Structural Learning Benefits in a Visuomotor Adaptation Task Generalize to a Contralateral Effector.

Structural learning is characterized by facilitated adaptation following training on a set of sensory perturbations all belonging to the same structure (e.g., 'visuomotor rotations'). This generalization of learning is a core feature of the motor system and is often studied in the context of interlimb transfer. However, such transfer has only been demonstrated when participants learn to counter a specific perturbation in the sensory feedback of their movements; we determined whether structural learning in one limb generalized to the contralateral limb. We trained 13 participants to counter random visual feedback rotations between +/-90 degrees with the right hand and subsequently tested the left hand on a fixed rotation. The structural training group showed faster adaptation in the left hand in both feedforward and feedback components of reaching compared to 13 participants who trained with veridical reaching, with lower initial reaching error, and straighter, faster, and smoother movements than in the control group. The transfer was ephemeral - benefits were confined to roughly the first 20 trials. The results demonstrate that the motor system can extract invariant properties of seemingly random environments in one limb, and that this information can be accessed by the contralateral limb.

Responsiveness to exoskeleton loading during bimanual reaching is associated with corticospinal tract integrity in stroke.

Background: Device-based rehabilitation of upper extremity impairment following stroke often employs one-sized-fits-all approaches that do not account for individual differences in patient characteristics. Objective: Determine if corticospinal tract lesion load could explain individual differences in the responsiveness to exoskeleton loading of the arms in chronic stroke participants. Methods: Fourteen stroke participants performed a bimanual shared cursor reaching task in virtual reality while exoskeletons decreased the effective weight of the more-impaired arm and increased the effective weight of the less-impaired arm. We calculated the change in relative displacement between the arms (RC) and the change in relative muscle activity (MC) between the arms from the biceps and deltoids. We calculated corticospinal tract lesion load (wCSTLL) in a subset of 10 participants. Results: Exoskeleton loading did not change RC (p = 0.07) or MC (p = 0.47) at the group level, but significant individual differences emerged. Participants with little overlap between the lesion and corticospinal tract responded to loading by decreasing muscle activity in the more-impaired arm relative to the less-impaired arm. The change in deltoid MC was associated with smaller wCSTLL (R2 = 0.43, p = 0.039); there was no such relationship for biceps MC (R2 < 0.001, p = 0.98). Conclusion: Here we provide evidence that corticospinal tract integrity is a critical feature that determines one's ability to respond to upper extremity exoskeleton loading. Our work contributes to the development of personalized device-based interventions that would allow clinicians and researchers to titrate constraint levels during bimanual activities.

Facilitated adaptation via structural learning increases bimanual interference.

Bimanual coordination is an essential feature of the motor system, yet interactions between the limbs during independent control remain poorly understood. Interference between the two hands, or the assimilation of movement characteristics between the two effectors, can be induced by perturbing one arm (e.g., via visuomotor rotation) and then measuring the effects in the contralateral limb. In this study, we sought to further determine the role adaptation plays in bimanual interference using a structural learning paradigm to alter feedback regulation in reaching. We trained healthy participants to counter 60 unique random rotations in right hand visual feedback over 240 reaches. Following this, we assessed feedforward and feedback measures of interference in a bimanual reaching task where the right hand was exposed to a fixed visual feedback rotation while the left hand reached without visual feedback. We found that participants who had been exposed to the structural training task in the right hand showed increased left hand interference during the first 20 trials of the test task. Moreover, interference was greater in feedback, rather than feedforward control parameters. The results further suggest that structural learning enhances bimanual interference via sensory feedback upregulation.

A trade-off between kinematic and dynamic control of bimanual reaching in virtual reality.

Bimanual coordination is an essential component of human movement. Cooperative bimanual reaching tasks are widely used to assess the optimal control of goal-directed reaching. However, little is known about the neuromuscular mechanisms governing these tasks. Twelve healthy, right-handed participants performed a bimanual reaching task in a three-dimensional virtual reality environment. They controlled a shared cursor, located at the midpoint between the hands, and reached targets located at 80% of full arm extension. Following a baseline of normal reaches, we placed a wrist weight on one arm and measured the change in coordination. Relative contribution (RC) was computed as the displacement of the right hand divided by the sum of displacements of both hands. We used surface electromyography placed over the anterior deltoid and biceps brachii to compute muscle contribution (MC) from root mean squared muscle activity data. We found RC was no different than 50% during baseline, indicating participants reached equal displacements when no weights were applied. Participants systematically altered limb coordination in response to altered limb dynamics. RC increased by 0.91% and MC decreased by 5.3% relative to baseline when the weight was applied to the left arm; RC decreased by 0.94% and MC increased by 6.3% when the weight was applied to the right arm. Participants adopted an optimal control strategy that attempted to minimize both kinematic and muscular asymmetries between limbs. What emerged was a trade-off between these two parameters, and we propose this trade-off as a potential neuromuscular mechanism of cooperative bimanual reaching.NEW & NOTEWORTHY This study is the first to propose a trade-off between kinematic and dynamic control parameters governing goal-directed reaching. We propose a straightforward tool to assess this trade-off without the need for computational modeling. The technologies and techniques developed in this study are discussed in the context of upper extremity rehabilitation.

Bimanual Interference Increases with Force Demands and is Facilitated by Visuomotor Adaptation.

When simultaneously performing asymmetrical movements with both hands, there is a tendency for the action of one limb to interfere with control of the other. Little is known about how sensory feedback influences interference. We conducted two experiments to determine how manipulating force feedback and visual feedback alter bimanual coordination during center-out reaching. In the adaptive experiment, asymmetrical reaching was induced by a visual feedback rotation for the right hand while the left hand operated under kinesthetic control (i.e., without visual feedback); in the non-adaptive experiment, asymmetrical reaching was induced by having participants move their right hand to rotated targets under veridical visual feedback, again with the left hand operating under kinesthetic control. In both experiments, we applied a spring resistive force to each hand, with different groups of participants experiencing 0 N/m, 30 N/m, or 60 N/m of resistance. In the adaptive experiment, interference increased with an increase in the force demands for movement in a dose-response fashion (i.e., the higher the resistive force, the larger the interference), but this result did not hold generally for the non-adaptive experiment. Our results indicate that adapting to a visuomotor perturbation may increase sensitivity to feedback gains, including to sensory information not present in the perturbation. Additionally, interference may reflect the application of an explicit strategy used for one limb to control the other, and the addition of an implicit adapting process may bolster this communication of motor information across motor cortices.

Neurophysiological Correlates of Adaptation and Interference during Asymmetrical Bimanual Movements.

In this study, we investigated brain dynamics during interference between hands during bimanual movements. Participants performed a bimanual center-out reaching task in which a visuomotor rotation was applied to the right hand while the left hand did not receive visual feedback of its movements. This manipulation resulted in interference from the adapting right hand to the kinesthetically guided left hand. Electroencephalography (EEG) recordings during the task showed that spectral power in the high and low beta frequency bands was elevated early in exposure, but decreased throughout learning. This may be representative of error-based updating of internal models of movement. Additionally, coherence, a measure of neural functional connectivity, was elevated both within and between hemispheres in the beta frequencies during the initial presentation of the visuomotor rotation, and then decreased throughout adaptation. This suggests that beta oscillatory neural activity may be marker for transmission of conflicting motor information between hemispheres, which manifests in interference between the hands during asymmetrical bimanual movements.