Robert L. Sainburg

Evidence for a dynamic-dominance hypothesis of handedness

Abstract. Handedness is a prominent behavioral phenomenon that emerges from asymmetrical neural organization of human motor systems. However, the aspects of motor performance that correspond to handedness remain largely undetermined. A recent study examining interlimb differences in coordination of reaching demonstrated dominant arm advantages in controlling limb segment inertial dynamics (Sainburg and Kalakanis 2000). Based on these findings, I now propose the dynamic-dominance hypothesis, which states that the essential factor that distinguishes dominant from nondominant arm performance is the facility governing the control of limb dynamics. The purpose of this study is to test two predictions of this hypothesis: 1) adaptation to novel intersegmental dynamics, requiring the development of new dynamic transforms, should be more effective for the dominant arm; 2) there should be no difference in adapting to visuomotor rotations performed with the dominant as compared with the nondominant arm. The latter prediction is based on the idea that visual information about target position is translated into an internal reference frame prior to transformation of the movement plan into dynamic properties, which reflect the forces required to produce movement. To test these predictions, dominant arm adaptation is compared to nondominant arm adaptation during exposure to novel inertial loads and to novel visuomotor rotations. The results indicate substantial interlimb differences in adaptation to novel inertial dynamics, but equivalent adaptation to novel visuomotor rotations. Inverse dynamic analysis revealed better coordination of dominant arm muscle torques across both shoulder and elbow joints, as compared with nondominant arm muscle torques. As a result, dominant arm movements were produced with a fraction of the mean squared muscle torque computed for nondominant arm movements made at similar speeds. These results support the dynamic-dominance hypothesis, indicating that interlimb asymmetries in control arise downstream to visuomotor transformations, when dynamic variables that correspond to the forces required for motion are specified.

Interlimb transfer of visuomotor rotations: independence of direction and final position information

Previous findings from our laboratory support the idea that the dominant arm is more proficient than the non-dominant arm in coordinating intersegmental dynamics for specifying trajectory direction and shape during multijoint reaching movements. We also showed that adaptation of right and left arms to novel visuomotor rotations was equivalent, suggesting that this process occurs upstream to processes that distinguish dominant and non-dominant arm performance. Because of this, we speculate that such visuomotor adaptations might transfer to subsequent performance during adaptation with the other arm. We now examine whether opposite arm training to novel visuomotor rotations transfers to affect adaptation using the right and left arms. Two subject groups, RL and LR, each comprising seven right-handed subjects, adapted to a 30° counterclockwise rotation in the visual display during a center-out reaching task performed in eight directions. Each group first adapted using either the right (RL) or left (LR) arm, followed by opposite arm adaptation. In order to assess transfer, we compared the same side arm movements (either right or left) following opposite arm adaptation to those performed prior to opposite arm adaptation. Our findings indicate unambiguous transfer of learning across the arms. Different features of movement transferred in different directions: Opposite arm training improved the initial direction of right arm movements under the rotated visual condition, whereas opposite arm training improved the final position accuracy, but not the direction of left arm movements. These findings confirm that transfer of training was not due to a general cognitive strategy, since such an effect should influence either hand equally. These findings support the hypothesis that each arm controller has access to information learned during opposite arm training. We suggest that each controller uses this information differently, depending on its proficiency for specifying particular features of movement. We discuss evidence that these two aspects of control are differentially mediated by the right and left cerebral hemispheres.

Handedness : Differential specializations for control of trajectory and position

Handedness is often portrayed as a nonfunctional artifact of cerebral asymmetry. Our data, however, indicate that handedness reflects cerebral specialization for specific control processes. Each hemisphere/limb system is specialized for different but complementary functions: the dominant system for controlling limb trajectory dynamics, and the nondominant system for controlling limb position.

Hemispheric Specialization and Functional Impact of Ipsilesional Deficits in Movement Coordination and Accuracy

Previous studies have demonstrated that following unilateral stroke, motor impairment occurs both contralateral, as well as ipsilateral, to the lesion. Although ipsilesional impairments can be functionally limiting, they can also provide important insight into the role of the ipsilateral hemisphere in controlling movement and the lateralization of specific motor control mechanisms, given that unilateral arm movements are thought to recruit processes in each hemisphere. The purpose of this study was to examine whether left and right hemisphere damage following stroke produces different ipsilesional deficits, and whether our dynamic dominance model of motor lateralization can predict such deficits. Specifically, the dynamic dominance model attributes control of multijoint dynamics to the left hemisphere, and control of steady-state position to the right hemisphere. Chronic stroke patients with either left or right hemisphere damage (LHD or RHD) used their ipsilesional arm, and the control subjects used either their left or right arm (LHC or RHC), to perform targeted reaching movements in different directions within the workspace ipsilateral to their reaching arm. We found that the LHD group showed deficits in controlling the arms trajectory due to impaired multijoint coordination, but no deficits in achieving accurate final positions. In contrast, the RHD group showed deficits in final position accuracy but not in the ability to coordinate multiple joints during movement, thereby providing additional evidence for the hemisphere-specific nature of motor deficits. Furthermore, while both the LHD and RHD groups were functionally impaired to the same degree on the Jebsen Hand Function Test (JHFT), our results suggest that the underlying mechanisms for such impairment may be hemisphere-dependent.

The dominant and nondominant arms are specialized for stabilizing different features of task performance.

We have previously proposed a model of motor lateralization, in which the two arms are differentially specialized for complementary control processes. During aimed movements, the dominant arm shows advantages for coordinating intersegmental dynamics as required for specifying trajectory speed and direction, while the nondominant arm shows advantages in controlling limb impedance, as required for accurate final position control. We now directly test this model of lateralization by comparing performance of the two arms under two different tasks: one in which reaching movement is made from one fixed starting position to three different target positions; and the other in which reaching is made from three different starting positions to one fixed target position. For the dominant arm, performance was most accurate when reaching from one fixed starting position to multiple targets. In contrast, nondominant arm performance was most accurate when reaching toward a single target from multiple start locations. These findings contradict the idea that motor lateralization reflects a global advantage of one “dominant” hemisphere/limb system. Instead, each hemisphere/limb system appears specialized for stabilizing different aspects of task performance.

Mechanisms underlying interlimb transfer of visuomotor rotations

We previously reported that opposite arm training improved the initial direction of dominant arm movements, whereas it only improved the final position accuracy of non-dominant arm movements. We now ask whether each controller accesses common, or separate, short-term memory resources. To address this question, we investigated interlimb transfer of learning for visuomotor rotations that were directed oppositely [clockwise (CW)/counterclockwise (CCW)] for the two arms. We expected that if information obtained by initial training was stored in the same short-term memory space for both arms, opposite arm training of a CW rotation would interfere with subsequent adaptation to a CCW rotation. All subjects first adapted to a 30° rotation (CW) in the visual display during reaching movements. Following this, they adapted to a 30° rotation in the opposite direction (CCW) with the other arm. In contrast to our previous findings for interlimb transfer of same direction rotations (CCW/CCW), no effects of opposite arm adaptation were indicated in the initial trials performed. This indicates that interlimb transfer is not obligatory, and suggests that short-term memory resources for the two limbs are independent. Through single trial analysis, we found that the direction and final position errors of the first trial of movement, following opposite arm training, were always the same as those of naive performance. This was true whether the opposite arm was trained with the same or the opposing rotation. When trained with the same rotation, transfer of learning did not occur until the second trial. These findings suggest that the selective use of opposite arm information is dependent on the first trial to probe current movement conditions. Interestingly, the final extent of adaptation appeared to be reduced by opposite arm training of opposing rotations. Thus, the extent of adaptation, but not initial information transfer, appears obligatorily affected by prior opposite arm adaptation. According to our findings, it is plausible that the initiation and the final extent of adaptation involve two independent neural processes. Theoretical implications of these findings are discussed.

Adaptation to Visuomotor Rotations Remaps Movement Vectors, Not Final Positions

When exposed to novel visuomotor rotations, subjects readily adapt reaching movements, such that the virtual display of the hand is brought to the target. Whereas this clearly reflects remapping of the relationship between hand movements and the visual display, the nature of this remapping is not well understood. We now examine whether such adaptation results in remapping of the position of the visually displayed target and the final limb position or between the target vector and the movement vector. The latter is defined relative to a starting position, whereas the former should be independent of the starting position. Subjects first adapted to a 30° rotation during reaching movements made from a single starting location to four different target locations. After adaptation, generalization trials were introduced, during which reaching movements were made under the same visual rotation condition but started from one of two locations outside the practiced workspace. These trials were directed to either the previously practiced targets or new targets that reflected the direction and distance of the practiced trials. Generalization was greatest for movements made in similar directions, regardless of changes in spatial location. Most significantly, when reaching to the previously adapted targets, subjects did not reach to the previously learned limb positions but rather to positions that reflected a near 30° rotation of the new target vector. These results indicate that learned visuomotor rotations remap the representations of movement vectors and not final positions of the limb in the workspace.

Differential influence of vision and proprioception on control of movement distance

The purpose of this study was to investigate the contribution of proprioceptive and visual information about initial limb position in controlling the distance of rapid, single-joint reaching movements. Using a virtual reality environment, we systematically changed the relationship between actual and visually displayed hand position as subjects’ positioned a cursor within a start circle. No visual feedback was given during the movement. Subjects reached two visual targets (115 and 125° elbow angle) from four start locations (90, 95, 100, and 105° elbow angle) under four mismatch conditions (0, 5, 10, or 15°). A 2×4×4 ANOVA enabled us to ask whether the subjects controlled the movement distance in accord with the virtual, or the actual hand location. Our results indicate that the movement distance was mainly controlled according to the virtual start location. Whereas distance modification was most extensive for the closer target, analysis of acceleration profiles revealed that, regardless of target position, visual information about start location determined the initial peak in tangential hand acceleration. Peak acceleration scaled with peak velocity and movement distance, a phenomenon termed “pulse-height” control. In contrast, proprioceptive information about actual hand location determined the duration of acceleration, which also scaled with peak velocity and movement distance, a phenomenon termed “pulse-width” control. Because pulse-height and pulse-width mechanisms reflect movement planning and sensory-based corrective processes, respectively, our current findings indicate that vision is used primarily for planning movement distance, while proprioception is used primarily for online corrections during rapid, unseen movements toward visual targets.

Limitations in interlimb transfer of visuomotor rotations

It has been shown that learning visuomotor rotations with multiple target directions, compared with a single target direction, leads to greater generalization to untrained targets within the same limb. This implies that multiple direction learning results in a more complete internal model of the visuomotor transform. It has also been documented that the extent of transfer of movement information regarding visuomotor adaptations between the limbs is limited, relative to that between different configurations of the same limb. The present study thus investigated the origin of this restriction in interlimb transfer, by comparing the effects of eight-direction and one-direction training conditions with one arm on the subsequent performance with the other arm. It was hypothesized that if multiple direction learning leads to a more complete model of the novel visuomotor transform, interlimb transfer should be enhanced relative to that following single direction training. However, if no differences are observed between single and multiple direction training conditions, this would suggest that such learning is effector dependent. We also tested the hypothesis that interlimb transfer of visuomotor adaptation is not obligatory, by examining the effects of visual rotation direction (same or oppositely directed visuomotor rotations for the two arms). All subjects first adapted to a 30° rotation, either clockwise or counterclockwise, in the visual display during reaching movements. Following this, they adapted to a 30° rotation in either the same or opposing direction with the other arm. Results showed that initial training with the non-dominant arm facilitated subsequent performance with the dominant arm in terms of initial direction control, but only under the same rotation condition. Both single and eight direction training conditions led to substantial transfer in subsequent performance with the other arm, but multiple direction training was no more beneficial than single direction training. This finding suggests that the previously reported intralimb advantages of multiple direction learning are effector specific. Our findings are discussed in the context of hierarchical models of motor control to explain the intralimb advantages of multiple direction training.

The effect of target modality on visual and proprioceptive contributions to the control of movement distance

The goal of this study was to determine whether the sensory nature of a target influences the roles of vision and proprioception in the planning of movement distance. Two groups of subjects made rapid, elbow extension movements, either toward a visual target or toward the index fingertip of the unseen opposite hand. Visual feedback of the reaching index fingertip was only available before movement onset. Using a virtual reality display, we randomly introduced a discrepancy between actual and virtual (cursor) fingertip location. When subjects reached toward the visual target, movement distance varied with changes in visual information about initial hand position. For the proprioceptive target, movement distance varied mostly with changes in proprioceptive information about initial position. The effect of target modality was already present at the time of peak acceleration, indicating that this effect include feedforward processes. Our results suggest that the relative contributions of vision and proprioception to motor planning can change, depending on the modality in which task relevant information is represented.