The complementary dominance hypothesis: a model for remediating the 'good' hand in stroke survivors.

The complementary dominance hypothesis is a novel model of motor lateralization substantiated by decades of research examining interlimb differences in the control of upper extremity movements in neurotypical adults and hemisphere-specific motor deficits in stroke survivors. In contrast to earlier ideas that attribute handedness to the specialization of one hemisphere, our model proposes complementary motor control specializations in each hemisphere. The dominant hemisphere mediates optimal control of limb dynamics as required for smooth and efficient movements, whereas the non-dominant hemisphere mediates impedance control, important for countering unexpected mechanical conditions and achieving steady-state limb positions. Importantly, this model proposes that each hemisphere contributes its specialization to both arms (though with greater influence from either arm's contralateral hemisphere) and thus predicts that lesions to one hemisphere should produce hemisphere-specific motor deficits in not only the contralesional arm, but also the ipsilesional arm of stroke survivors - a powerful prediction now supported by a growing body of evidence. Such ipsilesional arm motor deficits vary with contralesional arm impairment, and thus individuals with little to no functional use of the contralesional arm experience both the greatest impairments in the ipsilesional arm, as well as the greatest reliance on it to serve as the main or sole manipulator for activities of daily living. Accordingly, we have proposed and tested a novel intervention that reduces hemisphere-specific ipsilesional arm deficits and thereby improves functional independence in stroke survivors with severe contralesional impairment.

Symmetry and synchrony of bimanual movements are not predicated on interlimb control coupling.

Previous studies suggest that bimanual coordination recruits neural mechanisms that explicitly couple control of the arms, resulting in symmetric kinematics. However, the higher symmetry for actions that require congruous joint motions compared with noncongruous joint motions calls into question the concept of control coupling as a general policy. An alternative view proposes that codependence might emerge from an optimal feedback controller that minimizes control effort and costs in task performance. Support for this view comes from studies comparing conditions in which both hands move a shared or independent virtual objects. Because these studies have mainly focused on congruous bimanual movements, it remains unclear if kinematic symmetry emerges from such control policies. We now examine movements with congruous or noncongruous joint motions (inertially symmetric or asymmetric, respectively) under shared or independent cursors conditions. We reasoned that if a control policy minimizes kinematic differences between limbs, spatiotemporal symmetry should remain relatively unaffected by inertial asymmetries. As shared tasks reportedly elicit greater interlimb codependence, these conditions should elicit higher bilateral covariance regardless of inertial asymmetries. Our results indicate a robust spatiotemporal symmetry only under inertially symmetric conditions, regardless of cursor condition. We simulated bimanual reaching using an optimal feedback controller with and without explicit costs of kinematic asymmetry, finding that only the latter mirrored our empirical data. Our findings support the hypothesis that bimanual control policies do not include kinematic asymmetry as a cost when it is not demanded by task constraints suggesting that kinematic symmetry depends critically on mechanical movement conditions.NEW & NOTEWORTHY Previously, the control coupling hypothesis and task-dependent control hypothesis have been shown to be robust in the bimanually symmetrical movement, but whether the same policy remains robust in the bimanually asymmetrical movement remains unclear. Here, with evidence from empirical and simulation data, we show that a spatiotemporal symmetry between the arms is not predicated on control coupling, but instead it is predicated on the symmetry of mechanical conditions (e.g. limb inertia) between the arms.

Bilateral arm movements are coordinated via task-dependent negotiations between independent and codependent control, but not by a "coupling" control policy.

Prior research has shown that coordination of bilateral arm movements might be attributed to either control policies that minimize performance and control costs regardless of bilateral symmetry or by control coupling, which activates bilaterally homologous muscles as a single unit to achieve symmetric performance. We hypothesize that independent bimanual control (movements of one arm are performed without influence on the other) and codependent bimanual control (two arms are constrained to move together with high spatiotemporal symmetry) are two extremes on a coordination spectrum that can be negotiated to meet infinite variations in task demands. To better understand and distinguish between these views, we designed a task where minimization of either control costs or asymmetry would yield different patterns of coordination. Participants made bilateral reaches with a shared visual cursor to a midline target. We then covertly varied the gain contribution of either hand to the shared cursor's horizontal position. Across two experiments, we show that bilateral coordination retains high task-dependent sensitivity to subtle visual feedback gain asymmetries applied to the shared cursor. Specifically, we found a change from strong spatial covariation between hands during equal gains to more independent control during asymmetric gains, which occurred rapidly and with high specificity to the dimension of gain manipulation. Furthermore, the extent of spatial covariation was graded to the magnitude of perpendicular gain asymmetry between hands. These findings suggest coordination of bilateral arm movements flexibly maneuvers along a continuous coordination spectrum in a task-dependent manner that cannot be explained by bilateral control coupling.NEW & NOTEWORTHY Minimization of performance and control costs and efferent coupling between bilaterally homologous muscle groups have been separately hypothesized to describe patterns of bimanual coordination. Here, we address whether the mechanisms mediating independent and codependent control between limbs can be weighted for successful task performance. Using bilaterally asymmetric visuomotor gain perturbations, we show bimanual coordination can be characterized as a negotiation along a spectrum between extremes of independent and codependent control, but not efferent control coupling.

Individual sensorimotor adaptation characteristics are independent across orofacial speech movements and limb reaching movements.

Sensorimotor adaptation is critical for human motor control but shows considerable interindividual variability. Efforts are underway to identify factors accounting for individual differences in specific adaptation tasks. However, a fundamental question has remained unaddressed: Is an individual's capability for adaptation effector system specific or does it reflect a generalized adaptation ability? We therefore tested the same participants in analogous adaptation paradigms focusing on distinct sensorimotor systems: speaking with perturbed auditory feedback and reaching with perturbed visual feedback. Each task was completed once with the perturbation introduced gradually (ramped up over 60 trials) and, on a different day, once with the perturbation introduced suddenly. Consistent with studies of each system separately, visuomotor reach adaptation was more complete than auditory-motor speech adaptation (80% vs. 29% of the perturbation). Adaptation was not significantly correlated between the speech and reach tasks. Moreover, considered within tasks, 1) adaptation extent was correlated between the gradual and sudden conditions for reaching but not for speaking, 2) adaptation extent was correlated with additional measures of performance (e.g., trial duration, within-trial corrections) only for reaching and not for speaking, and 3) fitting individual participant adaptation profiles with exponential rather than linear functions offered a larger benefit [lower root mean square error (RMSE)] for the reach task than for the speech task. Combined, results suggest that the ability for sensorimotor adaptation relies on neural plasticity mechanisms that are effector system specific rather than generalized. This finding has important implications for ongoing efforts seeking to identify cognitive, behavioral, and neurochemical predictors of individual sensorimotor adaptation.NEW & NOTEWORTHY This study provides the first detailed demonstration that individual sensorimotor adaptation characteristics are independent across articulatory speech movements and limb reaching movements. Thus, individual sensorimotor learning abilities are effector system specific rather than generalized. Findings regarding one effector system do not necessarily apply to other systems, different underlying mechanisms may be involved, and implications for clinical rehabilitation or performance training also cannot be generalized.

Adaptation of reach action to a novel force-field is not predicted by acuity of dynamic proprioception in either older or younger adults.

Healthy ageing involves degeneration of the neuromuscular system which impacts movement control and proprioception. Yet the relationship between these sensory and motor deficits in upper limb reaching has not been examined in detail. Recently, we reported that age-related proprioceptive deficits were unrelated to accuracy in rapid arm movements, but whether this applied in motor tasks more heavily dependent on proprioceptive feedback was not clear. To address this, we have tested groups of younger and older adults on a force-field adaptation task under either full or limited visual feedback conditions and examined how performance was related to dynamic proprioceptive acuity. Adaptive performance was similar between the age groups, regardless of visual feedback condition, although older adults showed increased after-effects. Physically inactive individuals made larger systematic (but not variable) proprioceptive errors, irrespective of age. However, dynamic proprioceptive acuity was unrelated to adaptation and there was no consistent evidence of proprioceptive recalibration with adaptation to the force-field for any group. Finally, in spite of clear age-dependent loss of spatial working memory capacity, we found no relationship between memory capacity and adaptive performance or proprioceptive acuity. Thus, non-clinical levels of deficit in dynamic proprioception, due to age or physical inactivity, do not affect force-field adaptation, even under conditions of limited visual feedback that might require greater proprioceptive control.

Proprioceptive deficits in inactive older adults are not reflected in fast targeted reaching movements.

During normal healthy ageing there is a decline in the ability to control simple movements, characterised by increased reaction times, movement durations and variability. There is also growing evidence of age-related proprioceptive loss which may contribute to these impairments. However, this relationship has not been studied in detail for the upper limb. We recruited 20 younger adults (YAs) and 31 older adults (OAs) who each performed 2 tasks on a 2D robotic manipulandum. The first assessed dynamic proprioceptive acuity using active, multi-joint movements constrained by the robot to a pre-defined path. Participants made perceptual judgements of the lateral position of the unseen arm. The second task required fast, accurate and discrete movements to the same targets in the absence of visual feedback of the hand, and without robotic intervention. We predicted that the variable proprioceptive error (uncertainty range) assessed in Task 1 would be increased in physically inactive OAs and would predict increased movement variability in Task 2. Instead we found that physically inactive OAs had larger systematic proprioceptive errors (bias) than YAs (t[33] = 2.8, p = 0.009), and neither proprioceptive uncertainty nor bias was related to motor performance in either age group (all regression model R2 ≤ 0.06). We suggest that previously reported estimates of proprioceptive decline with ageing may be exaggerated by task demands and that the extent of these deficits is unrelated to control of discrete, rapid movement. The relationship between dynamic proprioceptive acuity and movement control in other tasks with greater emphasis on online feedback is still unclear and warrants further investigation.

Proprioceptive loss and the perception, control and learning of arm movements in humans: evidence from sensory neuronopathy.

It is uncertain how vision and proprioception contribute to adaptation of voluntary arm movements. In normal participants, adaptation to imposed forces is possible with or without vision, suggesting that proprioception is sufficient; in participants with proprioceptive loss (PL), adaptation is possible with visual feedback, suggesting that proprioception is unnecessary. In experiment 1 adaptation to, and retention of, perturbing forces were evaluated in three chronically deafferented participants. They made rapid reaching movements to move a cursor toward a visual target, and a planar robot arm applied orthogonal velocity-dependent forces. Trial-by-trial error correction was observed in all participants. Such adaptation has been characterized with a dual-rate model: a fast process that learns quickly, but retains poorly and a slow process that learns slowly and retains well. Experiment 2 showed that the PL participants had large individual differences in learning and retention rates compared to normal controls. Experiment 3 tested participants' perception of applied forces. With visual feedback, the PL participants could report the perturbation's direction as well as controls; without visual feedback, thresholds were elevated. Experiment 4 showed, in healthy participants, that force direction could be estimated from head motion, at levels close to the no-vision threshold for the PL participants. Our results show that proprioceptive loss influences perception, motor control and adaptation but that proprioception from the moving limb is not essential for adaptation to, or detection of, force fields. The differences in learning and retention seen between the three deafferented participants suggest that they achieve these tasks in idiosyncratic ways after proprioceptive loss, possibly integrating visual and vestibular information with individual cognitive strategies.