Research ReportTiming variability of reach trajectories in left versus right hemisphere stroke
Highlights
► Trajectory timing variability was studied in right and left brain strokes and healthy controls. ► Stroke survivors showed higher timing variability of both paretic and non-paretic arms compared to controls. ► The non-paretic arm of left hemisphere strokes and the left arm of controls had higher timing variability than the other arm. ► Target uncertainty increased timing variability except for the dominant arm of controls. ► Results were generally consistent with the left hemisphere's presumed greater role in trajectory formation.
Introduction
Individuals recovering from a cerebrovascular accident (CVA) frequently exhibit motor impairments of the paretic arm that limit their performance of activities of daily living, such as reaching to grasp an object. Movements of the paretic limb typically are slow and less smooth than those of healthy individuals, with increased variability of hand trajectories (Archambault et al., 1999, Levin, 1996). These characteristics of upper limb movements result from larger and less coordinated joint variations compared to healthy control individuals (Levin, 1996, Reisman and Scholz, 2006).
Many studies also have reported motor deficits of the non-paretic arm (Haaland et al., 2004, Kwon et al., 2007, Schaefer et al., 2007, Winstein and Pohl, 1995) that frequently affect motor timing. For example, in a tapping task, individuals with a left-sided stroke showed higher variability of the inter-tap interval with their left arm compared to the corresponding control individuals (Kwon et al., 2007). In contrast, persons with a right hemisphere stroke did not show this deficit when performing with their right arm, suggesting that the left hemisphere may play a bigger role in the control of movement timing. Schaefer et al. (2007) reported that persons with a right CVA had reduced modulation of acceleration duration and substantial errors in final position when performing targeted single joint elbow movements with their non-paretic limb. In contrast, left CVA survivors showed reduced modulation of acceleration amplitude but had fewer final position errors. Robertson and Roby-Brami (2011) reported differences between stroke victims with right and left hemisphere lesions in the coordination of trunk and arm movements during reaching. The above findings reinforce previously reported hemispheric specializations for controlling different aspects of movements (Elliott, 1985, Haaland and Delaney, 1981, Harrington and Haaland, 1991, Lavrysen et al., 2003, Todor and Doane, 1978).
Most studies of hemispheric differences have investigated tasks in which only a small number of joints were involved. Only a few studies have examined reaching movements that involved a large number of degrees of freedom of joint motion (Cirstea and Levin, 2007, Levin, 1996, Levin et al., 2002, Michaelsen et al., 2001, Reisman and Scholz, 2003, Reisman and Scholz, 2006). For example, Levin's group (Cirstea et al., 2003) was one of the first groups to quantitatively study coordination deficits among arm joints in persons following a stroke. Reisman and Scholz (2003) investigated differences between mildly paretic, left hemisphere stroke survivors and healthy persons in their joint coordination for reaching, using the Uncontrolled Manifold (UCM; Scholz and Schöner, 1999) approach to partition joint variance into ‘good’ variance (flexible combinations of joints across repetitions that led to a stable hand path) and ‘bad’ variance, which leads to hand path variability. They reported that stroke survivors actually exhibited more ‘good’ variance than did healthy controls when reaching to targets. However, the stroke survivors also showed less effective decoupling of joint space such that ‘bad’ joint configuration variance was significantly larger than for control subjects, leading to more hand path variability. These studies were limited to the study of persons with left hemisphere lesions, however.
Freitas and Scholz (2009) recently reported in young healthy individuals that the use of flexible patterns of joint coordination to produce a consistent hand path increased when the target of reaching could suddenly change location after reach onset compared to reaching to a fixed target, suggesting that movement planning can affect the use of motor abundance. The question of how movement planning affects the use of motor abundance in persons who have suffered a stroke currently is under investigation by our group. Preliminary results indicate that, as with healthy individuals, stroke survivors show more ‘good’ variance than bad variance related to the reach trajectories although they have higher bad variance than healthy controls. Therefore, they have higher overall task variable variability. However, this typical UCM variance analysis is based on positional variability at each point in a movement trajectory and does not address directly movement timing. Thus, a question that has not been investigated previously in multi-joint reaching is whether and to what extent the timing of reaches is affected when the target position is uncertain and whether lesions to different hemispheres affect movement timing under conditions of uncertainty. Haaland et al. (2004) studied the effect of target uncertainty on temporal events of reaching in person post stroke using the double-step paradigm. The authors observed longer reaction time and movement time for individuals that suffered a left hemisphere stroke compared to healthy adults whether the target location was certain or uncertain. However, when stroke survivors had to change direction with their left hand to acquire a target that had jumped, their movement was slower than for controls reaching with the same arm. In contrast, comparisons of temporal measures between healthy individuals and right hemisphere stroke survivors revealed non-significant differences related to target conditions.
It has been suggested that the brain is lateralized for the organization of time-domain characteristics of sequential action, but not for the metrical scaling of parameters of force production (Walter and Swinnen, 1990). Studies comparing movement timing characteristics between individuals with left and right brain lesions suggested a right hemisphere specialization for the timing of discrete, distal limb movements (Harrington et al., 1998) or left hemisphere specialization for sequential movements related to whole limb tapping (Winstein and Pohl, 1995). In addition, one study of movements involving trunk motion suggested that both hemispheres contribute to the temporal coordination of the body segments (Esparza et al., 2003). Uncertainty about hemispheric specialization in the literature is likely due to the different tasks used to evaluate movement timing as well as the different events investigated and the involvement of a different number of degrees of freedom.
Most studies that have investigated deficits of movement timing after brain lesions have focused on the temporal characteristics of individual events such as reaction time, movement time or time to peak velocity (Chang et al., 2008, Dipietro et al., 2007, Dipietro et al., 2009, Haaland et al., 2004, Harrington et al., 1998). However, such events are often difficult to identify in individual joint movements of persons with stroke due to the large number of movement subunits they exhibit (Dipietro et al., 2007, Dipietro et al., 2009). Thies et al. (2009) proposed a new method to quantify movement timing variability that includes the entire trajectory rather than individual timing events. This method has been used recently to compute timing characteristics of the upper limb motion during two functional tasks (drinking and moving a plate) in healthy individuals and stroke survivors. Overall, the authors found greater trajectory timing variability for the stroke group compared to control individuals, and these differences were larger for the unilateral task. That study only investigated the paretic limb, however, and did not report on performance differences between left and right hemisphere strokes (Thies et al., 2009).
The current study extends the work of Thies et al. (2009) by considering trajectory timing differences of the non-paretic as well as paretic arm, differences between individuals with right and left hemisphere strokes, the influence of planning for differences in task requirements, and by extending the analysis to joint trajectories. Stroke survivors and healthy, age-matched adults performed reaching towards either certain (fixed) and uncertain targets. Based on the Thies et al. (2009) study of trajectory timing variability of hand accelerations, we hypothesized to find greater timing variability for stroke survivors compared to the control group, but for the non-paretic as well as paretic arms. We also hypothesized that trajectory timing variability would be larger for persons with left-hemisphere lesions. A set of different combinations of arm joint accelerations could lead to same resultant hand acceleration. Thus, in the present study, the timing variability analysis was applied to the hand paths as well as joint motions. By examining timing variability of each joint, it was possible to investigate how the temporal involvement of each joint (across time) was affected by the brain lesion.
Section snippets
Results
Fig. 1 presents the time series of twenty resultant hand acceleration profiles from a representative participant from each group (RCVA, LCVA and control), reaching with the left and right arm [respectively, left and right panels of Fig. 1A–C; in the case of the stroke survivors, the panels are also represented as the arm ipsilateral (non-paretic) or contralateral (paretic) to the lesion]. These trajectories were time-normalized to 100% only for purposes of illustration. However, the
Discussion
In the current study, a novel method for examining the temporal variability of movement trajectories of arm reaching by computing the warping cost (Thies et al., 2009) was used to identify differences among persons with right and left hemisphere lesions and age-matched control subjects. This method provides the advantage of evaluating the correspondence of the entire reach trajectory across multiple reaches, not only the timing of individual events during the movement (e.g., time to reach the
Participants
Twenty-two individuals, 40–85 years old, twelve participants with a single left-brain stroke (LCVA) and ten participants with a single right-brain stroke (RCVA) more than 3 months prior to the study, participated. All stroke survivors performed the task with their paretic limb first, followed by their non-paretic limb. A summary of the stroke participant's characteristics is presented in Table 4. Thirteen age-matched control adults (9 females; 64 ± 5.77 years old) without brain damage also
Acknowledgments
The project described was supported by grant number NS050880 from the National Institute of Neurological Disorders and Stroke. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Neurological Disorders and Stroke or the National Institutes of Health, which had no part in the study design or implementation, or in the writing of this manuscript. The authors are grateful to Dr. Sibylle Thies of The University of
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2019, Human Movement ScienceCitation Excerpt :Hence, it was expected that the LCVA individuals should present more deficits in the movement trajectory (i.e., greater hand trajectory) compared to RCVA or healthy individuals. The hypotheses in function of the side of the brain lesion on the temporal and spatial characteristics of the movements are related to a specialization of the right hemisphere in movement planning, and the left hemisphere in movement execution (de Paiva Silva, Freitas, Silva, Banjai, & Alouche, 2014; Freitas, Gera, & Scholz, 2011; Schaefer, Haaland, & Sainburg, 2009). Note that the findings from previous studies about the specific role of each brain hemisphere on the control of arm movements were based on the performance of the alterations of the ipsilesional arm movements of stroke individuals in sitting position.
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2017, Journal of Stroke and Cerebrovascular DiseasesCitation Excerpt :Tretriluxana et al observed that individuals who had a stroke in their right brain hemisphere had greater difficulty in transporting their ipsilesional hands in space when compared with individuals who had an injury in the left hemisphere, taking longer to accomplish a reach-to-grasp task.7 Similarly, stroke individuals with a right brain damage (RBD) present deficits in controlling their hand's final position,1,3,8,9 which would affect the performance in tasks that require precision and fine hand control. Few studies examined the effect of the side of brain lesion on hand and digits dexterity.