Letter to the Editor

Smoothing of electromyographic signals can influence the number of extracted muscle synergies

Considering the relationship between aging and neuromuscular control decline, early detection of age-related changes can ensure that timely interventions are implemented to attenuate or restore neuromuscular deficits. The dynamic motor control index (DMCI), a measure based on variance accounted for (VAF) by one muscle synergy (MS), is a metric used to assess age-related changes in neuromuscular control. The aim of the study was to investigate the use of one-synergy VAF, and consecutively DMCI, in assessing age-related changes in neuromuscular control over a range of exercises with varying difficulty.

Thirty-one subjects walked on a flat and inclined treadmill, as well as performed forward and lateral stepping up tasks. Motion and muscular activity were recorded, and muscle synergy analysis was conducted using one-synergy VAF, DMCI, and number of synergies.

Difference between older and younger group was observed for one-synergy VAF, DMCI for forward stepping up task (one-synergy VAF difference of 2.45 (0.22, 4.68) and DMCI of 9.21 (0.81, 17.61), p = 0.033), but not for lateral stepping up or walking.

The use of VAF based metrics and specifically DMCI, rather than number of MS, in combination with stepping forward exercise can provide a low-cost and easy to implement approach for assessing neuromuscular control in clinical settings.

Using a machine learning algorithm, individuals can be accurately identified from their muscle activation patterns during gait, leading to the concept of individual muscle activation signatures.

Are muscle activation signatures robust across different walking speeds?

We used an open dataset containing electromyographic (EMG) signals from 8 lower limb muscles in 50 asymptomatic adults walking at 5 speeds (extremely slow, very slow, slow, spontaneous, and fast). A machine learning approach classified the EMG profiles based on similar (intra-speed classification) or different (inter-speed classification) walking speeds as training and testing conditions.

Intra-speed median classification rates of muscle activation profiles increased with walking speed, from 92 % for extremely slow, to 100 % for self-selected fast walking conditions. Inter-speed median classification rates increased when the speed of the training condition was closer to that of the testing condition. Higher median classification rates were found across slow, spontaneous, and fast walking speed conditions, from 56 % to 96 %, compared with classification rates involving extremely and very slow walking speed conditions, from 6 % to 62 %.

Our findings reveal that i) muscle activation signatures are detectable for a large range of walking speeds, even those involving different gait strategies (intra-speed median classification rates from 92 % to 100 %), and ii) muscle activation signatures observed during very low walking speeds are not consistent with those observed at higher speeds, suggesting a difference in motor control strategy. Caution should therefore be exercised when assessing gait deviations of a slow walking patient against a normative database obtained at higher speed. Identifying the robustness of individual muscle activation signatures across different movements could help in detecting changes in motor control, otherwise difficult to detect on classical time-varying EMG patterns.

Muscle synergies have been proposed as a strategy employed by the central nervous system to control movements. Muscle synergy analysis is a well-established framework to examine the pathophysiological basis of neurological diseases and has been applied for analysis and assessment in clinical applications in the last decades, even if it has not yet been widely used in clinical diagnosis, rehabilitative treatment and interventions. Even if inconsistencies in the outputs among studies and lack of a normative pipeline including signal processing and synergy analysis limit the progress, common findings and results are identifiable as a basis for future research. Therefore, a literature review that summarizes methods and main findings of previous works on upper limb muscle synergies in clinical environment is needed to i) summarize the main findings so far, ii) highlight the barriers limiting their use in clinical applications, and iii) suggest future research directions needed for facilitating translation of experimental research to clinical scenarios.

Articles in which muscle synergies were used to analyze and assess upper limb function in neurological impairments were reviewed. The literature research was conducted in Scopus, PubMed, and Web of Science. Experimental protocols (e.g., the aim of the study, number and type of participants, number and type of muscles, and tasks), methods (e.g., muscle synergy models and synergy extraction methods, signal processing methods), and the main findings of eligible studies were reported and discussed.

383 articles were screened and 51 were selected, which involved a total of 13 diseases and 748 patients and 1155 participants. Each study investigated on average 15 ± 10 patients. Four to forty-one muscles were included in the muscle synergy analysis. Point-to-point reaching was the most used task. The preprocessing of EMG signals and algorithms for synergy extraction varied among studies, and non-negative matrix factorization was the most used method. Five EMG normalization methods and five methods for identifying the optimal number of synergies were used in the selected papers. Most of the studies report that analyses on synergy number, structure, and activations provide novel insights on the physiopathology of motor control that cannot be gained with standard clinical assessments, and suggest that muscle synergies may be useful to personalize therapies and to develop new therapeutic strategies. However, in the selected studies synergies were used only for assessment; different testing procedures were used and, in general, study-specific modifications of muscle synergies were observed; single session or longitudinal studies mainly aimed at assessing stroke (71% of the studies), even though other pathologies were also investigated. Synergy modifications were either study-specific or were not observed, with few analyses available for temporal coefficients. Thus, several barriers prevent wider adoption of muscle synergy analysis including a lack of standardized experimental protocols, signal processing procedures, and synergy extraction methods. A compromise in the design of the studies must be found to combine the systematicity of motor control studies and the feasibility of clinical studies. There are however several potential developments that might promote the use of muscle synergy analysis in clinical practice, including refined assessments based on synergistic approaches not allowed by other methods and the availability of novel models. Finally, neural substrates of muscle synergies are discussed, and possible future research directions are proposed.

This review provides new perspectives about the challenges and open issues that need to be addressed in future work to achieve a better understanding of motor impairments and rehabilitative therapy using muscle synergies. These include the application of the methods on wider scales, standardization of procedures, inclusion of synergies in the clinical decisional process, assessment of temporal coefficients and temporal-based models, extensive work on the algorithms and understanding of the physio-pathological mechanisms of pathology, as well as the application and adaptation of synergy-based approaches to various rehabilitative scenarios for increasing the available evidence.

How do muscle synergies change as motor skills are learned? The purpose of this study was to investigate the relationship between synergy number and skill acquisition, and to examine learning-related changes in synergy structure and activation patterns. We performed muscle synergy analysis using non-negative matrix factorization to identify muscle synergies from activation patterns of ten major leg muscles before and after recreational cyclists learned a novel one-legged pedal force aiming task (Park, Van Emmerik, & Caldwell, 2021). Synergy number was defined as the smallest number of factors from the matrix factorization algorithm that could explain more than the predefined threshold values. Improvements in pedal force direction after practice occurred without a change in the number of muscle synergies (four), suggesting that task constraints (e.g. the need for smooth pedaling motion) in this novel targeting task may limit the CNS to the same number of muscle synergies before and after practice. Improved task performance while continuing to satisfy multiple biomechanical tasks was obtained with changes in structure (muscle weightings) for one synergy, and activation amplitudes without changes in timing or pattern for three synergies. In each crank cycle quadrant, multiple synergies were altered in either structure or activation amplitude, suggesting that the cooperative changes may be essential for improving task performance while producing a smooth pedaling motion. Changes in both synergy structure and activation levels could be muscle coordination strategies in motor skill learning.

Locomotion is a complex behaviour that requires the coordination of multiple body segments and muscle groups. Here we investigated how the weakness and spasticity in individuals with Hereditary Spastic Paraplegia (HSP) affect the coordination patterns of the lower limbs. We analysed kinematics and electromyographic (EMG) activity from 12 leg muscles in 21 persons with HSP and 20 control subjects at matched walking speeds. To assess the locomotor coordination, we examined the covariation between thigh, shank and foot elevation angles by means of principal component analysis and the modular organization of EMG patterns using the non-negative matrix factorization algorithm. The characteristic features of the HSP gait consisted in changes of the elevation angles covariation, the shape of the gait loop, reduced range of motion of the distal segments and significantly lower foot lift. The EMG factorization analysis revealed a comparable structure of the motor output between HSP and control groups, but significantly wider basic temporal patterns associated with muscles innervated from the sacral spinal segments in HSP. Overall, the applied methodology highlighted the impact of the corticospinal degeneration and spasticity on the coordination of distal limb segments and basic muscle modules associated with distal spinal segments.

Surface ElectroMyography (sEMG) is widely used as a non-invasive tool for the assessment of motor control strategies. However, the standardization of the methods used for the estimation of sEMG amplitude is a problem yet to be solved; in most cases, sEMG amplitude is estimated through the extraction of the envelope of the signal via different low-pass filtering procedures with fixed cut-off frequencies chosen by the experimenter. In this work, we have shown how it is not possible to find the optimal choice of the cut-off frequency without any a priori knowledge on the signal; considering this, we have proposed an updated version of an iterative adaptive algorithm already present in literature, aiming to completely automatize the sEMG amplitude estimation. We have compared our algorithm to most of the typical solutions (fixed window filters and the previous version of the adaptive algorithm) for the extraction of the sEMG envelope, showing how the proposed adaptive procedure significantly improves the quality of the estimation, with a lower fraction of variance unexplained by the extracted envelope for different simulated modulating waveforms (p < 0.005). The definition of an entropy-based convergence criterion has allowed for a complete automatization of the process. We infer that this algorithm can ensure repeatability of the estimation of the sEMG amplitude, due to its independence from the experimental choices, so allowing for a quantitative interpretation in a clinical environment.