Effect of repeated explicit instructions on visuomotor adaptation and intermanual transfer.

The aim of the present study was to investigate the effect of repeated explicit instructions on visuomotor adaptation, awareness, and intermanual transfer. In a comprehensive study design, 48 participants performed center-out reaching movements before and during exposure to a 60° rotation of visual feedback. Awareness and intermanual transfer were then determined. Twelve participants each were assigned to one of the following adaptation conditions: gradual adaptation, sudden adaptation without instructions, sudden adaptation with a single instruction before adaptation, and sudden adaptation with multiple instructions before and during adaptation. The explicit instructions explained the nature of the visual feedback perturbation and were given using an illustration of a clock face. Analysis of adaptation indices revealed neither increased nor decreased adaptation after repeated instructions compared with a single instruction. In addition, we found significant group differences for the awareness index, with lower awareness after gradual adaptation than after sudden, instructed adaptation. Our data also show increased initial adaptation in aware participants; regardless of whether awareness was developed independently or with instruction. Intermanual transfer did not differ between groups. However, we found a significant correlation between the awareness and intermanual transfer indices. We conclude that the magnitude of the explicit process cannot be further increased by repeated instruction and that intermanual transfer appears to be largely related to the explicit adaptation process.

Methods matter: Your measures of explicit and implicit processes in visuomotor adaptation affect your results.

Visuomotor rotations are frequently used to study the different processes underlying motor adaptation. Explicit aiming strategies and implicit recalibration are two of these processes. Various methods, which differ in their underlying assumptions, have been used to dissociate the two processes. Direct methods, such as verbal reports, assume explicit knowledge to be verbalizable, where indirect methods, such as the exclusion, assume that explicit knowledge is controllable. The goal of this study was thus to directly compare verbal reporting with exclusion in two different conditions: during consistent reporting and during intermittent reporting. Our results show that our two conditions lead to a dissociation between the measures. In the consistent reporting group, all measures showed similar results. However, in the intermittent reporting group, verbal reporting showed more explicit re-aiming and less implicit adaptation than exclusion. Curiously, when exclusion was measured again, after the end of learning, the differences were no longer apparent. We suspect this may reflect selective decay in implicit adaptation, as has been reported previously. All told, our results clearly indicate that methods of measurement can affect the amount of explicit re-aiming and implicit adaptation that is measured. Since it has been previously shown that both explicit re-aiming and implicit adaptation have multiple components, discrepancies between these different methods may arise because different measures reflect different components.

Martial arts training is related to implicit intermanual transfer of visuomotor adaptation.

Recent work identified an explicit and implicit transfer of sensorimotor adaptation with one limb to the other, untrained limb. Here, we pursue the idea that different individual factors contribute differently to the amount of explicit and implicit intermanual transfer. In particular, we tested a group of judo athletes who show enhanced right-hemispheric involvement in motor control and a group of equally trained athletes. After adaptation to a 60° visual rotation, we estimated awareness of the perturbation and transfer to the untrained, non-dominant left hand in two experiments. We measured the total amount of intermanual transfer (explicit plus implicit) by telling the participants to repeat what was learned during adaptation, and the amount of implicit transfer by instructing the participants to refrain from using what was learned and to perform movements as during baseline instead. We found no difference between the total intermanual transfer of judokas and running experts, with mean absolute transfer values of 42.4° and 47.0°. Implicit intermanual transfer was very limited, but larger in judokas than in general sports athletes, with mean values of 5.2° and 1.6°. A multiple linear regression analysis further revealed that total intermanual transfer, which mainly represents the explicit transfer, is related to awareness of the perturbation, while implicit intermanual transfer can be predicted by judo training, amount of total training, speed of adaptation, and handedness scores. The findings suggest that neuronal mechanisms such as hemispheric interactions and functional specialization underlying intermanual transfer of motor learning may be applied according to individual predisposition.

Neural correlates of adaptation to gradual and to sudden visuomotor distortions in humans.

This study aimed at scrutinizing the neural correlates of sensorimotor adaptation. Subjects were exposed either to a gradually (group G) or to a suddenly introduced perturbation (group S) followed by a test of aftereffects. They were also exposed to a control condition equated for their movement errors during the adaptation condition. We registered subjects' brain activity by functional magnetic resonance imaging. Behavioral data revealed no difference between aftereffects in G and S, while imaging data suggest different neural correlates. Direct comparison between groups showed more adaptation-related activation in left cingulate and inferior frontal as well as right caudate and temporal areas in S than in G. In contrast, no neural activity was related more to G than to S and no common activations were found for both groups. Within-group analyses further revealed right inferior parietal lobe, cerebellar and cingulate cortex activity in group S and activation of frontal lobe and left cerebellum in group G for a contrast between adaptation condition and baseline. Less brain activity was observed when controlled for movement errors: the contrast between adaptation and control condition yielded left occipital lobe activity in group S, and left posterior dentate nucleus and brainstem activity in group G. The present data confirm an involvement of the cerebellar cortex in error processing during sudden adaptation, since this activation was found for the contrast 'adaptation-baseline' but not for 'adaptation-control.' In addition, our data suggest an involvement of deep cerebellar nuclei in the adaptation to gradually introduced distortions.

Visuomotor adaptive improvement and aftereffects are impaired differentially following cerebellar lesions in SCA and PICA territory.

The aim of the present study was to elucidate the contribution of the superior and posterior inferior cerebellum to adaptive improvement and aftereffects in a visuomotor adaptation task. Nine patients with ischemic lesions within the territory of the posterior inferior cerebellar artery (PICA), six patients with ischemic lesions within the territory of the superior cerebellar artery (SCA) and 17 age-matched controls participated. All subjects performed center-out reaching movements under 60 degrees rotation of visual feedback. For the assessment of aftereffects, we tested retention of adaptation and de-adaptation under 0 degrees visual rotation. From this data we also quantified five measures of motor performance. Cerebellar lesion-symptom mapping was performed using magnetic resonance imaging subtraction analysis. Adaptive improvement during 60 degrees rotation was significantly degraded in PICA patients and even more in SCA patients. Subtraction analysis revealed that posterior (Crus I) as well as anterior cerebellar regions (lobule V) showed a common overlap related to deficits in adaptive improvement. However, for aftereffect measures as well as for motor performance variables only SCA patients, but not PICA patients showed significant differences to control subjects. Subtraction analysis showed that affection of lobules V and VI were more common in patients with impaired retention and de-adaptation, respectively. Data shows that areas both within the superior and posterior inferior cerebellum are involved in adaptive improvement. However, only the superior cerebellum including lobules V and VI appears to be important for aftereffects and therefore true adaptive ability.

The effect of cerebellar cortical degeneration on adaptive plasticity and movement control.

Clinical and neuroimaging studies provide converging evidence that the cerebellum plays an important role for sensorimotor adaptation by participating in the adaptive process per se, and/or by evaluating motor performance errors as a prerequisite for adaptation. Recent experimental evidence suggests that error signals pertinent to adaptation are related to sensory prediction rather than to online corrections (Tseng et al. in J Neurophysiol 98(1):54-62, 2007). To further elucidate the role of the cerebellum, the present study uses a multiple regression approach to separate out three independent determinants of adaptive success. Seventeen patients with cerebellar atrophy but without extra-cerebellar lesions, and 17 healthy, sex- and age-matched controls participated. Both subject groups performed center-out pointing movements before, during, and after exposure to 60 degrees rotated visual feedback. From the registered data, we quantified four indicators of adaptive success (adaptive improvement, retention without feedback, intermanual transfer, and de-adaptation under normal feedback), as well as five measures of motor performance (reaction time, peak velocity, movement time, response variability, and ability for online error corrections). The variance of each adaptation indicator was then partitioned into three components, one related to subject group but not to motor performance, a second related to group and motor performance, and a third related to motor performance but not to group. In accordance with previous work, adaptation and motor performance were degraded in patients. The deficit was similar in magnitude for all four adaptation indicators, which suggests that adaptive recalibration rather than strategic control were affected in our patients. No adaptation indicator shared statistically significant variance with group alone; we therefore found no evidence for cerebellar circuitry dedicated to adaptation but not motor performance. Three indicators shared significant variance jointly with group and motor performance; this suggests that the cerebellar contribution to motor performance is related to adaptive success. All four indicators shared significant variance with motor performance alone; this indicates that extracerebellar contributions to motor performance are also related to adaptive success. In conclusion, our data support the view that neural structures inside and outside the cerebellum are processing motor performance-related signals as a prerequisite for adaptation, but provide no evidence for a cerebellar structure related exclusively to adaptation.

Improved sensorimotor adaptation after exhaustive exercise is accompanied by altered brain activity.

Acute exercise has been shown to exhibit different effects on human sensorimotor behavior; however, the causes and mechanisms of the responses are often not clear. The primary aim of the present study was to determine the effects of incremental running until exhaustion on sensorimotor performance and adaptation in a tracking task. Subjects were randomly assigned to a running group (RG), a tracking group (TG), or a running followed by tracking group (RTG), with 10 subjects assigned to each group. Treadmill running velocity was initially set at 2.0 m s(-1), increasing by 0.5 m s(-1) every 5 min until exhaustion. Tracking consisted of 35 episodes (each 40 s) where the subjects' task was to track a visual target on a computer screen while the visual feedback was veridical (performance) or left-right reversed (adaptation). Resting electroencephalographic (EEG) activity was recorded before and after each experimental condition (running, tracking, rest). Tracking performance and the final amount of adaptation did not differ between groups. However, task adaptation was significantly faster in RTG compared to TG. In addition, increased alpha and beta power were observed following tracking in TG but not RTG although exhaustive running failed to induce significant changes in these frequency bands. Our results suggest that exhaustive running can facilitate adaptation processes in a manual tracking task. Attenuated cortical activation following tracking in the exercise condition was interpreted to indicate cortical efficiency and exercise-induced facilitation of selective central processes during actual task demands.

Intermanual transfer of visuomotor adaptation is related to awareness.

Previous studies compared the effects of gradual and sudden adaptation on intermanual transfer to find out whether transfer depends on awareness of the perturbation. Results from different groups were contradictory. Since results of our own study suggest that awareness depends on perturbation size, we hypothesize that awareness-related intermanual transfer will only appear after adaptation to a large, sudden perturbation but not after adaptation to a small sudden perturbation or a gradual perturbation, large or small. To confirm this, four groups (S30, G30, S75, G75) of subjects performed out-and-back reaching movements with their right arm. In a baseline block, they received veridical visual feedback of hand position. In the subsequent adaptation block, feedback was rotated by 30 deg (S30, G30) or 75 deg (S75, G75). This rotation was either introduced suddenly (S30, S75) or gradually in steps of 3 deg (G30, G75). After the adaptation block, subjects did an awareness test comprising exclusion and inclusion conditions. The experiment concluded with an intermanual transfer block, in which movements were performed with the left arm under rotated feedback, and a washout block again under veridical feedback. We used a hierarchical Bayesian model to estimate individual movement directions and group averages. The movement directions in different conditions were then used to calculate group and individual indexes of adaptation, awareness, unawareness, transfer and washout. Both awareness and transfer were larger in S75 than in other groups, while unawareness and washout were smaller in S75 than in other groups. Furthermore, the size of awareness indices correlated to intermanual transfer across subjects, even when transfer was normalized to final adaptation level. Thus, we show for the first time that the amount of intermanual transfer directly relates to the extent of awareness of the learned perturbation.

Awareness of sensorimotor adaptation to visual rotations of different size.

Previous studies on sensorimotor adaptation revealed no awareness of the nature of the perturbation after adaptation to an abrupt 30° rotation of visual feedback or after adaptation to gradually introduced perturbations. Whether the degree of awareness depends on the magnitude of the perturbation, though, has as yet not been tested. Instead of using questionnaires, as was often done in previous work, the present study used a process dissociation procedure to measure awareness and unawareness. A naïve, implicit group and a group of subjects using explicit strategies adapted to 20°, 40° and 60° cursor rotations in different adaptation blocks that were each followed by determination of awareness and unawareness indices. The awareness index differed between groups and increased from 20° to 60° adaptation. In contrast, there was no group difference for the unawareness index, but it also depended on the size of the rotation. Early adaptation varied between groups and correlated with awareness: The more awareness a participant had developed the more the person adapted in the beginning of the adaptation block. In addition, there was a significant group difference for savings but it did not correlate with awareness. Our findings suggest that awareness depends on perturbation size and that aware and strategic processes are differentially involved during adaptation and savings. Moreover, the use of the process dissociation procedure opens the opportunity to determine awareness and unawareness indices in future sensorimotor adaptation research.

Adaptation to mirror-reversed vision is based on directionally tuned modules.

Sensorimotor adaptation to rotated visual feedback is thought to be achieved by directionally tuned modules. Here we scrutinize whether adaptation to reversed vision utilizes similar mechanisms. Specifically, we hypothesize that adaptive transfer to unpracticed target directions is determined by the superposition of neighboring modules. One group of subjects adapted to a left-right reversal of visual feedback, which requires a 180°, ±90°, or no change of response direction, depending on target position. Two groups of control subjects adapted to a 180° and to a 90° rotation of visual feedback. We found that adaptation to a left-right reversal is less efficient than adaptation to rotations requiring the same adaptive change, and attribute this decrement to an overlap of neighboring modules. We further found that transfer to unpracticed targets is well predicted by a simple Gaussian model. From this we conclude that adaptation to a left-right reversal emerges in a regional and interdependent fashion, and can be modeled as overlapping Gaussian tuned processes.

Mechanisms for visuomotor adaptation to left-right reversed vision.

Behavioral studies suggest that the adaptation of planar arm movements to rotated visual feedback is achieved by the interplay of a gradual process which slowly rotates participants' responses by up to +/-90 degrees , and a discrete process which changes the responses by means of axis inversion. The processes for adaptation to left-right reversed visual feedback are far less well understood. To clarify this issue, 12 healthy participants performed pointing movements to targets presented in eight different directions, before and during exposure to left-right reversed visual feedback. We quantified the direction of each response 150ms after movement onset and analyzed the time-course of those directions throughout the adaptation phase, separately for different targets. For targets along the axis of inversion, we only found an increase of response variability, for targets perpendicular to that axis, we observed a discrete 180 degrees change of response direction, and for diagonal targets, we found a discrete 180 degrees change followed by a gradual "backward" shift of 90 degrees . The present findings confirm that sensorimotor adaptation is based on discrete and gradual processes, that both types of processes can occur concurrently, and suggests that those processes can contribute to adaptation in a target-specific fashion.

Effects of variable practice and declarative knowledge on sensorimotor adaptation to rotated visual feedback.

It has been shown before that sensorimotor adaptation to rotated vision is more generalized when subjects point at eight, rather than at four or less targets. Here we evaluate whether an even more variable practice has additional benefits. One group of subjects pointed at eight targets, and another group executed unconstrained arm movements throughout the workspace. We found no advantage of the latter group with respect to adaptive progress, persistence of adaptation without visual feedback, or transfer of adaptation to a new motor task. We therefore concluded that eight targets are sufficient to yield generalized adaptation. To determine the role of declarative knowledge for sensorimotor adaptation, subjects from both above groups were questioned regarding the nature of the distortion after they completed the experiment. We found that correct responders showed better adaptive progress, more persistence, but the same transfer as incorrect responders. We therefore concluded that the benefit of declarative knowledge is task-specific and short-lived, and is therefore probably related to strategic control rather than to an adaptive recalibration of the sensorimotor system.