Timing variability of reach trajectories in left versus right hemisphere stroke

Abstract

This study investigated trajectory timing variability in right and left stroke survivors and healthy controls when reaching to a centrally located target under a fixed target condition or when the target could suddenly change position after reach onset. Trajectory timing variability was investigated with a novel method based on dynamic programming that identifies the steps required to time warp one trial's acceleration time series to match that of a reference trial. Greater trajectory timing variability of both hand and joint motions was found for the paretic arm of stroke survivors compared to their non-paretic arm or either arm of controls. Overall, the non-paretic left arm of the LCVA group and the left arm of controls had higher timing variability than the non-paretic right arm of the RCVA group and right arm of controls. The shoulder and elbow joint warping costs were consistent predictors of the hand's warping cost for both left and right arms only in the LCVA group, whereas the relationship between joint and hand warping costs was relatively weak in control subjects and less consistent across arms in the RCVA group. These results suggest that the left hemisphere may be more involved in trajectory timing, although the results may be confounded by skill differences between the arms in these right hand dominant participants. On the other hand, arm differences did not appear to be related to differences in targeting error. The paretic left arm of the RCVA exhibited greater trajectory timing variability than the paretic right arm of the LCVA group. This difference was highly correlated with the level of impairment of the arms. Generally, the effect of target uncertainty resulted in slightly greater trajectory timing variability for all participants. The results are discussed in light of previous studies of hemispheric differences in the control of reaching, in particular, left hemisphere specialization for temporal control of reaching movements.

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.