Submitted as:
de Kam D, Geurts AC, Weerdesteyn V, Torres-Oviedo G. Deficient motor modules on the paretic side result in direction-specific postural instability after stroke.
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ABStrACt
Postural instability is a risk factor for falls in people after stroke. Defective muscle coordination of balance recovery responses may contribute to their greater fall risk. We investigated the association between postural response coordination deficits identified by muscle synergy analysis and perturbation-induced body sway in stroke survivors. Ten people after unilateral stroke (> 6 months) and 9 healthy controls were subjected to translational balance perturbations in 12 directions resulting in a feet-in-place balance correcting response. Activity of eight muscles was recorded bilaterally: erector spinae, gluteus medius, biceps femoris, semitendinosis, soleus, rectus femoris, peroneus and tibialis anterior. We extracted motor modules for each leg using nonnegative matrix factorization on the initial muscle activity (3 consecutive 75 ms time bins) following the first onset of activity. We also determined perturbation-induced body sway using a single-link inverted pendulum model. We used a repeated measures general linear model to compare the activation of motor modules that we identified in stroke survivors and controls to pinpoint abnormal directional tuning of postural responses. While three motor modules (W1-W3) were consistently found in healthy controls, some of these motor modules were either absent or abnormally activated in the paretic legs of stroke survivors. Specifically, motor module W3 (hamstrings and erector spinae, peroneus), which responded to forward body perturbations, was missing in 4 out of 10 paretic legs. Consequently, forward perturbations induced larger body sway in individuals without W3 than in those with it (p=0.02). Another deficit in the paretic legs of stroke survivors was the abnormally low initial activity of W2 (tibialis anterior, peroneus and rectus femoris), which responded to posterolateral body perturbations (p<0.05). Accordingly, the lower initial W2 activity was strongly associated with increased body sway following posterolateral perturbations (R2=0.68, p<0.01). Lastly, the deficits in muscle coordination were heterogene-ously distributed across people after stroke, indicating that they suffered from distinct deficiencies in muscle coordination. In conclusion, we identified specific stroke-related deficits in muscle coordination of postural responses that each resulted in a pattern of direction-specific postural instability. The heterogeneous distribution of these deficits across patients suggests that different pathophysiolo-gical mechanisms underlie each of the deficits. The deficits in paretic W2 and W3 hint at involvement of cerebral structures in activating these motor modules. In addition, identifying patient-specific postural control deficits is crucial for the deve-lopment of targeted interventions to improve postural stability in stroke survivors.
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Proper balance control is essential for mobility and activities of daily living.26,79,139,158,254
When balance is perturbed, fast ‘automatic’ postural muscle responses APRs are the first line of defense to prevent a fall. These postural responses are highly coordinated and tuned to the direction of the balance perturbation.106,285,286 Studies in cats have demonstrated that the brainstem harbors the circuitry for these responses.112,267 In ad-dition, cerebral structures seem to play a role as well, given the pronounced postural response deficits after lesions of one of the cerebral hemispheres.176,179 It is not yet fully understood how these cerebral structures are involved in postural control.131,167
The role of cerebral structures in postural responses can be studied using stroke as a disease model. People with stroke demonstrate smaller and later postural responses to balance perturbations compared to healthy individuals.10,11,145,146,176 Delays in postural responses are, however, not the same for all muscles, indicating that coordination of postural responses is disrupted after stroke.145,176 Moreover, postural response deficits affect stroke survivors differently, due to the known heterogeneity of the disease.145 With conventional EMG (electromyography) analysis techniques, it is difficult to capture the distinct muscle coordination deficits that can exist after stroke, as those techniques typically assess activity of individual muscles. Hence, more advanced analytical tools are needed to quantify deficits in activation across different muscles.
In this study, we will use muscle synergy or motor module analysis to characterize stroke-related muscle coordination deficits of both the early APR and later postural response components. With this technique, factorization algorithms are used to identify groups of muscles (motor modules) that are co-activated.251,280,281 Each motor module serves a distinct biomechanical function, thereby allowing for the study of functional consequences of stroke-related muscle coordination deficits.285 Previous studies have used this technique in gait and upper extremity tasks and found that particularly the more severely affected stroke survivors had fewer independently controlled motor modules.4,47,51 This may underlie the reduced flexibility of motor output after stroke.47 It is unknown, however, how stroke affects motor modules for postural control.
In the present study, we aimed to identify stroke-related deficits in motor modules used for postural responses and their functional consequences. We hypothesized that people with stroke would demonstrate deficits in structure of motor modules as well as in their temporal recruitment. We also hypothesized these deficits to be heterogeneously distri-buted across individuals with supratentorial stroke with each deficit resulting in a distinct
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pattern of direction-specific postural instability. Taking into account these individual deficits is crucial for the development of targeted balance rehabilitation interventions.