Abstract
Motor lateralization in humans has primarily been characterized as “handedness”, resulting in the view that one arm-hemisphere system is specialized for all aspects of movement while the other is simply a weaker analogue. We have proposed an alternative view that motor lateralization reflects proficiency of each arm for complementary functions that arises from a specialization of each hemisphere for distinct movement control mechanisms. However, before this idea of hemispheric specialization can be accepted, it is necessary to precisely identify these distinct, lateralized mechanisms. Here we show in right-handers that dominant arm movements rely on predictive mechanisms that anticipate and account for the dynamic properties of the arm, while the non-dominant arm optimizes positional stability by specifying impedance around equilibrium positions. In a targeted-reaching paradigm, we covertly and occasionally shifted the hand starting location either orthogonal to or collinear with a particular direction of movement. On trials on which the start positions were shifted orthogonally, we did not notice any strong interlimb differences. However, on trials on which start positions were shifted orthogonally, the dominant arm largely maintained the direction and straightness of its trajectory, while the non-dominant arm deviated towards the previously learned goal position, consistent with the hypothesized control specialization of each arm-hemisphere system. These results bring together two competing theories about mechanisms of movement control, and suggest that they coexist in the brain in different hemispheres. These findings also question the traditional view of handedness, because specialized mechanisms for each arm-hemisphere system were identified within a group of right-handers. It is likely that such hemispheric specialization emerged to accommodate increasing motor complexity during evolution.
Highlights
The modern view of brain lateralization, built upon early work in patients with unilateral brain damage and more recent work in split-brain patients [1,2], suggests that each cerebral hemisphere has become specialized for different, but complementary control processes that together govern a particular behavior
Distance and final position errors tended to be slightly, but statistically significantly, greater in the non-dominant arm compared to the dominant arm
Based on our previous results, we have developed a framework of motor lateralization, termed ‘‘dynamic dominance’’ [34], and put forth the idea that dominant arm performance reflects a controller that predicts and optimizes arm and task dynamics, whereas nondominant arm performance relies on a controller that is specialized for making movements and achieving a stable goal by specifying impedance around ‘‘equilibrium’’ positions
Summary
The modern view of brain lateralization, built upon early work in patients with unilateral brain damage and more recent work in split-brain patients [1,2], suggests that each cerebral hemisphere has become specialized for different, but complementary control processes that together govern a particular behavior. Note that the feedforward/feedback hypothesis makes no prediction about differences in the mean final position of the hand on these probe trials in the current study Instead, this framework predicts more variable initial directions for the nondominant arm, and more variable final positions for the dominant arm. It is important to emphasize that a condition necessary to observe the predicted movement patterns on probe trials, for the non-dominant arm, is that the specified control strategy does not change relative to baseline conditions This does not seem to be the case for movements from the collinear start positions [46]. It may be reasonable to consider that non-dominant arm movements will end more consistently near the baseline target while the dominant arm will show better maintenance of movement direction on these trials
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