Interlimb Transfer Research Articles

Somatosensory Electrical Stimulation Does Not Augment Motor Skill Acquisition and Intermanual Transfer in Healthy Young Adults—A Pilot Study

Sensory input can modify motor function and magnify interlimb transfer. We examined the effects of low-intensity somatosensory electrical stimulation (SES) on motor practice-induced skill acquisition and intermanual transfer. Participants practiced a visuomotor skill for 25min and received SES to the practice or the transfer arm. Responses to single- and double-pulse transcranial magnetic stimulation were measured in both extensor carpi radialis. SES did not further increase skill acquisition (motor practice with right hand [RMP]: 30.8% and motor practice with right hand + somatosensory electrical stimulation to the right arm [RMP + RSES]: 27.8%) and intermanual transfer (RMP: 13.6% and RMP + RSES: 9.8%) when delivered to the left arm (motor practice with right hand + somatosensory electrical stimulation to the left arm [RMP + LSES]: 44.8% and 18.6%, respectively). Furthermore, transcranial magnetic stimulation measures revealed no changes in either hand. Future studies should systematically manipulate SES parameters to better understand the mechanisms of how SES affords motor learning benefits documented but not studied in patients.

Inter-limb transfer of kinematic adaptation in individuals with motor difficulties.

A previous study suggested that adults with greater motor difficulties demonstrated less adaptation under a regular error feedback schedule (gain=1:1) but reached a similar level of adaptation compared to controls when feedback was enhanced (gain=1:2). In light of these findings, the present study examined inter-limb transfer after adults adapted to visuomotor distortions with their dominant hand on either regular or enhanced feedback schedules. Results revealed that successful transfer related to the magnitude of adaptation with their dominant hand regardless of the individuals' motor abilities on the regular feedback schedule. When the feedback was enhanced, the transfer was not related to either the adaptation of the dominant hand or individuals' motor abilities. We argue that a stable internal model is essential for inter-limb transfer in kinematic adaptation.

Interlimb transfer of motor skill learning during walking: No evidence for asymmetric transfer

Several studies have shown that learning a motor skill in one limb can transfer to the opposite limb—a phenomenon called as interlimb transfer. The transfer of motor skills between limbs, however, has shown to be asymmetric, where one side benefits to a greater extent than the other. While this phenomenon has been well-documented in the upper-extremity, evidence for interlimb transfer in the lower-extremity is limited and mixed. This study investigated the extent of interlimb transfer during walking, and tested whether this transfer was asymmetric using a foot trajectory-tracking paradigm that has been specifically used for gait rehabilitation. The paradigm involved learning a new gait pattern which required greater hip and knee flexion during the swing phase of the gait while walking on a treadmill. Twenty young adults were randomized into two equal groups, where one group (right-to-left: RL) practiced the task initially with the dominant right leg and the other group (left-to-right: LR) practiced the task initially with their non-dominant left leg. After training, both groups practiced the task with their opposite leg to test the transfer effects. The changes in tracking error on each leg were computed to quantify learning and transfer effects. The results indicated that practice with one leg improved the motor performance of the other leg; however, the amount of transfer was similar across groups, indicating that there was no asymmetry in transfer. This finding is contradictory to most upper-extremity studies (where asymmetric transfer has been reported) and points out that both differences in neural processes and types of tasks may mediate interlimb transfer.

Structural and Functional Cortical Connectivity Mediating Cross Education of Motor Function.

Cross-education (CE) is the process whereby training with one limb leads to subsequent improvement in performance by the opposite untrained limb. We used multimodal neuroimaging in humans to investigate the mediating neural mechanisms by relating quantitative estimates of functional and structural cortical connectivity to individual levels of interlimb transfer. Resting-state (rs)-fMRI and diffusion weighted imaging (DWI) scans were undertaken before unilateral ballistic wrist flexion training. The rs-fMRI sequence was repeated immediately afterward. The increase in performance of the untrained limb was 83.6% of that observed for the trained limb and significantly greater than that of a control group who undertook no training. Functional connectivity in the resting motor network between right and left supplementary motor areas (SMA) was elevated after training. These changes were not, however, correlated with individual levels of transfer. Analysis of the DWI data using constrained spherical deconvolution-based tractography indicated that fractional anisotropy and apparent fiber density in tracts connecting bilateral SMA were negatively correlated with and predictive of transfer. The findings suggest that interhemispheric interactions between bilateral SMA play an instrumental role in CE and that the structural integrity of the connecting white matter pathways influences the level of transfer.SIGNIFICANCE STATEMENT Strength or skill training with one limb also brings about improvements in the performance of the opposite, untrained limb. This phenomenon, termed cross-education (CE), has obvious potential for the rehabilitation of functional capacity that has been lost through brain insult or musculoskeletal injury. The neural mechanisms that give rise to CE are, however, poorly understood. We used a combination of neuroimaging methods to investigate the pathways in the human brain that mediate CE. We determined that the supplementary motor area (SMA) plays an important role in the interlimb transfer of performance gains and demonstrate that the quality of the white matter fibers connecting right and left SMA predicts the benefit that an individual derives from CE.

Cerebellar-M1 Connectivity Changes Associated with Motor Learning Are Somatotopic Specific.

One of the functions of the cerebellum in motor learning is to predict and account for systematic changes to the body or environment. This form of adaptive learning is mediated by plastic changes occurring within the cerebellar cortex. The strength of cerebellar-to-cerebral pathways for a given muscle may reflect aspects of cerebellum-dependent motor adaptation. These connections with motor cortex (M1) can be estimated as cerebellar inhibition (CBI): a conditioning pulse of transcranial magnetic stimulation delivered to the cerebellum before a test pulse over motor cortex. Previously, we have demonstrated that changes in CBI for a given muscle representation correlate with learning a motor adaptation task with the involved limb. However, the specificity of these effects is unknown. Here, we investigated whether CBI changes in humans are somatotopy specific and how they relate to motor adaptation. We found that learning a visuomotor rotation task with the right hand changed CBI, not only for the involved first dorsal interosseous of the right hand, but also for an uninvolved right leg muscle, the tibialis anterior, likely related to inter-effector transfer of learning. In two follow-up experiments, we investigated whether the preparation of a simple hand or leg movement would produce a somatotopy-specific modulation of CBI. We found that CBI changes only for the effector involved in the movement. These results indicate that learning-related changes in cerebellar-M1 connectivity reflect a somatotopy-specific interaction. Modulation of this pathway is also present in the context of interlimb transfer of learning.SIGNIFICANCE STATEMENT Connectivity between the cerebellum and motor cortex is a critical pathway for the integrity of everyday movements and understanding the somatotopic specificity of this pathway in the context of motor learning is critical to advancing the efficacy of neurorehabilitation. We found that adaptive learning with the hand affects cerebellar-motor cortex connectivity, not only for the trained hand, but also for an untrained leg muscle, an effect likely related to intereffector transfer of learning. Furthermore, we introduce a novel method to measure cerebellar-motor cortex connectivity during movement preparation. With this technique, we show that, outside the context of learning, modulation of cerebellar-motor cortex connectivity is somatotopically specific to the effector being moved.

Experiencing a reaching task passively with one arm while adapting to a visuomotor rotation with the other can lead to substantial transfer of motor learning across the arms

The extent of transfer following visuomotor adaptation across the arms is typically limited as compared to that within the same arm. However, we have demonstrated that interlimb transfer can occur nearly completely if one arm performs reaching movements associated with a desired trajectory repeatedly and actively during an initial training session in which the other arm adapts to a novel visuomotor adaptation. Based on that finding, we argued that the absence of instances associated with specific motor effectors is the major reason for limited interlimb transfer. Here, we examined whether providing movement instances associated with one arm passively while adapting to a visuomotor rotation with the opposite arm could also lead to a greater extent of interlimb transfer. We had subjects perform reaching movements either actively or passively with the right arm while adapting to a 30° visuomotor rotation with the left arm (training session), and then had them perform reaching movements under the rotation condition with the right arm (transfer session). Results showed that the extent of transfer observed in the active and the passive training groups was significantly greater than that observed in a control group who only experienced the testing session. This finding suggests that providing effector-specific instances can increase the extent of interlimb transfer substantially, regardless of whether the instances are provided actively or passively. The current finding may have implications for neurorehabilitation targeted for individuals with motor impairment, such as persons with stroke or spinal cord injury.

Lateralized motor control processes determine asymmetry of interlimb transfer

This experiment tested the hypothesis that interlimb transfer of motor performance depends on recruitment of motor control processes that are specialized to the hemisphere contralateral to the arm that is initially trained. Right-handed participants performed a single-joint task, in which reaches were targeted to 4 different distances. While the speed and accuracy was similar for both hands, the underlying control mechanisms used to vary movement speed with distance were systematically different between the arms: the amplitude of the initial acceleration profiles scaled greater with movement speed for the right-dominant arm, while the duration of the initial acceleration profile scaled greater with movement speed for the left-non-dominant arm. These two processes were previously shown to be differentially disrupted by left and right hemisphere damage, respectively. We now hypothesize that task practice with the right arm might reinforce left-hemisphere mechanisms that vary acceleration amplitude with distance, while practice with the left arm might reinforce right-hemisphere mechanisms that vary acceleration duration with distance. We thus predict that following right arm practice, the left arm should show increased contributions of acceleration amplitude to peak velocities, and following left arm practice, the right arm should show increased contributions of acceleration duration to peak velocities. Our findings support these predictions, indicating that asymmetry in interlimb transfer of motor performance, at least in the task used here, depends on recruitment of lateralized motor control processes.

A positive association between active lifestyle and hemispheric lateralization for motor control and learning in older adults

Physical activity (PA) is well known to have general health benefits for older adults, but it is unclear whether it can also positively affect brain function involved in motor control and learning. We have previously shown that interlimb transfer of visuomotor adaptation occurs asymmetrically in young adults, while that occurs symmetrically in older adults, which suggests that the lateralized function of each hemisphere during motor tasks is diminished with aging. Here, we investigated the association between the level of PA and hemispheric motor lateralization by comparing the pattern of interlimb transfer following visuomotor adaptation between physically active and inactive older adults. Subjects were divided into two groups based on their PA level (active, inactive). They were further divided into two groups, such that a half of the subjects in each group adapted to a 30° rotation during targeted reaching movements with the left arm first, then with the right arm; and the other half with the right arm first, then with the left arm. Results indicated asymmetrical transfer (from left to right only) in the active subjects, whereas symmetrical transfer (from left to right, and vice versa) was observed in the inactive subjects. These findings suggest that older adults who maintain active lifestyle have a central nervous system that is more intact in terms of its lateralized motor function as compared with those who are inactive.

Effect of coordinate frame compatibility on the transfer of implicit and explicit learning across limbs.

Insights into the neural representation of motor learning can be obtained by investigating how learning transfers to novel task conditions. We recently demonstrated that visuomotor rotation learning transferred strongly between left and right limbs when the task was performed in a sagittal workspace, which afforded a consistent remapping for the two limbs in both extrinsic and joint-based coordinates. In contrast, transfer was absent when performed in horizontal workspace, where the extrinsically defined perturbation required conflicting joint-based remapping for the left and right limbs. Because visuomotor learning is thought to be supported by both implicit and explicit forms of learning, however, it is unclear to what extent these distinct forms of learning contribute to interlimb transfer. In this study, we assessed the degree to which interlimb transfer, following visuomotor rotation training, reflects explicit vs. implicit learning by obtaining verbal reports of participants' aiming direction before each movement. We also determined the extent to which these distinct components of learning are constrained by the compatibility of coordinate systems by comparing transfer between groups of participants who reached to targets arranged in the horizontal and sagittal planes. Both sagittal and horizontal conditions displayed complete transfer of explicit learning to the untrained limb. In contrast, transfer of implicit learning was incomplete, but the sagittal condition showed greater transfer than the horizontal condition. These findings suggest that explicit strategies developed with one limb can be fully implemented in the opposite limb, whereas implicit transfer depends on the degree to which new sensorimotor maps are spatially compatible for the two limbs.

Neural Adaptations Associated with Interlimb Transfer in a Ballistic Wrist Flexion Task.

Cross education is the process whereby training of one limb gives rise to increases in the subsequent performance of its opposite counterpart. The execution of many unilateral tasks is associated with increased excitability of corticospinal projections from primary motor cortex (M1) to the opposite limb. It has been proposed that these effects are causally related. Our aim was to establish whether changes in corticospinal excitability (CSE) arising from prior training of the opposite limb determine levels of interlimb transfer. We used three vision conditions shown previously to modulate the excitability of corticospinal projections to the inactive (right) limb during wrist flexion movements performed by the training (left) limb. These were: (1) mirrored visual feedback of the training limb; (2) no visual feedback of either limb; and (3) visual feedback of the inactive limb. Training comprised 300 discrete, ballistic wrist flexion movements executed as rapidly as possible. Performance of the right limb on the same task was assessed prior to, at the mid point of, and following left limb training. There was no evidence that variations in the excitability of corticospinal projections (assessed by transcranial magnetic stimulation (TMS)) to the inactive limb were associated with, or predictive of, the extent of interlimb transfer that was expressed. There were however associations between alterations in muscle activation dynamics observed for the untrained limb, and the degree of positive transfer that arose from training of the opposite limb. The results suggest that the acute adaptations that mediate the bilateral performance gains realized through unilateral practice of this ballistic wrist flexion task are mediated by neural elements other than those within M1 that are recruited at rest by single-pulse TMS.

Peripheral neuropathy reduces asymmetries in inter-limb transfer in a visuo-motor task

ABSTRACTAsymmetry of inter-limb transfer has been associated with the specialization of the dominant and non-dominant motor system. Reductions of asymmetry have been interpreted as behavioural evidence showing a decline of hemispheric lateralization. A previous study showed that ageing did not qualitatively change the inter-limb transfer asymmetry of a visuo-motor task. The current study elaborates on these findings; it examines whether diminished somatosensory information as a result of peripheral neuropathy (PN) adversely affects inter-limb transfer asymmetry. Twenty individuals affected by PN and 20 older controls were recruited and divided equally across two groups. One group trained a visuo-motor task with the right hand while the other group trained it with the left hand. Performance (initial direction error) of the untrained hand before and after training was collected to determine learning effects from inter-limb transfer. Similar to previous studies, the current study showed asymmetric inter-limb transfer in older controls. In contrast, PN showed inter-limb transfer in both directions indicating that PN reduces inter-limb transfer asymmetry. Increased bilateral hemispheric recruitment is suggested to be responsible for this reduced asymmetry which may compensate for deteriorated tactile and/or proprioceptive inputs in PN. Two possible hypotheses are discussed explaining the relationship between declined somatosensory information and increases in bilateral hemispheric recruitment.

Generalization of force-field adaptation in proprioceptively-deafferented subjects

Humans have the remarkable ability to adapt their motor behaviour to changes in body properties and/or environmental conditions, based on sensory feedback such as vision and proprioception. The role of proprioception has been highlighted for the adaptation to new upper-limb dynamics, which is known to generalize to the opposite, non-adapted limb in healthy individuals. Such interlimb transfer seems to depend on sensory feedback, and the present study assessed whether the chronic loss of proprioception precludes interlimb transfer of dynamic adaptation by testing two well-characterized proprioceptively-deafferented subjects. These had to reach toward visual targets with vision of the limb. For both deafferented subjects, we observed adaptation of the dominant arm to Coriolis forces and after-effects on non-dominant arm movements in different movement directions, thus indicating interlimb transfer. Overall, our findings show that motor learning can generalize across limbs and movement directions despite the loss of proprioceptive afferents.

What Do TMS-Evoked Motor Potentials Tell Us About Motor Learning?

Thirty years ago, the first magnetic device capable of stimulating the human brain without discomfort through the intact skull was unveiled in Sheffield, England (Barker et al. in Lancet 1:1106-1107, 1985). Since that time, transcranial magnetic stimulation (TMS) has become the tool of choice for many scientists investigating human motor control and learning. In light of the fact that there are limits to the information that can be provided by any experimental technique, we first make the case that the necessarily restricted explanatory scope of the TMS technique-and the motor-evoked potentials to which it gives rise, is not yet reflected adequately in the research literature. We also argue that this inattention, coupled with the pervasive adoption of TMS as an investigative tool, may be restricting the elaboration of knowledge concerning the neural processes that mediate human motor learning. In order to make these points, we use as an exemplar the study of cross-education-the interlimb transfer of functional capacity.

Direct and crossed effects of somatosensory electrical stimulation on motor learning and neuronal plasticity in humans.

PurposeSensory input can modify voluntary motor function. We examined whether somatosensory electrical stimulation (SES) added to motor practice (MP) could augment motor learning, interlimb transfer, and whether physiological changes in neuronal excitability underlie these changes.MethodsParticipants (18–30 years, n = 31) received MP, SES, MP + SES, or a control intervention. Visuomotor practice included 300 trials for 25 min with the right-dominant wrist and SES consisted of weak electrical stimulation of the radial and median nerves above the elbow. Single- and double-pulse transcranial magnetic stimulation (TMS) metrics were measured in the intervention and non-intervention extensor carpi radialis.ResultsThere was 27 % motor learning and 9 % (both p < 0.001) interlimb transfer in all groups but SES added to MP did not augment learning and transfer. Corticospinal excitability increased after MP and SES when measured at rest but it increased after MP and decreased after SES when measured during contraction. No changes occurred in intracortical inhibition and facilitation. MP did not affect the TMS metrics in the transfer hand. In contrast, corticospinal excitability strongly increased after SES with MP + SES showing sharply opposite of these effects.ConclusionMotor practice and SES each can produce motor learning and interlimb transfer and are likely to be mediated by different mechanisms. The results provide insight into the physiological mechanisms underlying the effects of MP and SES on motor learning and cortical plasticity and show that these mechanisms are likely to be different for the trained and stimulated motor cortex and the non-trained and non-stimulated motor cortex.

To transfer or not to transfer? Kinematics and laterality quotient predict interlimb transfer of motor learning.

Humans can remarkably adapt their motor behavior to novel environmental conditions, yet it remains unclear which factors enable us to transfer what we have learned with one limb to the other. Here we tested the hypothesis that interlimb transfer of sensorimotor adaptation is determined by environmental conditions but also by individual characteristics. We specifically examined the adaptation of unconstrained reaching movements to a novel Coriolis, velocity-dependent force field. Right-handed subjects sat at the center of a rotating platform and performed forward reaching movements with the upper limb toward flashed visual targets in prerotation, per-rotation (i.e., adaptation), and postrotation tests. Here only the dominant arm was used during adaptation and interlimb transfer was assessed by comparing performance of the nondominant arm before and after dominant-arm adaptation. Vision and no-vision conditions did not significantly influence interlimb transfer of trajectory adaptation, which on average was significant but limited. We uncovered a substantial heterogeneity of interlimb transfer across subjects and found that interlimb transfer can be qualitatively and quantitatively predicted for each healthy young individual. A classifier showed that in our study, interlimb transfer could be predicted based on the subject's task performance, most notably motor variability during learning, and his or her laterality quotient. Positive correlations suggested that variability of motor performance and lateralization of arm movement control facilitate interlimb transfer. We further show that these individual characteristics can predict the presence and the magnitude of interlimb transfer of left-handers. Overall, this study suggests that individual characteristics shape the way the nervous system can generalize motor learning.

Limb Dominance and Its Effects on the Benefits of Intralimb Transfer of Learning: A Visuomotor Aiming Task

ABSTRACT Research has attempted to address what characteristics benefit from transfer of learning; however, it is still unclear which characteristics are effector dependent or independent. Furthermore, it is not clear if intralimb transfer shows, similarly to interlimb transfer, an asymmetry of benefits between the upper limbs. The purpose of the current study is to examine if effector independence effects emerge, as observed in interlimb transfer studies, when transfer to new effector group within the same limb occurs, and whether the pattern of intralimb transfer benefits differ between the limbs. Our results suggest that a visuomotor task transfers within both limbs, even though the transfer benefits within the limbs seem to differ. This was supported by more transfer occurring in the dominant limb than the nondominant limb. Potential control mechanisms used for intralimb transfer are discussed.

Inter-limb transfer of both simple and complex motor skills is maintained in elderly adults

Inter-limb transfer refers to the phenomenon whereby unilateral motor-skill training induces performance gains in both the trained limb and in the opposite, untrained limb. Evidence indicates that older adults exhibit a reduction in the capacity for inter-limb transfer following training on a simple ballistic movement task, but not after training on a complex task. Evidence also suggests that age-related over-activity in bilateral motor cortices may underlie the differential inter-limb transfer evident after simple and complex tasks in elderly adults.

Performing a reaching task with one arm while adapting to a visuomotor rotation with the other can lead to complete transfer of motor learning across the arms.

The extent to which motor learning is generalized across the limbs is typically very limited. Here, we investigated how two motor learning hypotheses could be used to enhance the extent of interlimb transfer. According to one hypothesis, we predicted that reinforcement of successful actions by providing binary error feedback regarding task success or failure, in addition to terminal error feedback, during initial training would increase the extent of interlimb transfer following visuomotor adaptation (experiment 1). According to the other hypothesis, we predicted that performing a reaching task repeatedly with one arm without providing performance feedback (which prevented learning the task with this arm), while concurrently adapting to a visuomotor rotation with the other arm, would increase the extent of transfer (experiment 2). Results indicate that providing binary error feedback, compared with continuous visual feedback that provided movement direction and amplitude information, had no influence on the extent of transfer. In contrast, repeatedly performing (but not learning) a specific task with one arm while visuomotor adaptation occurred with the other arm led to nearly complete transfer. This suggests that the absence of motor instances associated with specific effectors and task conditions is the major reason for limited interlimb transfer and that reinforcement of successful actions during initial training is not beneficial for interlimb transfer. These findings indicate crucial contributions of effector- and task-specific motor instances, which are thought to underlie (a type of) model-free learning, to optimal motor learning and interlimb transfer.

Mirror illusion reduces motor cortical inhibition in the ipsilateral primary motor cortex during forceful unilateral muscle contractions.

Forceful, unilateral contractions modulate corticomotor paths targeting the resting, contralateral hand. However, it is unknown whether mirror-viewing of a slowly moving but forcefully contracting hand would additionally affect these paths. Here we examined corticospinal excitability and short-interval intracortical inhibition (SICI) of the right-ipsilateral primary motor cortex (M1) in healthy young adults under no-mirror and mirror conditions at rest and during right wrist flexion at 60% maximal voluntary contraction (MVC). During the no-mirror conditions neither hand was visible, whereas in the mirror conditions participants looked at the right hand's reflection in the mirror. Corticospinal excitability increased during contractions in the left flexor carpi radialis (FCR) (contraction 0.41 mV vs. rest 0.21 mV) and extensor carpi radialis (ECR) (contraction 0.56 mV vs. rest 0.39 mV), but there was no mirror effect (FCR: P = 0.743, ηp (2) = 0.005; ECR: P = 0.712, ηp (2) = 0.005). However, mirror-viewing of the contracting and moving wrist attenuated SICI relative to test pulse in the left FCR by ∼9% compared with the other conditions (P < 0.05, d ≥ 0.62). Electromyographic activity in the resting left hand prior to stimulation was not affected by the mirror (FCR: P = 0.255, ηp (2) = 0.049; ECR: P = 0.343, ηp (2) = 0.035) but increased twofold during contractions. Thus viewing the moving hand in the mirror and not just the mirror image of the nonmoving hand seems to affect motor cortical inhibitory networks in the M1 associated with the mirror image. Future studies should determine whether the use of a mirror could increase interlimb transfer produced by cross-education, especially in patient groups with unilateral orthopedic and neurological conditions.

Specialization in interlimb transfer between dominant and non-dominant hand skills.

[Purpose] This study aimed to confirm the specialization of interlimb transfer in occupationally embedded tasks between dominant and non-dominant hands. [Subjects] Twelve neurologically intact participants were recruited. [Methods] The participants were divided into two training groups and performed training with their dominant or non-dominant hand. Three subtests of the Jebsen-Taylor Hand Function Test were used to practice interlimb transfer training in each group. All Jebsen-Taylor Hand Function Test subtests were evaluated using the untrained hand before and after 5 days of training. [Results] The dominant hand group showed significant differences after training when using the untrained hand in the simulated feeding and lifting large heavy objects subtests. Meanwhile, the non-dominant hand group showed significant differences after training when using the untrained hand in the turning cards, simulated feeding, stacking checkers, and lifting large heavy objects subtests. [Conclusion] When performing occupationally embedded tasks, the dominant hand has interlimb transfer advantages with respect to predictable dynamic movements, while the non-dominant hand has interlimb transfer advantages in stabilization.