scholarly journals Approaches to Revealing the Neural Basis of Muscle Synergies: A Review and A Critique

Author(s):  
Vincent C. K. Cheung ◽  
Kazuhiko Seki

The central nervous system (CNS) may produce coordinated motor outputs via the combination of motor modules representable as muscle synergies. Identification of muscle synergies has hitherto relied on applying factorization algorithms to multi-muscle electromyographic data (EMGs) recorded during motor behaviors. Recent studies have attempted to validate the neural basis of the muscle synergies identified by independently retrieving the muscle synergies through CNS manipulations and analytic techniques such as spike-triggered averaging of EMGs. Experimental data have demonstrated the pivotal role of the spinal premotor interneurons in the synergies' organization and the presence of motor cortical loci whose stimulations offer access to the synergies, but whether the motor cortex is also involved in organizing the synergies has remained unsettled. We argue that one difficulty inherent in current approaches to probing the synergies' neural basis is that the EMG generative model based on linear combination of synergies and the decomposition algorithms used for synergy identification are not grounded on enough prior knowledge from neurophysiology. Progress may be facilitated by constraining or updating the model and algorithms with knowledge derived directly from CNS manipulations or recordings. An investigative framework based on evaluating the relevance of neurophysiologically constrained models of muscle synergies to natural motor behaviors will allow a more sophisticated understanding of motor modularity, which will help the community move forward from the current debate on the neural versus non-neural origin of muscle synergies.

Biomechanics ◽  
2021 ◽  
Vol 1 (2) ◽  
pp. 253-263
Author(s):  
Ashar Turky Abd ◽  
Rajat Emanuel Singh ◽  
Kamran Iqbal ◽  
Gannon White

The human motor system is a complex neuro-musculo sensory system that needs further investigations of neuro-muscular commands and sensory-motor coupling to decode movement execution. Some researchers suggest that the central nervous system (CNS) activates a small set of modules termed muscle synergies to simplify motor control. Further, these modules form functional building blocks of movement as they can explain the neurophysiological characteristics of movements. We can identify and extract these muscle synergies from electromyographic signals (EMG) recorded in the laboratory by using linear decomposition algorithms, such as principal component analysis (PCA) and non-Negative Matrix Factorization Algorithm (NNMF). For the past three decades, the hypothesis of muscle synergies has received considerable attention as we attempt to understand and apply the concept of muscle synergies in clinical settings and rehabilitation. In this article, we first explore the concept of muscle synergies. We then present different strategies of adaptation in these synergies that the CNS employs to accomplish a movement goal.


2011 ◽  
Vol 106 (3) ◽  
pp. 1363-1378 ◽  
Author(s):  
Jinsook Roh ◽  
Vincent C. K. Cheung ◽  
Emilio Bizzi

Previous studies using intact and spinalized animals have suggested that coordinated movements can be generated by appropriate combinations of muscle synergies controlled by the central nervous system (CNS). However, which CNS regions are responsible for expressing muscle synergies remains an open question. We address whether the brain stem and spinal cord are involved in expressing muscle synergies used for executing a range of natural movements. We analyzed the electromyographic (EMG) data recorded from frog leg muscles before and after transection at different levels of the neuraxis—rostral midbrain (brain stem preparations), rostral medulla (medullary preparations), and the spinal-medullary junction (spinal preparations). Brain stem frogs could jump, swim, kick, and step, while medullary frogs could perform only a partial repertoire of movements. In spinal frogs, cutaneous reflexes could be elicited. Systematic EMG analysis found two different synergy types: 1) synergies shared between pre- and posttransection states and 2) synergies specific to individual states. Almost all synergies found in natural movements persisted after transection at rostral midbrain or medulla but not at the spinal-medullary junction for swim and step. Some pretransection- and posttransection-specific synergies for a certain behavior appeared as shared synergies for other motor behaviors of the same animal. These results suggest that the medulla and spinal cord are sufficient for the expression of most muscle synergies in frog behaviors. Overall, this study provides further evidence supporting the idea that motor behaviors may be constructed by muscle synergies organized within the brain stem and spinal cord and activated by descending commands from supraspinal areas.


Author(s):  
Joseph B. McMenamin ◽  
Bernadette Curry ◽  
Glen P. Taylor ◽  
Laurence E. Becker ◽  
E. Gordon Murphy

ABSTRACT:The clinical and neuropathological findings in two infants with congenital nemaline myopathy are described. One patient presented at birth with severe hypotonia, respiratory failure and contractures and died shortly after the neonatal period. The other presented at age two months with hypotonia and, following a period of clinical stability, died at age seven months from respiratory failure. Pathological findings in the fatal neonatal case revealed numerous rod bodies in lingual, pharyngeal, diaphragm and limb muscles, correlating with clinical findings. Significant, but less rod body involvement was found in the diaphragm and limb muscles of the second patient. Although a neural basis has been suggested for this disorder, no abnormalities were found in the central nervous system or in the peripheral nerves of these two severely affected patients.


It was in 1895 that Oliver & Schafer discovered the pressor activity of glycerol extracts of the pituitary. By 1928 it was clear that this activity, called vasopressin, was due to a peptide derived from the neural lobes of the pituitary and, in the early fifties, its structure and that of its ‘twin’, oxytocin, were determined by du Vigneaud and his colleagues, who were also able to prepare them synthetically. For a long time these two peptides, which were clearly of neural origin, were thought to have only peripheral physiological actions. However, evidence has gradually accumulated that these as well as some hormonal peptides not of neural origin, such as angiotensin and corticotrophin, could have actions on the central nervous system. The discovery of the enkephalins by Hughes & Kosterlitz in 1975 revealed the presence of an oligopeptide in the forebrain that could influence brain function and for which a specific receptor could be delineated which provided an immediate connection with the well documented non-peptide analgesic drugs of the morphine group. Within a short time discrete localization both of enkaphalin stores and of enkephalin receptors within the nervous system was demonstrated. In the ensuing period a growing number of peptides have either been isolated from the brain or have been inferred, from immunological evidence, to be present. Some of these peptides, such as insulin and gastrin, have well established peripheral biological actions, and their presence in the brain has engendered considerable surprise.


2000 ◽  
Vol 12 (1) ◽  
pp. 78-97 ◽  
Author(s):  
E. P. Loeb ◽  
S. F. Giszter ◽  
P. Saltiel and E. Bizzi ◽  
F. A. Mussa-Ivaldi

Cognitive approaches to motor control typically concern sequences of discrete actions without taking into account the stunning complexity of the geometry and dynamics of the muscles. This begs the question: Does the brain convert the intricate, continuous-time dynamics of the muscles into simpler discrete units of actions, and if so, how? One way for the brain to form discrete units of behavior from muscles is through the synergistic co-activation of muscles. While this possibility has long been known, the composition of potential muscle synergies has remained elusive. In this paper, we have focused on a method that allowed us to examine and compare the limb stabilization properties of all possible muscle combinations. We found that a small set (as few as 23 out of 65,536) of all possible combinations of 16 limb muscles are robust with respect to activation noise: these muscle combinations could stabilize the limb at predictable, restricted portions of the workspace in spite of broad variations in the force output of their component muscles. The locations at which the robust synergies stabilize the limb are not uniformly distributed throughout the leg's workspace, but rather, they cluster at four workspace areas. The simulated robust synergies are similar to the actual synergies we have previously found to be generated by activation of the spinal cord. Thus, we have developed a new analytical method that enabled us to select a few muscle synergies with interesting properties out of the set of possible muscle combinations. Beyond this, the identification of robustness as a common property of the synergies in simple motor behaviors will open the way to the study of dynamic stability, which is an important and distinct property of the vertebrate motor-control system.


2019 ◽  
Vol 238 (1) ◽  
pp. 121-138
Author(s):  
Laura Pellegrino ◽  
Martina Coscia ◽  
Maura Casadio

2014 ◽  
Vol 112 (2) ◽  
pp. 316-327 ◽  
Author(s):  
Shota Hagio ◽  
Motoki Kouzaki

To simplify redundant motor control, the central nervous system (CNS) may modularly organize and recruit groups of muscles as “muscle synergies.” However, smooth and efficient movements are expected to require not only low-dimensional organization, but also flexibility in the recruitment or combination of synergies, depending on force-generating capability of individual muscles. In this study, we examined how the CNS controls activations of muscle synergies as changing joint angles. Subjects performed multidirectional isometric force generations around right ankle and extracted the muscle synergies using nonnegative matrix factorization across various knee and hip joint angles. As a result, muscle synergies were selectively recruited with merging or decomposition as changing the joint angles. Moreover, the activation profiles, including activation levels and the direction indicating the peak, of muscle synergies across force directions depended on the joint angles. Therefore, we suggested that the CNS selects appropriate muscle synergies and controls their activation patterns based on the force-generating capability of muscles with merging or decomposing descending neural inputs.


2017 ◽  
Vol 114 (32) ◽  
pp. 8643-8648 ◽  
Author(s):  
Tomohiko Takei ◽  
Joachim Confais ◽  
Saeka Tomatsu ◽  
Tomomichi Oya ◽  
Kazuhiko Seki

Grasping is a highly complex movement that requires the coordination of multiple hand joints and muscles. Muscle synergies have been proposed to be the functional building blocks that coordinate such complex motor behaviors, but little is known about how they are implemented in the central nervous system. Here we demonstrate that premotor interneurons (PreM-INs) in the primate cervical spinal cord underlie the spatiotemporal patterns of hand muscle synergies during a voluntary grasping task. Using spike-triggered averaging of hand muscle activity, we found that the muscle fields of PreM-INs were not uniformly distributed across hand muscles but rather distributed as clusters corresponding to muscle synergies. Moreover, although individual PreM-INs have divergent activation patterns, the population activity of PreM-INs reflects the temporal activation of muscle synergies. These findings demonstrate that spinal PreM-INs underlie the muscle coordination required for voluntary hand movements in primates. Given the evolution of neural control of primate hand functions, we suggest that spinal premotor circuits provide the fundamental coordination of multiple joints and muscles upon which more fractionated control is achieved by superimposed, phylogenetically newer, pathways.


2006 ◽  
Vol 95 (4) ◽  
pp. 2199-2212 ◽  
Author(s):  
Matthew C. Tresch ◽  
Vincent C. K. Cheung ◽  
Andrea d'Avella

Several recent studies have used matrix factorization algorithms to assess the hypothesis that behaviors might be produced through the combination of a small number of muscle synergies. Although generally agreeing in their basic conclusions, these studies have used a range of different algorithms, making their interpretation and integration difficult. We therefore compared the performance of these different algorithms on both simulated and experimental data sets. We focused on the ability of these algorithms to identify the set of synergies underlying a data set. All data sets consisted of nonnegative values, reflecting the nonnegative data of muscle activation patterns. We found that the performance of principal component analysis (PCA) was generally lower than that of the other algorithms in identifying muscle synergies. Factor analysis (FA) with varimax rotation was better than PCA, and was generally at the same levels as independent component analysis (ICA) and nonnegative matrix factorization (NMF). ICA performed very well on data sets corrupted by constant variance Gaussian noise, but was impaired on data sets with signal-dependent noise and when synergy activation coefficients were correlated. Nonnegative matrix factorization (NMF) performed similarly to ICA and FA on data sets with signal-dependent noise and was generally robust across data sets. The best algorithms were ICA applied to the subspace defined by PCA (ICAPCA) and a version of probabilistic ICA with nonnegativity constraints (pICA). We also evaluated some commonly used criteria to identify the number of synergies underlying a data set, finding that only likelihood ratios based on factor analysis identified the correct number of synergies for data sets with signal-dependent noise in some cases. We then proposed an ad hoc procedure, finding that it was able to identify the correct number in a larger number of cases. Finally, we applied these methods to an experimentally obtained data set. The best performing algorithms (FA, ICA, NMF, ICAPCA, pICA) identified synergies very similar to one another. Based on these results, we discuss guidelines for using factorization algorithms to analyze muscle activation patterns. More generally, the ability of several algorithms to identify the correct muscle synergies and activation coefficients in simulated data, combined with their consistency when applied to physiological data sets, suggests that the muscle synergies found by a particular algorithm are not an artifact of that algorithm, but reflect basic aspects of the organization of muscle activation patterns underlying behaviors.


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