Abstract

We have proposed a model of motor lateralization, in which the left and right hemispheres are specialized for different aspects of motor control: the left hemisphere for predicting and accounting for limb dynamics and the right hemisphere for stabilizing limb position through impedance control mechanisms. Our previous studies, demonstrating different motor deficits in the ipsilesional arm of stroke patients with left or right hemisphere damage, provided a critical test of our model. However, motor deficits after stroke are most prominent on the contralesional side. Post-stroke rehabilitation has also, naturally, focused on improving contralesional arm impairment and function. Understanding whether contralesional motor deficits differ depending on the hemisphere of damage is, therefore, of vital importance for assessing the impact of brain damage on function and also for designing rehabilitation interventions specific to laterality of damage. We, therefore, asked whether motor deficits in the contralesional arm of unilateral stroke patients reflect hemisphere-dependent control mechanisms. Because our model of lateralization predicts that contralesional deficits will differ depending on the hemisphere of damage, this study also served as an essential assessment of our model. Stroke patients with mild to moderate hemiparesis in either the left or right arm because of contralateral stroke and healthy control subjects performed targeted multi-joint reaching movements in different directions. As predicted, our results indicated a double dissociation; although left hemisphere damage was associated with greater errors in trajectory curvature and movement direction, errors in movement extent were greatest after right hemisphere damage. Thus, our results provide the first demonstration of hemisphere specific motor control deficits in the contralesional arm of stroke patients. Our results also suggest that it is critical to consider the differential deficits induced by right or left hemisphere lesions to enhance post-stroke rehabilitation interventions.

lateralization, stroke, motor control, reaching movements, impairment
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Occasional Papers

Introduction

A large body of research has now established that the two cerebral hemispheres show a considerable degree of lateralization or a specialization for controlling different aspects of behaviour. Although such neural lateralization has been characterized primarily through studies of perceptual and cognitive processes, behavioural and neuroimaging studies have raised the possibility that the right and left hemispheres play different roles in the motor control of either arm. Based on our work in young healthy individuals, we have proposed a model of motor lateralization, in which each hemisphere has become specialized for different aspects of motor control, such that the ‘dominant/left’ hemisphere is critical for predicting limb and task dynamics, and the opposite, ‘non-dominant/right’ hemisphere is critical for specifying steady-state limb positions through impedance control mechanisms (see Sainburg, 2010 for a review). Our recent work in patients with unilateral brain damage (Schaefer et al., 2007, 2009a, b; Mutha et al., 2010, 2011a, b; Schaefer et al., 2012) and findings from other previous studies (Haaland and Harrington, 1989; Harrington and Haaland, 1991; Bernspang and Fisher, 1995; Winstein and Pohl, 1995; Haaland et al., 2004) have provided a confirmation for hemispheric specialization for movement control. For example, our study examining movement coordination in right-handed stroke patients (Schaefer et al., 2009b) showed a clear double dissociation between hemisphere status (healthy/hemisphere damage) and arm (right/left) for different features of movement. Patients with left hemisphere damage, but not right hemisphere damage, showed errors in direction and linearity of reaching movements that were associated with poor coordination of intersegmental dynamics. In contrast, patients with right hemisphere damage made well-coordinated and fairly straight movements, but they showed large and highly variable final position errors. In more recent studies, we have significantly expanded on these initial results by demonstrating differential deficits in motor adaptation and error correction mechanisms in left and right hemisphere damage stroke patients (Schaefer et al., 2009a; Mutha et al., 2011b; Schaefer et al., 2012). These studies have consistently revealed a deficit in predictive control after left hemisphere damage and final position control after right hemisphere damage, in line with the predictions of our model.

Our stroke studies were initiated as a critical test of this framework of hemispheric specialization for movement. We reasoned that if a hemisphere contributes its specialization to the movements of both arms, then motor deficits after damage to that hemisphere should be evident even if the ipsilesional arm in stroke patients is used to perform the task. Our studies, therefore, almost always required subjects to use their ipsilesional arm. However, given the crossed organization of the motor system, motor deficits after stroke are most prominent on the contralesional side. Therefore, most studies in stroke patients have, unsurprisingly, been dedicated to understanding the nature of these contralesional motor deficits. These studies have shown that although weakness and spasticity are common with contralesional hemiparesis (Bobath, 1990), discoordination is also a major problem, particularly during point-to-point reaching tasks. For example, Beer et al. (2000, 2004) demonstrated systematic direction errors and poor interjoint coordination with the contralesional arm in a 16-direction centre-out reaching task. In this task, all four directions comprised a quadrant in task space, and deficits were largest in the two quadrants where intersegmental coordination requirements were greatest. Similarly, Levin (1996) and Cirstea and Levin (2000) showed that when stroke patients made horizontal plane reaching movements with the paretic arm, their movements were characterized by high variability and poor synchrony between elbow and shoulder joint motions. In light of these significant contralesional deficits, motor rehabilitation after stroke has also focused on improving the functioning of the contralesional arm. In fact, newer therapeutic approaches, such as constraint-induced movement therapy (Taub et al., 1993; Mark and Taub, 2004), emphasize forced and repetitive use of the contralesional arm while also preventing use of the ipsilesional arm as a means to improve contralesional arm performance.

Despite such strong emphasis on understanding contralesional deficits and improving contralesional arm function, previous studies have not been coupled with the growing body of work that addresses hemispheric specificity for movement control mechanisms. One potential reason for this could be the concern that spasticity, weakness and variability in degree of impairment in the contralesional limb could mask any performance asymmetries. Nevertheless, understanding whether neural lateralization results in contralesional deficits that differ depending on the hemisphere of damage is of critical importance for assessing the impact of brain damage on function and also for designing rehabilitation protocols specific to the impaired limb. In this study, we ask whether the motor deficits in the contralesional arm of unilateral stroke patients reflect hemisphere-specific control mechanisms. Our model of lateralized control predicts clear differences in contralesional motor deficits depending on the laterality of stroke; therefore, this study also serves as a critical test of our model. We overcome the potential limitation of contralesional spasticity and reduced motor abilities by examining patients with only mild to moderate hemiparesis, defined by a score >45 (of a maximum possible 66) on the Fugl-Meyer Assessment of Upper Extremity Function.