org 3 December 2018 | Volume 9 | Article 1122