Alterations in motor modules and their contribution to limitations in force control in the upper extremity after stroke.

The generation of isometric force at the hand can be mediated by activating a few motor modules. Stroke induces alterations in motor modules underlying steady-state isometric force generation in the human upper extremity (UE). However, how the altered motor modules impact task performance (force production) remains unclear as stroke survivors develop and converge to the three-dimensional (3D) target force. Thus, we tested whether stroke-specific motor modules would be activated from the onset of force generation and also examined how alterations in motor modules would induce changes in force representation. During 3D isometric force development, electromyographic (EMG) signals were recorded from eight major elbow and shoulder muscles in the paretic arm of 10 chronic hemispheric stroke survivors and both arms of six age-matched control participants. A non-negative matrix factorization algorithm identified motor modules in four different time windows: three "exploratory" force ramping phases (Ramps 1-3; 0-33%, 33-67%, and 67-100% of target force magnitude, respectively) and the stable force match phase (Hold). Motor module similarity and between-force coupling were examined by calculating the scalar product and Pearson correlation across the phases. To investigate the association between the end-point force representation and the activation of the motor modules, principal component analysis (PCA) and multivariate multiple linear regression analyses were applied. In addition, the force components regressed on the activation profiles of motor modules were utilized to model the feasible force direction. Both stroke and control groups developed exploratory isometric forces with a non-linear relationship between EMG and force. During the force matching, only the stroke group showed abnormal between-force coupling in medial-lateral and backward-forward and medial-lateral and downward-upward directions. In each group, the same motor modules, including the abnormal deltoid module in stroke survivors, were expressed from the beginning of force development instead of emerging during the force exploration. The PCA and the multivariate multiple linear regression analyses showed that alterations in motor modules were associated with abnormal between-force coupling and limited feasible force direction after stroke. Overall, these results suggest that alterations in intermuscular coordination contribute to the abnormal end-point force control under isometric conditions in the UE after stroke.

The Effects of Selective Muscle Weakness on Muscle Coordination in the Human Arm.

Despite the fundamental importance of muscle coordination in daily life, it is currently unclear how muscle coordination adapts when the musculoskeletal system is perturbed. In this study, we quantified the impact of selective muscle weakness on several metrics of muscle coordination. Seven healthy subjects performed 2D and 3D isometric force target matches, while electromyographic (EMG) signals were recorded from 13 elbow and shoulder muscles. Subsequently, muscle weakness was induced by a motor point block of brachialis muscle. Postblock subjects repeated the force generation tasks. We quantified muscle coordination pre- and postblock using three metrics: tuning curve preferred direction, tuning curve area, and motor modules analysis via nonnegative matrix factorization. For most muscles, the tuning direction for the 2D protocol was not substantially altered postblock, while tuning areas changed more drastically. Typically, five motor modules were identified from the 3D task, and four motor modules were identified in the 2D task; this result held across both pre- and postblock conditions. The composition of one or two motor modules, ones that involved mainly the activation of shoulder muscles, was altered postblock. Our results demonstrate that selective muscle weakness can induce nonintuitive alternations in muscle coordination in the mechanically redundant human arm.

Evidence for altered upper extremity muscle synergies in chronic stroke survivors with mild and moderate impairment.

Previous studies indicate that motor coordination may be achieved by assembling task-dependent combinations of a few muscle synergies, defined here as fixed patterns of activation across a set of muscles. Our recent study of severely impaired chronic stroke survivors showed that some muscle synergies underlying isometric force generation at the hand are altered in the affected arm. However, whether similar alterations are evident in stroke survivors with lesser impairment remains unclear. Accordingly, we examined muscle synergies underlying spatial patterns of elbow and shoulder muscle activation recorded during an isometric force target matching protocol performed by 16 chronic stroke survivors, evenly divided across mild and moderate impairment levels. We applied non-negative matrix factorization to identify the muscle synergies and compared their structure across groups, including previously collected data from six age-matched control subjects and eight severely impaired stroke survivors. For all groups, EMG spatial patterns were well explained by task-dependent combinations of only a few (typically 4) muscle synergies. Broadly speaking, elbow-related synergies were conserved across stroke survivors, regardless of impairment level. In contrast, the shoulder-related synergies of some stroke survivors with mild and moderate impairment differed from controls, in a manner similar to severely impaired subjects. Cluster analysis of pooled synergies for the 30 subjects identified seven distinct clusters (synergies). Subsequent analysis confirmed that the incidences of three elbow-related synergies were independent of impairment level, while the incidences of four shoulder-related synergies were systematically correlated with impairment level. Overall, our results suggest that alterations in the shoulder muscle synergies underlying isometric force generation appear prominently in mild and moderate stroke, as in most cases of severe stroke, in an impairment level-dependent manner.

Alterations in upper limb muscle synergy structure in chronic stroke survivors.

Previous studies in neurologically intact subjects have shown that motor coordination can be described by task-dependent combinations of a few muscle synergies, defined here as a fixed pattern of activation across a set of muscles. Arm function in severely impaired stroke survivors is characterized by stereotypical postural and movement patterns involving the shoulder and elbow. Accordingly, we hypothesized that muscle synergy composition is altered in severely impaired stroke survivors. Using an isometric force matching protocol, we examined the spatial activation patterns of elbow and shoulder muscles in the affected arm of 10 stroke survivors (Fugl-Meyer <25/66) and in both arms of six age-matched controls. Underlying muscle synergies were identified using non-negative matrix factorization. In both groups, muscle activation patterns could be reconstructed by combinations of a few muscle synergies (typically 4). We did not find abnormal coupling of shoulder and elbow muscles within individual muscle synergies. In stroke survivors, as in controls, two of the synergies were comprised of isolated activation of the elbow flexors and extensors. However, muscle synergies involving proximal muscles exhibited consistent alterations following stroke. Unlike controls, the anterior deltoid was coactivated with medial and posterior deltoids within the shoulder abductor/extensor synergy and the shoulder adductor/flexor synergy in stroke was dominated by activation of pectoralis major, with limited anterior deltoid activation. Recruitment of the altered shoulder muscle synergies was strongly associated with abnormal task performance. Overall, our results suggest that an impaired control of the individual deltoid heads may contribute to poststroke deficits in arm function.

Robustness of muscle synergies underlying three-dimensional force generation at the hand in healthy humans.

Previous studies using advanced matrix factorization techniques have shown that the coordination of human voluntary limb movements may be accomplished using combinations of a small number of intermuscular coordination patterns, or muscle synergies. However, the potential use of muscle synergies for isometric force generation has been evaluated mostly using correlational methods. The results of such studies suggest that fixed relationships between the activations of pairs of muscles are relatively rare. There is also emerging evidence that the nervous system uses independent strategies to control movement and force generation, which suggests that one cannot conclude a priori that isometric force generation is accomplished by combining muscle synergies, as shown in movement control. In this study, we used non-negative matrix factorization to evaluate the ability of a few muscle synergies to reconstruct the activation patterns of human arm muscles underlying the generation of three-dimensional (3-D) isometric forces at the hand. Surface electromyographic (EMG) data were recorded from eight key elbow and shoulder muscles during 3-D force target-matching protocols performed across a range of load levels and hand positions. Four synergies were sufficient to explain, on average, 95% of the variance in EMG datasets. Furthermore, we found that muscle synergy composition was conserved across biomechanical task conditions, experimental protocols, and subjects. Our findings are consistent with the view that the nervous system can generate isometric forces by assembling a combination of a small number of muscle synergies, differentially weighted according to task constraints.

Impact of gravity loading on post-stroke reaching and its relationship to weakness.

The ability to extend the elbow following stroke depends on the magnitude and direction of torques acting at the shoulder. The mechanisms underlying this link remain unclear. The purpose of this study was to evaluate whether the effects of shoulder loading on elbow function were related to weakness or its distribution in the paretic limb. Ten subjects with longstanding hemiparesis performed movements with the arm either passively supported against gravity by an air bearing, or by activation of shoulder muscles. Isometric maximum voluntary torques at the elbow and shoulder were measured using a load cell. The speed and range of elbow extension movements were negatively impacted by actively supporting the paretic limb against gravity. However, the effects of gravity loading were not related to proximal weakness or abnormalities in the elbow flexor-extensor strength balance. The findings support the existence of abnormal descending motor commands that constrain the ability of stroke survivors to generate elbow extension torque in combination with abduction torque at the shoulder.

Modifiability of abnormal isometric elbow and shoulder joint torque coupling after stroke.

Unlike individuals with mild stroke, individuals with severe stroke are constrained to stereotypical movement patterns attributed to abnormal coupling of shoulder abductors with elbow flexors, and shoulder adductors with elbow extensors. Whether abnormal muscle coactivation and associated joint torque patterns can be changed in this population is important to determine given that it bears on the development of effective rehabilitation interventions. Eight subjects participated in a protocol that was designed to reduce abnormal elbow/shoulder joint torque coupling by training them to generate combinations of isometric elbow and shoulder joint torques away from the constraining patterns. After training, subjects demonstrated a significant reduction in abnormal torque coupling and a subsequent significant increase in ability to generate torque patterns away from the abnormal pattern. We suggest the rapid time-course of these changes reflects a residual capacity of the central nervous system to adapt to a novel behavioral training environment.

Target-dependent differences between free and constrained arm movements in chronic hemiparesis.

This study compares the kinematic and kinetic characteristics of constrained and free upper limb movements in eight subjects with chronic hemiparesis. Movements of the dominant and nondominant limbs were also examined in five control subjects. Rapid movements were performed in the horizontal plane from a central starting point to five targets located to require various combinations of flexion/extension rotations at the elbow and shoulder. Support of the upper limb against gravity loading was provided either by a low-friction air-bearing apparatus (constrained condition) or by voluntary generation of abduction and external rotation torques at the shoulder (free condition). Data analysis focused on the peak joint torques generated during the acceleratory phase of movement, and on the net change in joint angles at the elbow and shoulder. We found that movement parameters were broadly invariant with support condition for either limb of control subjects, as well as for the nonparetic limb of hemiparetic subjects. In contrast, support condition had a target-dependent effect on movements of the paretic limb. Relative to the constrained condition, peak torques for free arm movements were significantly reduced for distal targets requiring elbow extension and/or shoulder flexion torques. However, peak elbow flexion and shoulder extension joint torques for proximal targets were relatively unaffected by support condition. Of perhaps more functional importance, free movements were characterized by a target-dependent restriction in the hand's work area that reflected a reduced range of active elbow extension, relative to constrained movements. The target-dependent effects of support condition on movements of the paretic limb are consistent with the existence of abnormal constraints on muscle activation patterns in subjects with chronic hemiparesis, namely an abnormal linkage between activation of the elbow flexors and shoulder extensors, abductors, and external rotators.