Abstract

The brain processes involved in the restoration of motor skill after hemiparetic stroke are not fully understood. The current study compared cortical activity in chronic stroke patients who successfully recovered hand motor skill and normal control subjects during performance of kinematically matched unskilled and skilled hand movements using functional magnetic resonance imaging. We found that cortical activation during performance of the unskilled movement was increased in the patients relative to controls in the contralesional primary sensorimotor cortex. Performance of the skilled movement elicited increased activation in the patients relative to controls in the contralesional primary sensorimotor cortex, ventral premotor cortex, supplementary motor area/cingulate, and occipitoparietal cortex. Further, the activation change in the contralesional occipitoparietal cortex was greater in the patients relative to controls with the increase in motor skill challenge. Kinematic differences, mirror movements, and residual motor deficits did not account for the enhanced activation in the contralesional cortices in the patients. These results suggest that activation in the contralesional cortical network was enhanced as a function of motor skill challenge in stroke patients with good motor recovery. The findings of the current study suggest that successful recovery of motor skill after hemiparetic stroke involves participation of the contralesional cortical network.

cerebral ischemia, functional recovery, motor tasks, MRI/fMRI, neuroplasticity
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Introduction

Stroke often causes hemiparesis due to direct damage and/or secondary functional disruption of brain areas controlling movement. Recovery of motor function, when it occurs, typically starts with regaining limb synergies characterized by gross, undifferentiated movements of the stroke-affected limb (Twitchell 1951; Brunnstrom 1966). Recovery may proceed by regaining the ability to perform skilful, nonsynergistic limb movements in which intralimb joints can be controlled independently. Recovery of hand motor function also follows this trajectory, with early restoration of synergistic movements in which the digits can grasp and release in unison and later restoration of dexterous, nonsynergistic movements in which the digits can be moved independent of one another. Recovery of nonsynergistic hand movements is critical to functional use of the hand in daily activities, such as tool usage and object manipulation.

The changes in brain activity mediating recovery of motor function after stroke are beginning to be unraveled. Early after hemiparetic stroke in patients, performance of a gripping task (i.e., a synergistic movement) by the affected hand has been shown to increase activity in several cortices within the ipsilesional and contralesional hemispheres to a greater degree than in normal control subjects (Ward et al. 2003a). Progressive normalization of cortical activity elicited by hand gripping appears to occur during the recovery process in stroke patients (Ward et al. 2003a). Further, cortical activity associated with hand gripping in chronic stroke patients with good motor recovery has been shown to be indistinguishable from that in normal controls (Ward et al. 2003b). In contrast, during index finger or sequential finger tapping (i.e., nonsynergistic movements), cortical activity in chronic stroke patients with good motor recovery has been observed to be enhanced relative to that in normal controls, most commonly in the primary motor cortex, premotor cortex, and parietal cortex of the contralesional hemisphere (Chollet et al. 1991; Weiller et al. 1993; Cramer et al. 1997; Cao et al. 1998; Foltys et al. 2003; Gerloff et al. 2006; Lotze et al. 2006). These observations suggest that differences in motor task–related cortical activity between well-recovered stroke patients and normal controls are more pronounced as the skill demanded by the motor task is increased. However, the relationship between cortical activity and motor skill challenge in stroke patients has not been tested directly. This is partly due to previous studies, with the exception of a few, having stroke patients perform only a single motor task, either synergistic or nonsynergistic. In the few studies in which more than one motor task was performed (Cramer et al. 2001; Foltys et al. 2003; Nair et al. 2007), comparison between resultant activation patterns was confounded by the tasks not being matched for kinematic parameters of performance (e.g., force, amplitude, frequency, range of motion, number of body segments moved, and which body segments moved).

The purpose of the current study was to gain insight into the cortical processes involved in the restoration of motor skill after stroke. To meet this goal, cortical activity in chronic stroke patients who successfully recovered motor skill was compared with that in normal control subjects using functional magnetic resonance imaging (fMRI). The fMRI was conducted while the subjects performed a pair of kinematically matched hand motor tasks that were developed by Ehrsson et al. (2002) to examine differences in the neural control of synergistic versus nonsynergistic movements in normal healthy subjects. The synergistic task involved movement of all 5 digits in unison, whereas the nonsynergistic task involved independent movement of the thumb relative to the unified movement of the other 4 digits. As the nonsynergistic task involved independent digit movement, this task required more skill than the synergistic task. Understanding the effect of motor skill challenge on cortical activation in stroke patients could ultimately lead to the development of interventions aimed at maximizing motor recovery after hemiparetic stroke.