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Alterations in intermuscular coordination underlying isokinetic exercise after a stroke and their implications on neurorehabilitation
Journal of NeuroEngineering and Rehabilitation volume 18, Article number: 110 (2021)
Abstract
Background
Abnormal intermuscular coordination limits the motor capability of stroke-affected upper limbs. By evaluating the intermuscular coordination in the affected limb under various biomechanical task constraints, the impact of a stroke on motor control can be analyzed and intermuscular coordination-based rehabilitation strategies can be developed. In this study, we investigated upper limb intermuscular coordination after a stroke during isokinetic movements.
Methods
Sixteen chronic stroke survivors and eight neurologically intact individuals were recruited. End-point forces and electromyographic activities of the shoulder and elbow muscles were measured while the participants performed isokinetic upper limb movements in a three-dimensional space. Intermuscular coordination of the stroke survivors and the control participants was quantified in the form of muscle synergies. Then, we compared the number, composition, and activation coefficients of muscle synergies and the end-point force between the groups. The correlation between the alteration of muscle synergies and the level of motor impairment was investigated.
Results
Four and five muscle synergies in the stroke and control groups were observed, respectively. The composition of muscle synergies was comparable between the groups, except that the three heads of the deltoid muscle were co-activated and formed one synergy in the stroke group, whereas those muscles formed two synergies in the control group. When the number of muscle synergies between the groups matched, the comparable composition of muscle synergies was observed in both groups. Alternatively, the modulation of synergy activation coefficients was altered after a stroke. The severity of motor impairments was negatively correlated with the similarity of the post-stroke synergies with respect to the mean control synergies.
Conclusions
Stroke-affected upper limbs seemed to modularize the activation of the shoulder and elbow muscles in a fairly similar way to that of neurologically intact individuals during isokinetic movements. Compared with free (i.e., unconstrained) movement, exercise under biomechanical constraints including the isokinetic constraint might promote the activation of muscle synergies independently in stroke survivors. We postulated the effect of biomechanical constraints on the intermuscular coordination and suggested a possible intermuscular coordination-based rehabilitation protocol that provides the biomechanical constraint appropriate to a trainee throughout the progress of rehabilitation.
Background
Motor impairments following a stroke affect the daily lives, social participation activities, and the quality of life of stroke survivors. In addition to spasticity and muscle weakness, abnormal and stereotypical intermuscular coordination contributes to the limited motor capability of the stroke-affected limb. In the case of upper limbs, two classical patterns of abnormal intermuscular coordination are the coupling of shoulder abduction and elbow flexion (termed 'flexor synergy’) and the coupling of shoulder adduction and elbow extension (called 'extensor synergy’) [1, 2]. Previous studies have reported that abnormal intermuscular coordination produces the reduction of reaching distance and the horizontal work area of the hand [3,4,5] as well as the torque coupling between upper limb joints [3, 6].
Intermuscular coordination has been quantitatively evaluated in the form of muscle synergies for the last few decades. According to the muscle synergy hypothesis, the human body simplifies intermuscular coordination to manipulate the numerous degrees of freedom in the musculoskeletal system by modulating the activation of a limited number of muscle synergies (i.e., consistent co-activation patterns of muscle groups) rather than by controlling individual muscles. The information obtained from muscle synergy analysis includes the number, composition, and activation coefficients of muscle synergies. The number of muscle synergies indicates the complexity of intermuscular coordination. The composition of muscle synergies quantifies the muscles that are co-activated to achieve specific motor goals required for the given motor tasks, whereas the activation coefficient indicates the timing and activation magnitude of the synergies. From the perspective of data analysis, note that the muscle synergy patterns can be affected by biomechanical task constraints, selected muscles, and specification of electromyographic (EMG) data processes such as filtering and scaling [7,8,9].
How a stroke alters muscle synergies under varying biomechanical task constraints must be investigated to understand the impact of a stroke on neuromuscular control because intermuscular coordination can be affected by task constraints. Various motor tasks can be applied for upper limb rehabilitation depending on whether the training is focused on restoring the movement pattern or strength and on the external constraints applied to the trainee. We define an external constraint as the physical interaction between the trainee and the rehabilitative device, which is designed to provide an assistive or resistive force to or restrict the movement of the trainee. If no contact exists between the trainee and the device (i.e., a task has to be performed in free space) or if the device is compliant enough to ignore the interaction, then the task can be considered as unconstrained. Biomechanical task constraints used for upper limb rehabilitation can be categorized roughly as follows: unconstrained movement in free space, constrained movement assisted or resisted by a mechanical device, static (isometric) strengthening, and dynamic strengthening during movement. These task constraints can also be adopted for the training of intermuscular coordination; therefore, investigation of intermuscular coordination across various motor tasks is also important for developing effective training strategies for intermuscular coordination.
Different mechanisms of post-stroke changes in intermuscular coordination underlying shoulder and elbow joints have been reported for the following task constraints: free movement [10, 11], constrained (particularly, assisted) movement [12,13,14], and static strengthening [15, 16] (see Table 1). When stroke survivors performed free movements with their affected upper limbs, a higher number of muscles were activated together as a synergistic muscle group compared with the muscles of the unaffected limbs [10, 11]. The increased coupling between muscles was interpreted as the ‘merging’ of the two or more intact muscle synergies, and the extent of merging was proportionally correlated with the level of motor impairment [10]. In addition, merging could reduce the number of muscle synergies (i.e., reduce the complexity of intermuscular coordination) from five to one [11]. Furthermore, the complexity of intermuscular coordination was also reduced in free gait [17] and static strengthening using the hand and wrist at unconstrained (i.e., self-selected) postures [18]. In contrast, when static strengthening was performed using the shoulder and elbow under postural constraint (i.e., controlled upper limb posture), intermuscular coordination of neurologically intact controls and three-stroke groups with varying severity of motor impairment (i.e., mild, moderate, and severe) was explained with the same number of muscle synergies [15, 16]. While the composition of the synergies was comparable across all groups in general, a stroke induced changes in the composition of shoulder-related synergies mainly because of the co-activation of the three heads of the deltoid muscle. The prevalence of altered shoulder-related synergies increased under isometric conditions as the severity of motor impairment increased after a stroke.
Previous studies focusing on post-stroke patients suggest that the characteristics of intermuscular coordination, underlying the movement performed in support of external devices, can be different from those evaluated in free space after a stroke. The number and composition of muscle synergies during assisted horizontal or three-dimensional reaching tasks were comparable between stroke survivors and neurologically intact individuals; however, increased coupling of the deltoid muscles affected the composition of the shoulder-related synergies in the stroke group [12, 14]. When the three-dimensional reaching task of the affected limb was supported by weight supporters or therapeutic robots, the expression of the abnormal synergistic pattern of the shoulder muscles including deltoid muscles was reduced compared to when no assistance was provided [13, 14]. The motor deficit during the assisted reaching task after a stroke was mainly caused by the alteration of the activation coefficients of muscle synergies instead of the number and the composition of muscle synergies [12].
While previous studies have addressed upper limb intermuscular coordination that underlies free, constrained, and supported movement and static strengthening after a stroke, to the best of our knowledge, upper limb intermuscular coordination of dynamic strengthening tasks post stroke has not been investigated thus far. Isokinetic movement, which is a type of dynamic strengthening task, has been adopted for the restoration of motor capability as well as evaluation for stroke rehabilitation [19, 20]. In addition, few previous studies reported that isokinetic exercise improved upper limb motor function rated by the Fugl-Meyer assessment or box and block test and kinematic characteristics such as movement time and peak velocity [21, 22]. Thus, isokinetic movement has potential advantages during training for intermuscular coordination. Exercise at a controlled speed within the limited range of motion can prevent secondary muscle injury. In addition, it was reported that isokinetic movement promotes the activation of agonist muscles without provoking co-contraction of antagonist muscles [23]. Thus, the characterization of intermuscular coordination during isokinetic movements can provide a scientific foundation to design intermuscular coordination-based training strategies to improve the motor function of stroke survivors.
In our current study, we investigated the characteristics of upper limb intermuscular coordination of chronic stroke survivors during three-dimensional linear isokinetic movements. In addition to differences in the isokinetic muscle synergies between stroke survivors and neurologically intact people, we also evaluated how the characteristics of the stroke-affected isokinetic muscle synergies (such as the number of muscle synergies, synergy composition and activation profile after stroke with respect to those of control synergies) varies according to the level of motor impairment. Constraining the trajectory of the end-point of the upper limb on linear paths allowed stroke participants and healthy controls to achieve comparable end-point trajectories, while variations in joint kinematics caused by the differences in intermuscular coordination were still expressed. We expected that matching of end-point trajectories between the stroke and control groups would reduce undesired variations of the intermuscular coordination caused by differences in motion. By comparing the findings of this study with those of previous literature, we discussed how intermuscular coordination was affected by a stroke under various external biomechanical constraints. We also addressed how isokinetic task constraints can be adopted for training of intermuscular coordination in the stroke-affected upper limb. Specifically, stroke survivors and neurologically intact controls were recruited to perform eight upper limb movements in the three-dimensional space. Their muscle synergies underlying the activities of shoulder and elbow muscles as well as the end-point forces were analyzed. Correlations between alterations of muscle synergies and the level of motor impairment were examined.
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