A Systematic Review of EMG Applications for the Characterization of Forearm and Hand Muscle Activity during Activities of Daily Living: Results, Challenges, and Open Issues

The role of the hand is crucial for the performance of activities of daily living, thereby ensuring a full and autonomous life. Its motion is controlled by a complex musculoskeletal system of approximately 38 muscles. Therefore, measuring and interpreting the muscle activation signals that drive hand motion is of great importance in many scientific domains, such as neuroscience, rehabilitation, physiotherapy, robotics, prosthetics, and biomechanics. Electromyography (EMG) can be used to carry out the neuromuscular characterization, but it is cumbersome because of the complexity of the musculoskeletal system of the forearm and hand. This paper reviews the main studies in which EMG has been applied to characterize the muscle activity of the forearm and hand during activities of daily living, with special attention to muscle synergies, which are thought to be used by the nervous system to simplify the control of the numerous muscles by actuating them in task-relevant subgroups. The state of the art of the current results are presented, which may help to guide and foster progress in many scientific domains. Furthermore, the most important challenges and open issues are identified in order to achieve a better understanding of human hand behavior, improve rehabilitation protocols, more intuitive control of prostheses, and more realistic biomechanical models

A non-invasive human-machine interfacing framework for investigating dexterous control of hand muscles

The recent fast development of virtual reality and robotic assistive devices enables to augment the capabilities of able-body individuals as well as to overcome the motor missing functions of neurologically impaired or amputee individuals. To control these devices, movement intentions can be captured from biological structures involved in the process of motor planning and execution, such as the central nervous system (CNS), the peripheral nervous system (in particular the spinal motor neurons) and the musculoskeletal system. Thus, human-machine interfaces (HMI) enable to transfer neural information from the neuro-muscular system to machines. To prevent any risks due to surgical operations or tissue damage in implementing these HMIs, a non-invasive approach is proposed in this thesis. In the last five decades, surface electromyography (sEMG) has been extensively explored as a non-invasive source of neural information. EMG signals are constituted by the mixed electrical activity of several recruited motor units, the fundamental components of muscle contraction. High-density sEMG (HD-sEMG) with the use of blind source separation methods enabled to identify the discharge patterns of many of these active motor units. From these decomposed discharge patterns, the net common synaptic input (CSI) to the corresponding spinal motor neurons was quantified with cross-correlation in the time and frequency domain or with principal component analysis (PCA) on one or few muscles. It has been hypothesised that this CSI would result from the contribution of spinal descending commands sent by supra-spinal structures and afferences integrated by spinal interneurons. Another motor strategy implying the integration of descending commands at the spinal level is the one regarding the coordination of many muscles to control a large number of articular joints. This neurophysiological mechanism was investigated by measuring a single EMG amplitude per muscle, thus without the use of HD-sEMG and decomposition. In this case, the aim was to understand how the central nervous system (CNS) could control a large set of muscles actuating a vast set of combinations of degrees of freedom in a modular way. Thus, time-invariant patterns of muscle coordination, i.e. muscle synergies , were found in animals and humans from EMG amplitude of many muscles, modulated by time-varying commands to be combined to fulfil complex movements. In this thesis, for the first time, we present a non-invasive framework for human-machine interfaces based on both spinal motor neuron recruitment strategy and muscle synergistic control for unifying the understanding of these two motor control strategies and producing control signals correlated to biomechanical quantities. This implies recording both from many muscles and using HD-sEMG for each muscle. We investigated 14 muscles of the hand, 6 extrinsic and 8 intrinsic. The first two studies, (in Chapters 2 and 3, respectively) present the framework for CSI quantification by PCA and the extraction of the synergistic organisation of spinal motor neurons innervating the 14 investigated muscles. For the latter analysis, in Chapter 3, we proposed the existence of what we named as motor neuron synergies extracted with non-negative matrix factorisation (NMF) from the identified motor neurons. In these first two studies, we considered 7 subjects and 7 grip types involving differently all the four fingers in opposition with the thumb. In the first study, we found that the variance explained by the CSI among all motor neuron spike trains was (53.0 ± 10.9) % and its cross-correlation with force was 0.67 ± 0.10, remarkably high with respect to previous findings. In the second study, 4 motor neuron synergies were identified and associated with the actuation of one finger in opposition with the thumb, finding even higher correlation values with force (over 0.8) for each synergy associated with a finger during the actuation of the relative finger. In Chapter 4, we then extended the set of analysed movements in a vast repertoire of gestures and repeated the analysis of Chapter 3 by finding a different synergistic organisation during the execution of tens of tasks. We divided the contribution among extrinsic and intrinsic muscles and we found that intrinsic better enable single-finger spatial discrimination, while no difference was found in regression of joint angles by dividing the two groups of muscles. Finally, in Chapter 5 we proposed the techniques of the previous chapters for cases of impairment due both to amputation and stroke. We analysed one case of pre and post rehabilitation sessions of a trans-humeral amputee, the case of a post-stroke trans-radial amputee and three cases of acute stroke, i.e. less than one month from the stroke event. We present future perspectives (Chapter 6) aimed to design and implement a platform for both rehabilitation monitoring and myoelectric control. Thus, this thesis provides a bridge between two extensively studied motor control mechanisms, i.e. motor neuron recruitment and muscle synergies, and proposes this framework as suitable for rehabilitation monitoring and control of assistive devices.Open Acces

Down-Conditioning of Soleus Reflex Activity using Mechanical Stimuli and EMG Biofeedback

Spasticity is a common syndrome caused by various brain and neural injuries, which can severely impair walking ability and functional independence. To improve functional independence, conditioning protocols are available aimed at reducing spasticity by facilitating spinal neuroplasticity. This down-conditioning can be performed using different types of stimuli, electrical or mechanical, and reflex activity measures, EMG or impedance, used as biofeedback variable. Still, current results on effectiveness of these conditioning protocols are incomplete, making comparisons difficult. We aimed to show the within-session task- dependent and across-session long-term adaptation of a conditioning protocol based on mechanical stimuli and EMG biofeedback. However, in contrast to literature, preliminary results show that subjects were unable to successfully obtain task-dependent modulation of their soleus short-latency stretch reflex magnitude

Motor unit discharge variability is increased in mild-to-moderate Parkinson\u27s disease

Individuals with Parkinson\u27s disease (PD) demonstrate deficits in muscle activation such as decreased amplitude and inappropriate bursting. There is evidence that some of these disturbances are more pronounced in extensor vs. flexor muscles. Surface EMG has been used widely to quantify muscle activation deficits in PD, but analysis of discharge of the underlying motor units may provide greater insight and be more sensitive to changes early in the disease. Of the few studies that have examined motor unit discharge in PD, the majority were conducted in the first dorsal interosseous, and no studies have measured motor units from extensor and flexor muscles within the same cohort. The objective of this study was to characterize the firing behavior of single motor units in the elbow flexor and extensor muscles during isometric contractions in people with mild-to-moderate PD. Ten individuals with PD (off-medication) and nine healthy controls were tested. Motor unit spike times were recorded via intramuscular EMG from the biceps and triceps brachii muscles during 30-s isometric contractions at 10% maximum voluntary elbow flexion and elbow extension torque, respectively. We selected variables of mean motor unit discharge rate, discharge variability, and torque variability to evaluate motor abnormalities in the PD group. The effects of group, muscle, and group-by-muscle on each variable were determined using separate linear mixed models. Discharge rate and torque variability were not different between groups, but discharge variability was significantly higher in the PD group for both muscles combined

Neural pathways of movement fractionation

PhD THesis PhD ThesisStroke is a common neurological event which often results in motor deficits of the hand and arm. The reticulospinal tract (RST) may partly underlie residual hand and arm movement ability after a stroke but remains poorly characterised. A greater understanding of the RST could inform work to improve motor recovery. Additionally, the development of non-invasive methods of probing the RST in humans should allow comparison of the characteristics of the RST across species. It has been suggested that the RST is involved in mediating muscle responses to auditory startle, experimentally known as the StartReact paradigm. However, it was not clear how this pathway was involved. A human experiment presented here suggests that the RST comprises the final pathway in the StartReact effect, confirming it as a technique to probe the RST in humans. Other factors such as habituation and the validity of a marker of the StartReact effect were also further explored; these findings may inform future use of the technique. The output divergence, co-activation patterns, level of fractionation and synergies produced by the RST were further characterised in macaques and baboons; these factors had previously been mostly unexplored. In macaques, two subdivisions of primary motor cortex (M1) were also characterised in order to compare to the RST. These subdivisions are based upon the presence of corticomotoneuronal (CM) cells, and consist of ‘old’ (CM cells absent) and ‘new’ (CM cells present) M1. Stimulation of new M1 produced a higher level of fractionation of movement than stimulation of old M1 and the reticular formation (RF). The RF is suggested to produce slightly more fractionated behaviour than old M1, though the baboon RF responses may be less fractionated than those from macaque old M1. Output divergence of the RF as well as old and new M1 was also explored. However, methodological limitations may have biased the results towards muscles with more excitable motoneurons, or monosynaptic connections. Abstract ii In baboons, threshold stimulation elicited responses in upper limb and axial muscles only, with higher stimulation intensities or trains of pulses required to activate leg muscles. In contrast to long-held beliefs about RST output, distal upper limb muscles were more commonly activated than proximal ones. Previously reported attempts to record natural electromyography (EMG) data from macaques were limited to controlled experimental settings, and hence may have differed from EMG observed during truly natural behaviours. Here, EMG was recorded from 18 muscles in one macaque over several hours of natural, untrained activity in her home cage. Two matrix decomposition algorithms extracted three to four dominant synergies from the data. This number is comparable to that previously described for ‘natural’ behaviour in more controlled conditions, suggesting that it accurately reflects the dominant synergies used across both conditions. Future work should aim to delineate the respective contributions of the RST and corticospinal tract to natural movement and to develop approaches to manipulate RST projections in humans to improve post-stroke motor outcomes

Advancing Medical Technology for Motor Impairment Rehabilitation: Tools, Protocols, and Devices

Excellent motor control skills are necessary to live a high-quality life. Activities such as walking, getting dressed, and feeding yourself may seem mundane, but injuries to the neuromuscular system can render these tasks difficult or even impossible to accomplish without assistance. Statistics indicate that well over 100 million people are affected by diseases or injuries, such as stroke, Parkinson’s Disease, Multiple Sclerosis, Cerebral Palsy, peripheral nerve injury, spinal cord injury, and amputation, that negatively impact their motor abilities. This wide array of injuries presents a challenge to the medical field as optimal treatment paradigms are often difficult to implement due to a lack of availability of appropriate assessment tools, the inability for people to access the appropriate medical centers for treatment, or altogether gaps in technology for treating the underlying impairments causing the disability. Addressing each of these challenges will improve the treatment of movement impairments, provide more customized and continuous treatment to a larger number of patients, and advance rehabilitative and assistive device technology. In my research, the key approach was to develop tools to assess and treat upper extremity movement impairment. In Chapter 2.1, I challenged a common biomechanical[GV1] modeling technique of the forearm. Comparing joint torque values through inverse dynamics simulation between two modeling platforms, I discovered that representing the forearm as a single cylindrical body was unable to capture the inertial parameters of a physiological forearm which is made up of two segments, the radius and ulna. I split the forearm segment into a proximal and distal segment, with the rationale being that the inertial parameters of the proximal segment could be tuned to those of the ulna and the inertial parameters of the distal segment could be tuned to those of the radius. Results showed a marked increase in joint torque calculation accuracy for those degrees of freedom that are affected by the inertial parameters of the radius and ulna. In Chapter 2.2, an inverse kinematic upper extremity model was developed for joint angle calculations from experimental motion capture data, with the rationale being that this would create an easy-to-use tool for clinicians and researchers to process their data. The results show accurate angle calculations when compared to algebraic solutions. Together, these chapters provide easy-to-use models and tools for processing movement assessment data. In Chapter 3.1, I developed a protocol to collect high-quality movement data in a virtual reality task that is used to assess hand function as part of a Box and Block Test. The goal of this chapter is to suggest a method to not only collect quality data in a research setting but can also be adapted for telehealth and at home movement assessment and rehabilitation. Results indicate that the data collected in this protocol are good and the virtual nature of this approach can make it a useful tool for continuous, data driven care in clinic or at home. In Chapter 3.2 I developed a high-density electromyography device for collecting motor unit action potentials of the arm. Traditional surface electromyography is limited by its ability to obtain signals from deep muscles and can also be time consuming to selectively place over appropriate muscles. With this high-density approach, muscle coverage is increased, placement time is decreased, and deep muscle activity can potentially be collected due to the high-density nature of the device[GV2] . Furthermore, the high-density electromyography device is built as a precursor to a high-density electromyography-electrical stimulation device for functional electrical stimulation. The customizable nature of the prototype in Chapter 3.2 allows for the implementation both recording and stimulating electrodes. Furthermore, signal results show that the electromyography data obtained from the device are of high quality and are correlated with gold standard surface electromyography sensors. One key factor in a device that can record and then stimulate based on the information from the recorded signals is an accurate movement intent decoder. High-quality movement decoders have been designed by closed-loop device controllers in the past, but they still struggle when the user interacts with objects of varying weight due to underlying alterations in muscle signals. In Chapter 4, I investigate this phenomenon by administering an experiment where participants perform a Box and Block Task with objects of 3 different weights, 0 kg, 0.02 kg, and 0.1 kg. Electromyography signals of the participants right arm were collected and co-contraction levels between antagonistic muscles were analyzed to uncover alterations in muscle forces and joint dynamics. Results indicated contraction differences between the conditions and also between movement stages (contraction levels before grabbing the block vs after touching the block) for each condition. This work builds a foundation for incorporating object weight estimates into closed-loop electromyography device movement decoders. Overall, we believe the chapters in this thesis provide a basis for increasing availability to movement assessment tools, increasing access to effective movement assessment and rehabilitation, and advance the medical device and technology field

Mechanisms of Impaired Motor Unit Firing Behavior in the Vastus Lateralis Muscle after Stroke

The purpose of this dissertation research project was to examine the role of impaired motor unit firing behavior on force generation after a stroke. We studied the relationship between intrinsic motoneuron properties and inhibitory sensory pathways to deficient motoneuron activity in the vastus lateralis muscle after a stroke. Individuals with stroke often have deficits with force generation and volitional relaxation. Current models of impaired force output after a stroke focus primarily on the pathology within the corticospinal pathway because of decreased descending drive. Though this is an important aspect of deficient motoneuron output, it is incomplete because motoneurons receive other inputs that can shape motor output. Because the motoneuron is the last site of signal integration for muscle contractions, using methods that study motor unit activity can provide a window to the activity in the spinal circuitry. This research study utilized a novel algorithm that decomposed electromyography (EMG) signals into the contributions of the individual motor units. This provided the individual firing instances for a large number of concurrently active motor units during isometric contractions of the knee extensors. In the first aim, the association between the hyperemic response and motor unit firing rate modulation to intermittent, fatiguing contractions was investigated. It was found that the magnitude of blood flow was lower for individuals with stroke compared to healthy controls, but both groups increased blood flow similarly in response to fatiguing contractions. This did not relate to changes in muscle fiber contractibility for the participants with stroke; rather, participants better able to increase blood flow showed greater modulation in motor unit firing rates. To further investigate how ischemic conditions impact motor unit output, the second aim used a blood pressure cuff to completely occlude blood flow through the femoral artery with the intent of activating inhibitory afferent pathways. We found that ischemic conditions had a greater inhibitory impact on motor unit output for individuals with stroke compared to healthy controls, possibly because of hyper-excitable group III/IV afferent pathways. The final aim investigated how stroke related changes in the intrinsic excitability of the motoneurons impacted prolonged motor unit firing during voluntary relaxation. A serotonin reuptake inhibitor was administered to quantify motoneuron sensitivity to neuromodulatory inputs. This study found that the serotonin reuptake inhibitor increased muscle relaxation and may have reduced persistent inward current contributions to prolonged motor unit firing. In conclusion, while damage to the corticospinal tract is a major component to poor functionality, the intrinsic properties of the motoneuron and sensory pathways to the motoneuron pool are essential for understanding deficient motor control after a stroke

A Biomimetic Approach to Controlling Restorative Robotics

Movement is the only way a person can interact with the world around them. When trauma to the neuromuscular systems disrupts the control of movement, quality of life suffers. To restore limb functionality, active robotic interventions and/or rehabilitation are required. Unfortunately, the primary obstacle in a person’s recovery is the limited robustness of the human-machine interfaces. Current systems rely on control approaches that rely on the person to learn how the system works instead of the system being more intuitive and working with the person naturally. My research goal is to design intuitive control mechanisms based on biological processes termed the biomimetic approach. I have applied this control scheme to problems with restorative robotics focused on the upper and lower limb control. Operating an advanced active prosthetic hand is a two-pronged problem of actuating a high-dimensional mechanism and controlling it with an intuitive interface. Our approach attempts to solve these problems by going from muscle activity, electromyography (EMG), to limb kinematics calculated through dynamic simulation of a musculoskeletal model. This control is more intuitive to the user because they attempt to move their hand naturally, and the prosthetic hand performs that movement. The key to this approach was validating simulated muscle paths using both experimental measurements and anatomical constraints where data is missing. After the validation, simulated muscle paths and forces are used to decipher the intended movement. After we have calculated the intended movement, we can move a prosthetic hand to match. This approach required minimal training to give an amputee the ability to control prosthetic hand movements, such as grasping. A more intuitive controller has the potential to improve how people interact and use their prosthetic hands. Similarly, the rehabilitation of the locomotor system in people with damaged motor pathways or missing limbs require appropriate interventions. The problem of decoding human motor intent in a treadmill walking task can be solved with a biomimetic approach. Estimated limb speed is essential for this approach according to the theoretical input-output computation performed by spinal central pattern generators (CPGs), which represents neural circuitry responsible for autonomous control of stepping. The system used the locomotor phases, swing and stance, to estimate leg speeds and enable self-paced walking as well as steering in virtual reality with congruent visual flow. The unique advantage of this system over the previous state-of-art is the independent leg speed control, which is required for multidirectional movement in VR. This system has the potential to contribute to VR gait rehab techniques. Creating biologically-inspired controllers has the potential to improve restorative robotics and allow people a better opportunity to recover lost functionality post-injury. Movement is the only way a person can interact with the world around them. When trauma to the neuromuscular systems disrupts the control of movement, quality of life suffers. To restore limb functionality, active robotic interventions and/or rehabilitation are required. Unfortunately, the primary obstacle in a person’s recovery is the limited robustness of the human-machine interfaces. Current systems rely on control approaches that rely on the person to learn how the system works instead of the system being more intuitive and working with the person naturally. My research goal is to design intuitive control mechanisms based on biological processes termed the biomimetic approach. I have applied this control scheme to problems with restorative robotics focused on the upper and lower limb control.Operating an advanced active prosthetic hand is a two-pronged problem of actuating a high-dimensional mechanism and controlling it with an intuitive interface. Our approach attempts to solve these problems by going from muscle activity, electromyography (EMG), to limb kinematics calculated through dynamic simulation of a musculoskeletal model. This control is more intuitive to the user because they attempt to move their hand naturally, and the prosthetic hand performs that movement. The key to this approach was validating simulated muscle paths using both experimental measurements and anatomical constraints where data is missing. After the validation, simulated muscle paths and forces are used to decipher the intended movement. After we have calculated the intended movement, we can move a prosthetic hand to match. This approach required minimal training to give an amputee the ability to control prosthetic hand movements, such as grasping. A more intuitive controller has the potential to improve how people interact and use their prosthetic hands.Similarly, the rehabilitation of the locomotor system in people with damaged motor pathways or missing limbs require appropriate interventions. The problem of decoding human motor intent in a treadmill walking task can be solved with a biomimetic approach. Estimated limb speed is essential for this approach according to the theoretical input-output computation performed by spinal central pattern generators (CPGs), which represents neural circuitry responsible for autonomous control of stepping. The system used the locomotor phases, swing and stance, to estimate leg speeds and enable self-paced walking as well as steering in virtual reality with congruent visual flow. The unique advantage of this system over the previous state-of-art is the independent leg speed control, which is required for multidirectional movement in VR. This system has the potential to contribute to VR gait rehab techniques.Creating biologically-inspired controllers has the potential to improve restorative robotics and allow people a better opportunity to recover lost functionality post-injury