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Levin, M. F., Berman, S., Weiss, N., Parmet, Y., Banina, M. C., Frenkel-Toledo, S., et al. (2023). ENHANCE proof-of-concept three-arm randomized trial: effects of reaching training of the hemiparetic upper limb restricted to the spasticity-free elbow range (Vol. 13).
Abstract: Post-stroke motor recovery processes remain unknown. Timescales and patterns of upper-limb (UL) recovery suggest a major impact of biological factors, with modest contributions from rehabilitation. We assessed a novel impairment-based training motivated by motor control theory where reaching occurs within the spasticity-free elbow range. Patients with subacute stroke (</= 6 month; n = 46) and elbow flexor spasticity were randomly allocated to a 10-day UL training protocol, either personalized by restricting reaching to the spasticity-free elbow range defined by the tonic stretch reflex threshold (TSRT) or non-personalized (non-restricted) and with/without anodal transcranial direct current stimulation. Outcomes assessed before, after, and 1 month post-intervention were elbow flexor TSRT angle and reach-to-grasp arm kinematics (primary) and stretch reflex velocity sensitivity, clinical impairment, and activity (secondary). Results were analyzed for 3 groups as well as those of the effects of impairment-based training. Clinical measures improved in both groups. Spasticity-free range training resulted in faster and smoother reaches, smaller (i.e., better) arm-plane path length, and closer-to-normal shoulder/elbow movement patterns. Non-personalized training improved clinical scores without improving arm kinematics, suggesting that clinical measures do not account for movement quality. Impairment-based training within a spasticity-free elbow range is promising since it may improve clinical scores together with arm movement quality.Clinical Trial Registration: URL: http://www.clinicaltrials.gov . Unique Identifier: NCT02725853; Initial registration date: 01/04/2016.
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Davidowitz, I., Parmet, Y., Frenkel-Toledo, S., Banina, M. C., Soroker, N., Solomon, J. M., et al. (2019). Relationship Between Spasticity and Upper-Limb Movement Disorders in Individuals With Subacute Stroke Using Stochastic Spatiotemporal Modeling. Neurorehabil Neural Repair, 33(2), 141–152.
Abstract: BACKGROUND: Spasticity is common in patients with stroke, yet current quantification methods are insufficient for determining the relationship between spasticity and voluntary movement deficits. This is partly a result of the effects of spasticity on spatiotemporal characteristics of movement and the variability of voluntary movement. These can be captured by Gaussian mixture models (GMMs). OBJECTIVES: To determine the influence of spasticity on upper-limb voluntary motion, as assessed by the bidirectional Kullback-Liebler divergence (BKLD) between motion GMMs. METHODS: A total of 16 individuals with subacute stroke and 13 healthy aged-equivalent controls reached to grasp 4 targets (near-center, contralateral, far-center, and ipsilateral). Two-dimensional GMMs (angle and time) were estimated for elbow extension motion. BKLD was computed for each individual and target, within the control group and between the control and stroke groups. Movement time, final elbow angle, average elbow velocity, and velocity smoothness were computed. RESULTS: Between-group BKLDs were much larger than within control-group BKLDs. Between-group BKLDs for the near-center target were lower than those for the far-center and contralateral targets, but similar to that for the ipsilateral target. For those with stroke, the final angle was lower for the near-center target, and the average velocity was higher. Velocity smoothness was lower for the near-center than for the ipsilateral target. Elbow flexor and extensor passive muscle resistance (Modified Ashworth Scale) strongly explained BKLD values. CONCLUSIONS: Results support the view that individuals with poststroke spasticity have a velocity-dependent reduction in active elbow joint range and that BKLD can be used as an objective measure of the effects of spasticity on reaching kinematics.
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Frenkel-Toledoa, S., Bentin, S., Perry, A., Liebermann, D. G., & Soroker, N. (2014). Mirror-neuron system recruitment by action observation: Effects of focal brain damage on mu suppression. NeuroImage, 87, 127–137.
Abstract: Mu suppression is the attenuation of EEG power in the alpha frequency range (8-12 Hz), recorded over the sensorimotor cortex during execution and observation of motor actions. Based on this dual characteristic it is thought to signalize activation of a human analogue of the mirror neuron system (MNS) found in macaque monkeys, though much uncertainty remains concerning its specificity and full significance. To further explore the hypothesized relationship between mu suppression and MNS activation, we investigated how it is affected by damage to cortical regions, including areas where the MNS is thought to reside. EEG was recorded in 33 first-event stroke patients during observation of video-clips showing reaching and grasping hand movements. We examined the modulation of EEG oscillations at central and occipital sites, and analyzed separately the lower (8-10 Hz) and higher (10-12 Hz) segments of the alpha/mu range. Suppression was determined relative to observation of a non-biological movement. Normalized lesion data were used to investigate how damage to regions of the fronto-parietal cortex affects the pattern of suppression. The magnitude of mu suppression during action observation was significantly reduced in the affected hemisphere compared to the unaffected hemisphere. Differences between the hemispheres were significant at central (sensorimotor) sites but not at occipital (visual) sites. Total hemispheric volume loss did not correlate with mu suppression. Suppression in the lower mu range in the unaffected hemisphere (C3) correlated with lesion extent within the right inferior parietal cortex. Our lesion study supports the role of mu suppression as a marker of MNS activation, as suggested by findings gathered in previous studies in normal subjects.
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Lackritz, H., Parmet, Y., Frenkel-Toledo, S., Banina, M. C., Soroker, N., Solomon, J. M., et al. (2021). Effect of post-stroke spasticity on voluntary movement of the upper limb. J Neuroeng Rehabil, 18(1), 81.
Abstract: BACKGROUND: Hemiparesis following stroke is often accompanied by spasticity. Spasticity is one factor among the multiple components of the upper motor neuron syndrome that contributes to movement impairment. However, the specific contribution of spasticity is difficult to isolate and quantify. We propose a new method of quantification and evaluation of the impact of spasticity on the quality of movement following stroke. METHODS: Spasticity was assessed using the Tonic Stretch Reflex Threshold (TSRT). TSRT was analyzed in relation to stochastic models of motion to quantify the deviation of the hemiparetic upper limb motion from the normal motion patterns during a reaching task. Specifically, we assessed the impact of spasticity in the elbow flexors on reaching motion patterns using two distinct measures of the 'distance' between pathological and normal movement, (a) the bidirectional Kullback-Liebler divergence (BKLD) and (b) Hellinger's distance (HD). These measures differ in their sensitivity to different confounding variables. Motor impairment was assessed clinically by the Fugl-Meyer assessment scale for the upper extremity (FMA-UE). Forty-two first-event stroke patients in the subacute phase and 13 healthy controls of similar age participated in the study. Elbow motion was analyzed in the context of repeated reach-to-grasp movements towards four differently located targets. Log-BKLD and HD along with movement time, final elbow extension angle, mean elbow velocity, peak elbow velocity, and the number of velocity peaks of the elbow motion were computed. RESULTS: Upper limb kinematics in patients with lower FMA-UE scores (greater impairment) showed greater deviation from normality when the distance between impaired and normal elbow motion was analyzed either with the BKLD or HD measures. The severity of spasticity, reflected by the TSRT, was related to the distance between impaired and normal elbow motion analyzed with either distance measure. Mean elbow velocity differed between targets, however HD was not sensitive to target location. This may point at effects of spasticity on motion quality that go beyond effects on velocity. CONCLUSIONS: The two methods for analyzing pathological movement post-stroke provide new options for studying the relationship between spasticity and movement quality under different spatiotemporal constraints.
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Frenkel-Toledo, S., Bentin, S., Perry, A., Liebermann, D. G., & Soroker, N. (2013). Dynamics of the EEG Power in the Frequency and Spatial Domains During Observation and Execution of Manual Movements. Brain Res, 1509, 43–57.
Abstract: Mu suppression is the attenuation of EEG power in the alpha frequency range (8-12Hz) while executing or observing a motor action. Whereas typically observed at central scalp sites, there are diverging reports about the extent of the attenuation over the cortical mantle, its exact frequency range and the specificity of this phenomenon. We investigated the modulation of EEG oscillations in frequency-bands from 4 to 12Hz at frontal, central, parietal and occipital sites during the execution of manual movements and during observation of similar actions from allocentric (i.e., facing the actor) and egocentric (i.e., seeing the actor from behind) viewpoints. Suppression was determined relative to observation of a non-biological movement. Action observation elicited greater suppression in the lower (8-10Hz) compared to the higher mu range (10-12Hz), and greater suppression in the entire 4-12Hz range at frontal and central sites compared to parietal and occipital sites. In addition, suppression tended to be greater during observation of a motor action from allocentric compared to egocentric viewpoints. During execution of movement, suppression of the EEG occurred primarily in the higher alpha range and was absent at occipital sites. In the theta range (4-8Hz), the EEG amplitude was suppressed during action observation and execution. The results suggest a functional distinction between modulation of mu and alpha rhythms, and between the higher and lower ranges of the mu rhythms. The activity of the presumed human mirror neuron system seems primarily evident in the lower mu range and in the theta range.
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