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Temporal control of muscle synergies is linked with alpha-band neural drive.

ABSTRACT:

Key points

It is theorized that the nervous system controls groups of muscles together as functional units, or 'synergies', resulting in correlated electromyographic (EMG) signals among muscles. However, such correlation does not necessarily imply group-level neural control. Oscillatory synchronization (coherence) among EMG signals implies neural coupling, but it is not clear how this relates to control of muscle synergies. EMG was recorded from seven arm muscles of 10 adult participants rotating an upper limb ergometer, and EMG-EMG coherence, EMG amplitude correlations and their relationship with each other were characterized. A novel method to derive multi-muscle synergies from EMG-EMG coherence is presented and these are compared with classically defined synergies. Coherent alpha-band (8-16 Hz) drive was strongest among muscles whose gross activity levels are well correlated within a given task. The cross-muscle distribution and temporal modulation of coherent alpha-band drive suggests a possible role in the neural coordination/monitoring of synergies.

Abstract

During movement, groups of muscles may be controlled together by the nervous system as an adaptable functional entity, or 'synergy'. The rules governing when (or if) this occurs during voluntary behaviour in humans are not well understood, at least in part because synergies are usually defined by correlated patterns of muscle activity without regard for the underlying structure of their neural control. In this study, we investigated the extent to which comodulation of muscle output (i.e. correlation of electromyographic (EMG) amplitudes) implies that muscles share intermuscular neural input (assessed via EMG-EMG coherence analysis). We first examined this relationship among pairs of upper limb muscles engaged in an arm cycling task. We then applied a novel multidimensional EMG-EMG coherence analysis allowing synergies to be characterized on the basis of shared neural drive. We found that alpha-band coherence (8-16 Hz) is related to the degree to which overall muscle activity levels correlate over time. The extension of this coherence analysis to describe the cross-muscle distribution and temporal modulation of alpha-band drive revealed a close match to the temporal and structural features of traditionally defined muscle synergies. Interestingly, the coherence-derived neural drive was inversely associated with, and preceded, changes in EMG amplitudes by ∼200 ms. Our novel characterization of how alpha-band neural drive is dynamically distributed among muscles is a fundamental step forward in understanding the neural origins and correlates of muscle synergies.

SUBMITTER: Laine CM

PROVIDER: S-EPMC9009735 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Much debate has arisen from research on muscle synergies with respect to both limb impedance control and energy consumption. Studies of limb impedance control in the context of reaching movements and postural tasks have produced divergent findings, and this study explores whether the use of synergies by the central nervous system (CNS) can resolve these findings and also provide insights on mechanisms of energy consumption. In this study, we phrase these debates at the conceptual level of interactions between neural degrees of freedom and tasks constraints. This allows us to examine the ability of experimentally-observed synergies--correlated muscle activations--to control both energy consumption and the stiffness component of limb endpoint impedance. In our nominal 6-muscle planar arm model, muscle synergies and the desired size, shape, and orientation of endpoint stiffness ellipses, are expressed as linear constraints that define the set of feasible muscle activation patterns. Quadratic programming allows us to predict whether and how energy consumption can be minimized throughout the workspace of the limb given those linear constraints. We show that the presence of synergies drastically decreases the ability of the CNS to vary the properties of the endpoint stiffness and can even preclude the ability to minimize energy. Furthermore, the capacity to minimize energy consumption--when available--can be greatly affected by arm posture. Our computational approach helps reconcile divergent findings and conclusions about task-specific regulation of endpoint stiffness and energy consumption in the context of synergies. But more generally, these results provide further evidence that the benefits and disadvantages of muscle synergies go hand-in-hand with the structure of feasible muscle activation patterns afforded by the mechanics of the limb and task constraints. These insights will help design experiments to elucidate the interplay between synergies and the mechanisms of learning, plasticity, versatility and pathology in neuromuscular systems.

Project description:Purpose: A muscle synergies model was suggested to represent a simplifying motor control mechanism by the brainstem and spinal cord. The aim of the study was to investigate the feasibility of such control mechanisms in the rehabilitation of post-stroke individuals during the execution of hand-reaching movements in multiple directions, compared to non-stroke individuals. Methods: Twelve non-stroke and 13 post-stroke individuals participated in the study. Muscle synergies were extracted from EMG data that was recorded during hand reaching tasks, using the NMF algorithm. The optimal number of synergies was evaluated in both groups using the Variance Accounted For (VAF) and the Mean Squared Error (MSE). A cross validation procedure was carried out to define a representative set of synergies. The similarity index and the K-means algorithm were applied to validate the existence of such a set of synergies, but also to compare the modulation properties of synergies for different movement directions between groups. The similarity index and hierarchical cluster analysis were also applied to compare between group synergies. Results: Four synergies were chosen to optimally capture the variances in the EMG data, with mean VAF of 0.917 ± 0.034 and 0.883 ± 0.046 of the data variances, with respective MSE of 0.007 and 0.016, in the control and study groups, respectively. The representative set of synergies was set to be extracted from movement to the center of the reaching space. Two synergies had different muscle activation balance between groups. Seven and 17 clusters partitioned the muscle synergies of the control and study groups. The control group exhibited a gradual change in the activation in the amplitude in the time domain (modulation) of synergies, as reflected by the similarity index, whereas the study group exhibited consistently significant differences between all movement directions and the representative set of synergies. The study findings support the existence of a representative set of synergies, which are modulated to execute movements in different directions. Conclusions: Post-stroke individuals differently modulate the activation of synergies to different movement directions than do non-stroke individuals. The conclusion was supported by different muscle activation balances, similarity values and different classifications of synergies among groups.

Project description:The large number of mechanical degrees of freedom of the hand is not fully exploited during actual movements such as grasping. Usually, angular movements in various joints tend to be coupled, and EMG activities in different hand muscles tend to be correlated. The occurrence of covariation in the former was termed kinematic synergies, in the latter muscle synergies. This study addresses two questions: (i) Whether kinematic and muscle synergies can simultaneously accommodate for kinematic and kinetic constraints. (ii) If so, whether there is an interrelation between kinematic and muscle synergies. We used a reach-grasp-and-pull paradigm and recorded the hand kinematics as well as eight surface EMGs. Subjects had to either perform a precision grip or side grip and had to modify their grip force in order to displace an object against a low or high load. The analysis was subdivided into three epochs: reach, grasp-and-pull, and static hold. Principal component analysis (PCA, temporal or static) was performed separately for all three epochs, in the kinematic and in the EMG domain. PCA revealed that (i) Kinematic- and muscle-synergies can simultaneously accommodate kinematic (grip type) and kinetic task constraints (load condition). (ii) Upcoming grip and load conditions of the grasp are represented in kinematic- and muscle-synergies already during reach. Phase plane plots of the principal muscle-synergy against the principal kinematic synergy revealed (iii) that the muscle-synergy is linked (correlated, and in phase advance) to the kinematic synergy during reach and during grasp-and-pull. Furthermore (iv), pair-wise correlations of EMGs during hold suggest that muscle-synergies are (in part) implemented by coactivation of muscles through common input. Together, these results suggest that kinematic synergies have (at least in part) their origin not just in muscular activation, but in synergistic muscle activation. In short: kinematic synergies may result from muscle synergies.

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Temporal control of muscle synergies is linked with alpha-band neural drive.

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