Motor Task Difficulty and Brain Activity: Investigation of Goal-Directed Reciprocal Aiming Using Positron Emission Tomography

Abstract

Winstein, Carolee J., Scott T. Grafton, and Patricia S. Pohl. Motor task difficulty and brain activity: investigation of goal-directed reciprocal aiming using positron emission tomography. J. Neurophysiol. 77: 1581–1594, 1997. Differences in the kinematics and pattern of relative regional cerebral blood flow (rCBF) during goal-directed arm aiming were investigated with the use of a Fitts continuous aiming paradigm with three difficulty conditions (index of difficulty, ID) and two aiming types (transport vs. targeting) in six healthy right-handed young participants with the use of video-based movement trajectory analysis and positron emission tomography. Movement time and kinematic characteristics were analyzed together with the magnitude of cerebral blood flow to identify areas of brain activity proportionate to task and movement variables. Significant differences in rCBF between task conditions were determined by analysis of variance with planned comparisons of means with the use of group mean weighted linear contrasts. Data were first analyzed for the group. Then individual subject differences for the movement versus no movement and task difficulty comparisons were related to each individual subjects' anatomy by magnetic resonance imaging. Significant differences in rCBF during reciprocal aiming compared with no-movement conditions were found in a mosaic of well-known cortical and subcortical areas associated with the planning and execution of goal-directed movements. These included cortical areas in the left sensorimotor, dorsal premotor, and ventral premotor cortices, caudal supplementary motor area (SMA) proper, and parietal cortex, and subcortical areas in the left putamen, globus pallidus, red nucleus, thalamus, and anterior cerebellum. As aiming task difficulty (ID) increased, rCBF increased in areas associated with the planning of more complex movements requiring greater visuomotor processing. These included bilateral occipital, left inferior parietal, and left dorsal cingulate cortices—caudal SMA proper and right dorsal premotor area. These same areas showed significant increases or decreases, respectively, when contrast means were compared with the use of movement time or relative acceleration time, respectively, as the weighting factor. Analysis of individual subject differences revealed a correspondence between the spatial extent of rCBF changes as a function of task ID and the individuals' movement times. As task ID decreased, significant increases in rCBF were evident in the right anterior cerebellum, left middle occipital gyrus, and right ventral premotor area. Functionally, these areas are associated with aiming conditions in which the motor execution demands are high (i.e., coordination of rapid reversals) and precise trajectory planning is minimal. These same areas showed significant increases or decreases, respectively, when contrast means were compared with the use of movement time or relative acceleration time, respectively, as the weighting factor. A functional dissociation resulted from the weighted linear contrasts between larger (limb transport) or smaller (endpoint targeting) type amplitude/target width aiming conditions. Areas with significantly greater rCBF for targeting were the left motor cortex, left intraparietal sulcus, and left caudate. In contrast, those areas with greater rCBFassociated with limb transport included bilateral occipital lingual gyri and the right anterior cerebellum. Various theoretical explanations for the speed/accuracy tradeoffs of rapid aiming movements have been proposed since the original information theory hypothesis of Fitts. This is the first report to relate the predictable variations in motor control under changing task constraints with the functional anatomy of these rapid goal-directed aiming movements. Differences in unimanual aiming task difficulty lead to dissociable activation of cortical-subcortical networks. Further, these data suggest that when more precise targeting is required, independent of task difficulty, a cortical-subcortical loop composed of the contralateral motor cortex, intraparietal sulcus, and caudate is activated. This is consistent with the role of motor cortex for controlling direction of movement on the basis of population encoding.