The neural foundations of handedness: insights from a rare case of deafferentation.

The role of proprioceptive feedback on motor lateralization remains unclear. We asked whether motor lateralization is dependent on proprioceptive feedback by examining a rare case of proprioceptive deafferentation (GL). Motor lateralization is thought to arise from asymmetries in neural organization, particularly at the cortical level. For example, we have previously provided evidence that the left hemisphere mediates optimal motor control that allows execution of smooth and efficient arm trajectories, while the right hemisphere mediates impedance control that can achieve stable and accurate final arm postures. The role of proprioception in both of these processes has previously been demonstrated empirically, bringing into question whether loss of proprioception will disrupt lateralization of motor performance. In this study, we assessed whether the loss of online sensory information produces deficits in integrating specific control contributions from each hemisphere by using a reaching task to examine upper limb kinematics in GL and five age-matched controls. Behavioral findings revealed differential deficits in the control of the left and right hands in GL and performance deficits in each of GL's hands compared with controls. Computational simulations can explain the behavioral results as a disruption in the integration of postural and trajectory control mechanisms when no somatosensory information is available. This rare case of proprioceptive deafferentation provides insights into developing a more accurate understanding of handedness that emphasizes the role of proprioception in both predictive and feedback control mechanisms.NEW & NOTEWORTHY The role of proprioceptive feedback on the lateralization of motor control mechanisms is unclear. We examined upper limb kinematics in a rare case of peripheral deafferentation to determine the role of sensory information in integrating motor control mechanisms from each hemisphere. Our empirical findings and computational simulations showed that the loss of somatosensory information results in an impaired integration of control mechanisms, thus providing support for a complementary dominance hypothesis of handedness.

Effects of unilateral stroke on multi-finger synergies and their feed-forward adjustments.

We explored the changes in multi-finger synergies in patients after a single cortical stroke with mild motor impairments. We hypothesized that both synergy indices and anticipatory synergy adjustments prior to the initiation of a self-paced quick action would be diminished in the patients compared to age-matched controls. The patients with history of cortical stroke, and age-matched controls (n=12 in each group) performed one-finger and multi-finger accurate force production tasks involving both steady-state and quick force pulse production. Finger interdependence (enslaving) and multi-finger synergies stabilizing total force were quantified. The stroke patients showed lower maximal finger forces, in particular in the contralesional hand, which also showed increased enslaving indices. Multi-finger synergies during steady-state force production were, however, unchanged after stroke. In contrast, a drop in the synergy index prior to the force pulse generation was significantly delayed in the stroke patients. Our results show that mild cortical stroke leads to no significant changes in multifinger synergies, but there is impairment in feed-forward adjustments of the synergies prior to a quick action, a drop in the maximal force production, and an increase in enslaving. We conclude that studies of synergies reveal two aspects of synergic control differentially affected by cortical stroke.

Handedness can be explained by a serial hybrid control scheme.

Our previous studies on healthy individuals and stroke patients led us to propose that the dominant and nondominant arms are specialized for distinct motor control processes. We hypothesize that the dominant arm is specialized for predictive control of limb dynamics, and the nondominant arm is specialized for impedance control. We previously introduced a hybrid control scheme to explain lateralization of single-joint elbow movements. In this paper we apply a similar computational framework to explore interlimb differences in multi-joint reaching movements: the movements of both arms are initiated using predictive control mechanisms, and terminated using impedance mechanisms. Four parameters characterize predictive mechanisms, four parameters characterize impedance mechanisms, and the ninth parameter describes the instant of switch between the two modes of control. Based on our hypothesis of motor lateralization, we predict an early switch to impedance control for the nondominant arm, but a late switch, near the end of motion, for the dominant arm. We fit our model to multi-joint reaching movements of each arm, made in the horizontal plane. Our results reveal that the more curved trajectories of the nondominant arm are characterized by an early switch to impedance mechanisms, in the initial phase of motion near peak velocity. In contrast, the trajectories of the dominant arm were best fit, when the switch to impedance mechanisms occurred late in the deceleration phase of motion. These results support a model of motor lateralization in which the dominant controller is specialized for predictive control of task dynamics, while the nondominant arm is specialized for impedance control mechanisms. For the first time, we are able to operationally define handedness expressed during multi-joint movements by applying a computational control model.

Sensorimotor performance asymmetries predict hand selection.

Handedness is most often measured by questionnaires that assess an individual's preference for using a particular hand to perform a variety of tasks. While such assessments have proved reliable, they do not address the underlying neurobehavioral processes that give rise to the choice of which hand to use. Recent research has indicated that handedness is associated with hemispheric specializations for different aspects of sensorimotor performance. We now hypothesize that an individual's choice of which hand to use for a given task should result from an interaction between these underlying neurobehavioral asymmetries with task conditions. We test this hypothesis by manipulating two factors in targeted reaching movements: (1) region of workspace and (2) visual feedback conditions. The first manipulation modified the geometric and dynamic requirements of the task for each arm, whereas the second modified the sensorimotor performance asymmetries, an effect predicted by previous literature. We expected that arm choice would be reflected by an interaction between these factors. Our results indicated that removing visual feedback both improved the relative performance of the non-dominant arm and increased the choice to use this arm for targets near midline, an effect that was enhanced for targets requiring larger movement amplitudes. We explain these findings in the context of the dynamic dominance hypothesis of handedness and discuss their implications for the link between hemispheric asymmetries in neural control and hand preference.

Motor lateralization is characterized by a serial hybrid control scheme.

Our previous studies of limb coordination in healthy right- and left-handers led to the development of a theoretical model of motor lateralization, dynamic dominance, which was recently supported by studies in patients with unilateral stroke. One of our most robust findings was on single-joint movements in young healthy subjects [Sainburg and Schaefer (2004) J Neurophysiol 92:1374-1383]. In this study, subjects made elbow joint reaching movements toward four targets of different amplitudes with each arm. Although both arms achieved equivalent task performance, each did so through different strategies. The dominant arm strategy scaled peak acceleration with peak velocity and movement extent, while the nondominant strategy adjusted acceleration duration to achieve the different velocities and distances. We now propose that these observed interlimb differences can be explained using a serial hybrid controller in which movements are initiated using predictive control and terminated using impedance control. Further, we propose that the two arms should differ in the relative time that control switches from the predictive to the impedance mechanisms. We present a mathematical formulation of our hybrid controller and then test the plausibility of this control paradigm by investigating how well our model can explain interlimb differences in experimental data. Our findings confirm that the model predicts early shifts between controllers for left arm movements, which rely on impedance control mechanisms, and late shifts for right arm movements, which rely on predictive control mechanisms. This is the first computational model of motor lateralization and is consistent with our theoretical model that emerged from empirical findings. It represents a first step in consolidating our theoretical understanding of motor lateralization into an operational model of control.

The influence of target sensory modality on motor planning may reflect errors in sensori-motor transformations.

Multi-sensory integration studies have shown that combining heterogeneous signals can optimize motor performance by reducing errors inherent to any single modality. However, it has also been suggested that errors could arise from erroneous transformations between heterogeneous coordinate systems. Here we investigated the effect of visuo-proprioceptive integration on the control of multi-joint arm movements by manipulating target modality. When the target was visual, movement control required the integration of visual target signals with proprioceptive signals about limb configuration. In contrast, when the target was the unseen fingertip, movement control relied solely on proprioceptive signals since visual feedback of hand position was precluded. We hypothesized that a faulty integration of visual target signals with proprioceptive arm signals would result in a less accurate planning of visually-targeted movements with respect to proprioceptively-targeted movements. Different inter-joint coordinations patterns were tested by varying starting hand position. Results showed larger initial trajectory deviations from target direction for visually-targeted movements involving substantial shoulder and elbow motions. Inverse dynamic analysis revealed that these deviations were associated with less efficient intersegmental coordination. The control of visually-targeted movements thus appeared sub-optimal compared to proprioceptively-targeted movements when considering theoretical models of motor planning assuming kinematic or dynamic optimizations. Additional experiments further highlighted the effect of target position, and visual feedback of starting hand position, on motor planning for proprioceptively- and visually-targeted movements. Our findings suggest that the integration of heterogeneous sensory signals related to hand and target positions introduces errors in motor planning.

Differences in control of limb dynamics during dominant and nondominant arm reaching.

This study compares the coordination patterns employed for the left and right arms during rapid targeted reaching movements. Six right-handed subjects reached to each of three targets, designed to elicit progressively greater amplitude interaction torques at the elbow joint. All targets required the same elbow excursion (20 degrees ), but different shoulder excursions (5, 10, and 15 degrees, respectively). Movements were restricted to the shoulder and elbow and supported on a horizontal plane by a frictionless air-jet system. Subjects received visual feedback only of the final hand position with respect to the start and target locations. For motivation, points were awarded based on final position accuracy for movements completed within an interval of 400-600 ms. For all subjects, the right and left hands showed a similar time course of improvement in final position accuracy over repeated trials. After task adaptation, final position accuracy was similar for both hands; however, the hand trajectories and joint coordination patterns during the movements were systematically different. Right hand paths showed medial to lateral curvatures that were consistent in magnitude for all target directions, whereas the left hand paths had lateral to medial curvatures that increased in magnitude across the three target directions. Inverse dynamic analysis revealed substantial differences in the coordination of muscle and intersegmental torques for the left and right arms. Although left elbow muscle torque contributed largely to elbow acceleration, right arm coordination was characterized by a proximal control strategy, in which movement of both joints was primarily driven by the effects of shoulder muscles. In addition, right hand path direction changes were independent of elbow interaction torque impulse, indicating skillful coordination of muscle actions with intersegmental dynamics. In contrast, left hand path direction changes varied directly with elbow interaction torque impulse. These findings strongly suggest that distinct neural control mechanisms are employed for dominant and non dominant arm movements. However, whether interlimb differences in neural strategies are a consequence of asymmetric use of the two arms, or vice versa, is not yet understood. The implications for neural organization of voluntary movement control are discussed.

Intersegmental dynamics are controlled by sequential anticipatory, error correction, and postural mechanisms.

The purpose of this study is to examine the mechanisms underlying control of intersegmental dynamics during reaching movements. Two experiments were conducted to determine the relative contributions of anticipatory and somatosensory feedback mechanisms in controlling intersegmental dynamics and whether adaptation to novel intersegmental dynamics generalizes across a range of movement directions. The mechanisms used to control interaction torques were examined by altering the inertial load of the forearm. Movements were restricted to the shoulder and elbow and supported on a horizontal plane by a frictionless air-jet system. Subjects made rapid out-and-back movements over a target line presented on a computer screen. The screen cursor disappeared at movement onset, and hand paths were displayed after each movement. After subjects adapted to a novel inertial configuration, the position of an attached mass was changed on pseudorandom trials. During these "surprise" trials, movements were initiated with the torque patterns appropriate to the previously learned inertial condition. As a result, characteristic errors in initial movement direction were predicted by an open-looped forward simulation. After these errors occurred, feedback mediated changes in torque emerged that, surprisingly, further decreased the accuracy of movement reversals. Nevertheless at the end of movement, the hand consistently returned to the starting position. It is plausible that the final position was determined completely by feedback-mediated changes in torque. In a second experiment, adaptation to a novel inertial load during movements made in a single direction showed limited transfer across a range of directions. These findings support and extend those of previous reports, which indicated combined anticipatory and postural mechanisms to coordinate rapid reaching movements. The current results indicate a three-stage control system that sequentially links anticipatory, error correction, and postural mechanisms to control intersegmental dynamics. Our results, showing limited generalization across directions, are consistent with previous reports examining adaptation to externally applied forces and extend those findings to indicate that the nervous system uses sensory information to recalibrate internal representations of the musculoskeletal apparatus itself.

Control of limb dynamics in normal subjects and patients without proprioception.

1. We recently showed that patients lacking proprioceptive input from their limbs have particular difficulty performing multijoint movements. In a pantomimed slicing gesture requiring sharp reversals in hand path direction, patients showed large hand path distortions at movement reversals because of failure to coordinate the timing of the separate reversals at the shoulder and elbow joints. We hypothesized that these reversal errors resulted from uncompensated effects of inertial interactions produced by changes in shoulder joint acceleration that were transferred to the elbow. We now test this hypothesis and examine the role of proprioceptive input by comparing the motor performance of five normal subjects with that of two patients with large-fiber sensory neuropathy. 2. Subjects were to trace each of six template lines presented randomly on a computer screen by straight overlapping out-and-back movements of the hand on a digitizing tablet. The lines originated from a common starting position but were in different directions and had different lengths. Directions and lengths were adjusted so that tracing movements would all require the same elbow excursion, whereas shoulder excursion would vary. The effects of varying interaction torques on elbow kinematics were then studied. The subject's dominant arm was supported in the horizontal plane by a low-inertia brace equipped with ball bearing joints and potentiometers under the elbow and shoulder. Hand position was monitored by a magnetic pen attached to the brace 1 cm above a digitizing tablet and could be displayed as a screen cursor. Vision of the subject's arm was blocked and the screen cursor was blanked at movement onset to prevent visual feedback during movement. Elbow joint torques were calculated from joint angle recordings and compared with electromyographic recordings of elbow joint musculature. 3. In control subjects, outward and inward paths were straight and overlapped the template lines regardless of their direction. As prescribed by the task, elbow kinematics remained the same across movement directions, whereas interaction torques varied substantially. The timing of the onsets of biceps activity and the offsets of triceps activity during elbow flexion varied systematically with direction-dependent changes in interaction torques. Controls exploited or dampened these interaction torques as needed to meet the kinematic demands of the task. 4. In contrast, the patients made characteristic errors at movement reversals that increased systematically across movement directions. These reversal errors resulted from improper timing of elbow and shoulder joint reversals.(ABSTRACT TRUNCATED AT 400 WORDS)

Loss of proprioception produces deficits in interjoint coordination.

1. We analyzed the performance of a simple pantomimed gesture in 2 patients with large-fiber sensory neuropathy and 11 control subjects to determine how proprioceptive deafferentation disrupts unconstrained multijoint movements. Both patients had near-total loss of joint position, vibration, and discriminative touch sensation in the upper extremities. Muscle strength remained intact. 2. Subjects performed a gesture similar to slicing a loaf of bread. In this gesture, the hand first moves outward from the body, reverses direction sharply, and then moves back toward the body. Accurate performance requires precise coordination between the shoulder and elbow joints during movement reversals. Movements were performed under two conditions: with eyes open and with eyes closed. Three dimensional shoulder, elbow, wrist, and hand trajectories were recorded on a WATSMART system. 3. When control subjects performed the gesture with their eyes closed, their wrist trajectories were relatively straight and individual cycles of motion were planar. Movements reversed direction sharply, such that outward and inward portions of the wrist path were closely aligned. Corresponding to this spatial profile, the reversals in movement direction at the shoulder joint, from flexion to extension, and at the elbow joint, from extension to flexion, were synchronous. 4. In contrast, when deafferented patients performed the gesture with their eyes closed, their wrist trajectories were highly curved and individual cycles were severely nonplanar. The wrist paths showed a characteristic anomaly during the reversal in movement direction, when elbow joint movement became transiently locked. Correspondingly, the movement reversals at the shoulder and elbow joints were severely temporally decoupled. 5. When patients were able to view their limbs during performance of this gesture there was significant improvement in the linearity and planarity of movements. However, the patients remained unable to synchronize the movements at the shoulder and elbow joints to produce spatially precise wrist paths. 6. We conclude that loss of proprioception disrupts interjoint coordination and discuss the hypothesis that this interjoint coordination deficit results from a failure to control the interaction forces that arise between limb segments during multijoint movements.