Visual target separation determines the extent of generalisation between opposing visuomotor rotations

Here we investigated the influence of angular separation between visual and motor targets on concurrent adaptation to two opposing visuomotor rotations. We inferred the extent of generalisation between opposing visuomotor rotations at individual target locations based on whether interference (negative transfer) was present. Our main finding was that dual adaptation occurred to opposing visuomotor rotations when each was associated with different visual targets but shared a common motor target. Dual adaptation could have been achieved either within a single sensorimotor map (i.e. with different mappings associated with different ranges of visual input), or by forming two different internal models (the selection of which would be based on contextual information provided by target location). In the present case, the pattern of generalisation was dependent on the relative position of the visual targets associated with each rotation. Visual targets nearest the workspace of the opposing visuomotor rotation exhibited the most interference (i.e. generalisation). When the minimum angular separation between visual targets was increased, the extent of interference was reduced. These results suggest that the separation in the range of sensory inputs is the critical requirement to support dual adaptation within a single sensorimotor mapping.     

Dual adaptation to opposing visuomotor rotations with similar hand movement trajectories

This research explored specific contextual cues that might facilitate human motor learning. Using a dual adaptation task, humans performed manual reaches to visual targets while experiencing a 30° clockwise or counterclockwise rotation, which randomly alternated between trials, of a seen cursor representing their unseen hand. Groups had different cues to distinguish between rotations: ‘Cue’ (colours and shapes), ‘Workspace’ (target locations) and ‘Workspace with Cue’ (combination of cues). Importantly, the workspace groups required similar hand movement trajectories to accurately acquire pairs of targets. Our data show that only the ‘Workspace’ and ‘Workspace with Cue’ groups, but not ‘Cue’ group, adapted to both rotations concurrently (dual adaption). These findings suggest that colour and shape cues, even when integrated with the end-effector and targets, do not facilitate dual adaptation. However, target separation is sufficient to facilitate dual adaptation, even when hand movement trajectories are similar. Interestingly, adaptation was less complete when required hand trajectories were completely overlapping for pairs of targets (versus being similar), suggesting an important role for the motor system as well. Nonetheless, the location of targets and consequent differences in motor planning may play a larger role in facilitating adaptation than previously thought.     

The efficacy of colour cues in facilitating adaptation to opposing visuomotor rotations

We investigated visuomotor adaptation using an isometric, target-acquisition task. Following trials with no rotation, two participant groups were exposed to a random sequence of 30° clockwise (CW) and 60° counter-clockwise (CCW) rotations, with (DUAL-CUE), or without (DUAL-NO CUE), colour cues that enabled each environment (non-rotated, 30° CW and 60° CCW) to be identified. A further three groups experienced only 30° CW trials or only 60° CCW trials (SINGLE rotation groups) in which each visuomotor mapping was again associated with a colour cue. During training, all SINGLE groups reduced angular deviations of the cursor path during the initial portion of the movements, indicating feedforward adaptation. Consistent with the view that the adaptation occurred automatically via recalibration of the visuomotor mapping (Krakauer et al. 1999), post-training aftereffects were observed, despite colour cues that indicated that no rotation was present. For the DUAL-CUE group, angular deviations decreased with training in the 60° trials, but were unchanged in the 30° trials, while for the DUAL-NO CUE group angular deviations decreased for the 60° CW trials but increased for the 30° CW trials. These results suggest that in a dual adaptation paradigm a colour cue can permit delineation of the two environments, with a subsequent change in behaviour resulting in improved performance in at least one of these environments. Increased reaction times within the training block, together with the absence of aftereffects in the post-training period for the DUAL-CUE group suggest an explicit cue-dependent strategy was used in an attempt to compensate for the rotations.     

Generalization of visuomotor adaptation depends on the spatial characteristic of visual workspace

The present study aims to address a novel aspect of visuomotor adaptation and its generalization. It is based on the assumption that the spatial structure of the distal action space is crucial for generalization. In the experiments, the distal action spaces could manifest either a symmetric or parallel structure. The imposed visuomotor rotations in the adaptation and the following generalization were either the same or opposing each other. In the generalization phase, motor bias resulting from prior adaptation was observed, and it turned out to substantially depend on the property of the workspace. In Experiment 1 with a parallel workspace, preceding adaptation to the same rotation was more advantageous than adaptation to an opposing rotation. This observation was reversed in Experiment 2 with the symmetrical workspace: prior adaptation to an opposing rotation was more advantageous for the generalization than prior adaptation to the same rotation. Mechanisms possibly underlying the observed influence of the workspace configuration were discussed.     

Random presentation enables subjects to adapt to two opposing forces on the hand

Studies have shown that humans cannot simultaneously learn opposing force fields or opposing visuomotor rotations, even when provided with arbitrary contextual information, probably because of interference in their working memory. In contrast, we found that subjects can adapt to two opposing force fields when provided with contextual cues and can consolidate motor memories if random and frequent switching occurs. Because significant aftereffects were seen, this study suggests that multiple internal models can be acquired simultaneously during learning and predictively switched, depending only on contextual information.     

Task-specific internal models for kinematic transformations

Numerous studies of motor learning have focused on how people adapt their reaching movements to novel dynamic and visuomotor perturbations that alter the actual or visually perceived motion of the hand. An important finding from this work is that learning of novel dynamics generalizes across different movement tasks. Thus adaptation to an unusual force field generalizes from center-out reaching movements to circular movements (Conditt et al. 1997). This suggests that subjects acquired an internal model of the dynamic environment that could be used to determine the motor commands needed for untrained movements. Using a task interference paradigm, we investigated whether transfer across tasks is also observed when learning visuomotor transformations. On day 1, all subjects adapted to a +30 degrees rotation while making center-out-and-back reaching movements. After a delay of 5 min, different groups of subjects then adapted to a -30 degrees rotation while performing either a continuous tracking task, a figure-eight drawing task, or the center-out-and-back reaching task. All subjects were then retested the next day on the +30 degrees rotation in the reaching task. As expected, subjects who experienced the opposing rotations while performing the same reaching tasks showed no retention of learning for the first rotation when tested on day 2 (Krakauer et al. 1999). In contrast, such retrograde interference was not observed in the two groups of subjects who experienced the opposing rotations while performing different tasks. In fact, their performance on day 2 was similar to that of control subjects who never experienced the opposite rotation. This lack of interference suggests that memory resources for visuomotor rotations are task specific.     

Visuomotor learning generalizes between bilateral and unilateral conditions despite varying degrees of bilateral interference

Bilateral interference, referring to the tendency of movements of one arm to disrupt the intended movements made simultaneously with the other arm, is often observed in a task that involves differential planning of each arm movement during sensorimotor adaptation. In the present study, we examined two questions: 1) how does the compatibility between visuomotor adaptation tasks performed with both arms affect bilateral interference during bimanual performance? and 2) how do variations in bilateral interference affect transfer of visuomotor adaptation between bilateral and unilateral conditions? To examine these questions, we manipulated visuomotor compatibility using two kinematic variables (direction of required hand motion, direction of an imposed visual rotation). Experiment 1 consisted of two conditions in which the direction of visual rotations for both arms was either in the same or opposing directions, whereas the target direction for both arms was always the same. In experiment 2, we examined the pattern of generalization between the bilateral and unilateral conditions when both the target and rotation directions were opposing between the arms. In both experiments, subjects first adapted to a 30° visual rotation with one arm (preunilateral), then with both arms (bilateral), and finally with the arm that was not used in the first session (postunilateral). Our results show that bilateral interference was smallest when both variables were the same between the arms. Our data also show extensive transfer of visuomotor adaptation between bilateral and unilateral conditions, regardless of degree of bilateral interference.     

Concurrent adaptation to four different visual rotations

The human sensorimotor system can concurrently adapt to two different distortions without interference when the distortions are cued by different contexts. We investigated whether this holds with four distortions as well. Subjects were exposed to an interlaced sequence of +30°, −30°, +60°, and −60° visuomotor rotations as the adaptation phase, cued by combinations of workspace location and by the arm used. Adaptation phase was followed by two episodes in each condition without any distortion testing the aftereffects. Results showed that the error at the onset of adaptation gradually decreased during adaptation to all four distortions without any sign of interference between the conditions. Furthermore, aftereffects of adaptation to ±30° rotation were significantly greater than of adaptation to ±60° rotation. We conclude that the human sensorimotor system is able to concurrently adapt to four different visual distortions when they are cued by different contexts. However, the results of aftereffects are ambiguous: Recalibration could be based on at least four parallel modules.     

Interference between velocity-dependent and position-dependent force-fields indicates that tasks depending on different kinematic parameters compete for motor working memory

Humans demonstrate motor learning when exposed to changes in the dynamics of movement or changes in the visuomotor map. However, when two opposing dynamic transformations are learned in succession, the memory of the first is overwritten by learning of the second; the same is true for two opposing visuomotor rotations. This retrograde interference is not seen for all combinations of transformations, however. When a dynamic transformation is learned subsequent to a visuomotor rotation, the presence or absence of interference appears to depend crucially on the structure of the dynamic task: a force-field dependent on the position of the hand produces interference, whereas an inertial load applied lateral to the hand does not. To explain these results, it has been hypothesized that two transformations can be learned without interference if they depend on two different kinematic parameters of movement (such as position and velocity of the hand). Here we demonstrate, contrary to this hypothesis, interference between a dynamic transformation that depends on the position of the hand and one that depends on its velocity. However, the interference was found to be incomplete, supporting the view that the ability to retain motor memories for different tasks depends on the degree to which their representations conflict in working memory.     

Concurrent adaptation to opposing visual displacements during an alternating movement

It has been suggested that, during tasks in which subjects are exposed to a visual rotation of cursor feedback, alternating bimanual adaptation to opposing rotations is as rapid as unimanual adaptation to a single rotation (Bock et al. in Exp Brain Res 162:513–519, 2005). However, that experiment did not test strict alternation of the limbs but short alternate blocks of trials. We have therefore tested adaptation under alternate left/right hand movement with opposing rotations. It was clear that the left and right hand, within the alternating conditions, learnt to adapt to the opposing displacements at a similar rate suggesting that two adaptive states were formed concurrently. We suggest that the separate limbs are used as contextual cues to switch between the relevant adaptive states. However, we found that during online correction the alternating conditions had a significantly slower rate of adaptation in comparison to the unimanual conditions. Control conditions indicate that the results are not directly due the alternation between limbs or to the constant switching of vision between the two eyes. The negative interference may originate from the requirement to dissociate the visual information of these two alternating displacements to allow online control of the two arms.Support contributed by: Wellcome Trust & EPSRC studentship.     

Explicit contextual information selectively contributes to predictive switching of internal models

Many evidences suggest that the central nervous system (CNS) acquires and switches internal models for adaptive control in various environments. However, little is known about the neural mechanisms responsible for the switching. A recent computational model for simultaneous learning and switching of internal models proposes two separate switching mechanisms: a predictive mechanism purely based on contextual information and a postdictive mechanism based on the difference between actual and predicted sensorimotor feedbacks. This model can switch internal models solely based on contextual information in a predictive fashion immediately after alteration of the environment. Here we show that when subjects simultaneously adapted to alternating blocks of opposing visuomotor rotations, explicit contextual information about the rotations improved the initial performance at block alternations and asymptotic levels of performance within each block but not readaptation speeds. Our simulations using separate switching mechanisms duplicated these effects of contextual information on subject performance and suggest that improvement of initial performance was caused by improved accuracy of the predictive switch while adaptation speed corresponds to a switch dependent on sensorimotor feedback. Simulations also suggested that a slow change in output signals from the switching mechanisms causes contamination of motor commands from an internal model used in the previous context (anterograde interference) and partial destruction of internal models (retrograde interference). Explicit contextual information prevents destruction and assists memory retention by improving the changes in output signals. Thus, the asymptotic levels of performance improved. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The interference effects of non-rotated versus counter-rotated trials in visuomotor adaptation

An isometric torque-production task was used to investigate interference and retention in adaptation to multiple visuomotor environments. Subjects produced isometric flexion–extension and pronation–supination elbow torques to move a cursor to acquire targets as quickly as possible. Adaptation to a 30° counter-clockwise (CCW) rotation (task A), was followed by a period of rest (control), trials with no rotation (task B0), or trials with a 60° clockwise (CW) rotation (task B60). For all groups, retention of task A was assessed 5 h later. With initial training, all groups reduced the angular deviation of cursor paths early in the movements, indicating feedforward adaptation. For the control group, performance at commencement of the retest was significantly better than that at the beginning of the initial learning. For the B0 group, performance in the retest of task A was not dissimilar to that at the start of the initial learning, while for the B60 group retest performance in task A was markedly worse than initially observed. Our results indicate that close juxtaposition of two visuomotor environments precludes improved retest performance in the initial environment. Data for the B60 group, specifically larger angular errors upon retest compared with initial exposures, are consistent with the presence of anterograde interference. Furthermore, full interference occurred even when the visuomotor environment encountered in the second task was not rotated (B0). This latter novel result differs from those obtained for force field learning, where interference does not occur when task B does not impose perturbing forces, i.e., when B consists of a null field (Brashers-Krug et al., Nature 382:252–255, 1996). The results are consistent with recent proposals suggesting different interference mechanisms for visuomotor (kinematic) compared to force field (dynamic) adaptations, and have implications for the use of washout trials when studying interference between multiple visuomotor environments.     

Adaptation of arm trajectory during continuous drawing movements in different dynamic environments

Human subjects can readily adapt their movement trajectories to different dynamic or visuomotor environments. The focus of the current study was to determine whether subjects could simultaneously adapt to multiple dynamic environments. Subjects (n=5) drew ellipses continuously for 70 s using a torquable manipulandum under six distinct dynamic conditions, representing the combination of load type (spring, viscous, and inertia) and load direction (assisting and opposing). Each subject performed two control, ten load, and five washout trials. A significant effect of force condition on the trajectory of the movement was found in 26 of 30 cases (6 conditions × 5 subjects); the magnitude of the distortion differed across the conditions. The extent of adaptation also differed across the loads. Opposing inertia and viscosity led to fast adaptation. However, assisting inertia and viscosity were associated with relatively slow adaptation. The results of adaptation to the stiffness conditions were not consistent. Following sudden removal of the load we saw an additional disturbance of the trajectory (after-effect), which was often the mirror image of the original distortion. The shape and size of the after-effect were different across load conditions. These results show that human subjects can adapt to a variety of different dynamic transformations and that the time-course of adaptation is dependent on both the state space and the direction of the load. Electronic Publication     

Pattern discrimination and visuomotor behavior following rotation of one or both eyes in kittens and in adult cats

Summary Sixteen cats, each of which had one or both eyes rotated at the time of natural eye opening (group K), were tested for visuomotor behavior and for learning and interocular transfer of two-choice visual discriminations. Their behavior was compared to that of two cats given monocular rotations in adulthood (group A) and to two normal controls (group N). These animals were all reared in the same colony. All cats, including those with monocular rotations up to 180 ° and those with binocular rotations up to 80 ° in each eye, showed good visuomotor behavior when using the rotated eye (i.e., with the normal eye covered). Both the group K and group A animals showed comparable visuomotor adaptation. All animals except those with monocular rotations of 180 ° were able to learn several oriented pattern discriminations and showed considerable though incomplete interocular transfer of such information. The three animals with 180 ° rotations were able to learn brightness, but not pattern discriminations.Seven further animals with large rotations were used for histological studies of the retina and primary visual pathways. Areas of reduced ganglion cell density were not observed in whole mounts of the retinae, nor were regions of reduced transport of ³H-proline from the retina to the lateral geniculate nuclei or superior colliculi detectable from autoradiographs.     

Interlimb transfer of novel inertial dynamics is asymmetrical

Mechanisms underlying interlimb transfer of adaptation to visuomotor rotations have recently been explored in depth. However, little data are available regarding interlimb transfer of adaptation to novel inertial dynamics. The present study thus investigated interlimb transfer of dynamics by examining the effect of initial training with one arm on subsequent performance with the other in adaptation to a 1.5-kg mass attached eccentrically to the forearm. Using inverse dynamic analysis, we examined the changes in torque strategies associated with adaptation to the extra mass, and with interlimb transfer of that adaptation. Following initial training with the dominant arm, nondominant arm performance improved substantially in terms of linearity and initial direction control as compared with na?ve performance. However, initial training with the nondominant arm had no effect on subsequent performance with the dominant arm. Inverse dynamic analysis revealed that improvements in kinematics were implemented by increasing flexor muscle torques at the elbow to counter load-induced increases in extensor interaction torques as well as increasing flexor muscle torques at the shoulder to counter the extensor actions of elbow muscle torque. Following opposite arm adaptation, the nondominant arm adopted this dynamic strategy early in adaptation. These findings suggest that dominant arm adaptation to novel inertial dynamics leads to information that can be accessed and utilized by the opposite arm controller, but not vice versa. When compared with our previous findings on interlimb transfer of visuomotor rotations, our current findings suggest that adaptations to visuomotor and dynamic transformations are mediated by distinct neural mechanisms.     

Abnormal Purkinje cell activity in vivo in experimental allergic encephalomyelitis

It has been shown that learning visuomotor rotations with multiple target directions, compared with a single target direction, leads to greater generalization to untrained targets within the same limb. This implies that multiple direction learning results in a more complete internal model of the visuomotor transform. It has also been documented that the extent of transfer of movement information regarding visuomotor adaptations between the limbs is limited, relative to that between different configurations of the same limb. The present study thus investigated the origin of this restriction in interlimb transfer, by comparing the effects of eight-direction and one-direction training conditions with one arm on the subsequent performance with the other arm. It was hypothesized that if multiple direction learning leads to a more complete model of the novel visuomotor transform, interlimb transfer should be enhanced relative to that following single direction training. However, if no differences are observed between single and multiple direction training conditions, this would suggest that such learning is effector dependent. We also tested the hypothesis that interlimb transfer of visuomotor adaptation is not obligatory, by examining the effects of visual rotation direction (same or oppositely directed visuomotor rotations for the two arms). All subjects first adapted to a 30° rotation, either clockwise or counterclockwise, in the visual display during reaching movements. Following this, they adapted to a 30° rotation in either the same or opposing direction with the other arm. Results showed that initial training with the non-dominant arm facilitated subsequent performance with the dominant arm in terms of initial direction control, but only under the same rotation condition. Both single and eight direction training conditions led to substantial transfer in subsequent performance with the other arm, but multiple direction training was no more beneficial than single direction training. This finding suggests that the previously reported intralimb advantages of multiple direction learning are effector specific. Our findings are discussed in the context of hierarchical models of motor control to explain the intralimb advantages of multiple direction training.     

Visuomotor adaptation and generalization with repeated and varied training

Many studies have shown that reaching movements to visual targets can rapidly adapt to altered visual feedback of hand motion (i.e., visuomotor rotation) and generalize to new target directions. This generalization is thought to reflect the acquisition of a neural representation of the novel visuomotor environment that is localized to the particular trained direction. In these studies, participants perform movements to a small number of target locations repeatedly. However, it is unclear whether adaptation and generalization are comparable when target locations are constantly varied and participants reach to visual targets one time only. Here, we compared performance for reaches to a 30° counter-clockwise visuomotor rotation to four targets, spaced 90° apart across four areas of workspace 18 times each (repeated practice (RP)) with one time only reaching movements to 72 targets, spaced 5° apart (varied practice (VP)). For both training groups, participants performed 18 reaches to radial targets (either at the repeated or varied location) in a specific area of the workspace (i.e., one of four quadrants) before reaching in the adjacent workspace. We found that the RP group adapted more completely compared to the VP group. Conversely, the VP group generalized to new target directions more completely when reaching without cursor feedback compared to the RP group. This suggests that RP and VP follow a mainly common pattern of adaptation and generalization represented in the brain, with benefits of faster adaptation with RP and more complete generalization with VP.     

Evidence for a dynamic-dominance hypothesis of handedness

Handedness is a prominent behavioral phenomenon that emerges from asymmetrical neural organization of human motor systems. However, the aspects of motor performance that correspond to handedness remain largely undetermined. A recent study examining interlimb differences in coordination of reaching demonstrated dominant arm advantages in controlling limb segment inertial dynamics (Sainburg and Kalakanis 2000). Based on these findings, I now propose the dynamic-dominance hypothesis, which states that the essential factor that distinguishes dominant from nondominant arm performance is the facility governing the control of limb dynamics. The purpose of this study is to test two predictions of this hypothesis: 1) adaptation to novel intersegmental dynamics, requiring the development of new dynamic transforms, should be more effective for the dominant arm; 2) there should be no difference in adapting to visuomotor rotations performed with the dominant as compared with the nondominant arm. The latter prediction is based on the idea that visual information about target position is translated into an internal reference frame prior to transformation of the movement plan into dynamic properties, which reflect the forces required to produce movement. To test these predictions, dominant arm adaptation is compared to nondominant arm adaptation during exposure to novel inertial loads and to novel visuomotor rotations. The results indicate substantial interlimb differences in adaptation to novel inertial dynamics, but equivalent adaptation to novel visuomotor rotations. Inverse dynamic analysis revealed better coordination of dominant arm muscle torques across both shoulder and elbow joints, as compared with nondominant arm muscle torques. As a result, dominant arm movements were produced with a fraction of the mean squared muscle torque computed for nondominant arm movements made at similar speeds. These results support the dynamic-dominance hypothesis, indicating that interlimb asymmetries in control arise downstream to visuomotor transformations, when dynamic variables that correspond to the forces required for motion are specified.     

Interlimb transfer of visuomotor rotations: independence of direction and final position information

Previous findings from our laboratory support the idea that the dominant arm is more proficient than the non-dominant arm in coordinating intersegmental dynamics for specifying trajectory direction and shape during multijoint reaching movements. We also showed that adaptation of right and left arms to novel visuomotor rotations was equivalent, suggesting that this process occurs upstream to processes that distinguish dominant and non-dominant arm performance. Because of this, we speculate that such visuomotor adaptations might transfer to subsequent performance during adaptation with the other arm. We now examine whether opposite arm training to novel visuomotor rotations transfers to affect adaptation using the right and left arms. Two subject groups, RL and LR, each comprising seven right-handed subjects, adapted to a 30 degrees counterclockwise rotation in the visual display during a center-out reaching task performed in eight directions. Each group first adapted using either the right (RL) or left (LR) arm, followed by opposite arm adaptation. In order to assess transfer, we compared the same side arm movements (either right or left) following opposite arm adaptation to those performed prior to opposite arm adaptation. Our findings indicate unambiguous transfer of learning across the arms. Different features of movement transferred in different directions: Opposite arm training improved the initial direction of right arm movements under the rotated visual condition, whereas opposite arm training improved the final position accuracy, but not the direction of left arm movements. These findings confirm that transfer of training was not due to a general cognitive strategy, since such an effect should influence either hand equally. These findings support the hypothesis that each arm controller has access to information learned during opposite arm training. We suggest that each controller uses this information differently, depending on its proficiency for specifying particular features of movement. We discuss evidence that these two aspects of control are differentially mediated by the right and left cerebral hemispheres.     

Mechanisms underlying interlimb transfer of visuomotor rotations

We previously reported that opposite arm training improved the initial direction of dominant arm movements, whereas it only improved the final position accuracy of non-dominant arm movements. We now ask whether each controller accesses common, or separate, short-term memory resources. To address this question, we investigated interlimb transfer of learning for visuomotor rotations that were directed oppositely [clockwise (CW)/counterclockwise (CCW)] for the two arms. We expected that if information obtained by initial training was stored in the same short-term memory space for both arms, opposite arm training of a CW rotation would interfere with subsequent adaptation to a CCW rotation. All subjects first adapted to a 30° rotation (CW) in the visual display during reaching movements. Following this, they adapted to a 30° rotation in the opposite direction (CCW) with the other arm. In contrast to our previous findings for interlimb transfer of same direction rotations (CCW/CCW), no effects of opposite arm adaptation were indicated in the initial trials performed. This indicates that interlimb transfer is not obligatory, and suggests that short-term memory resources for the two limbs are independent. Through single trial analysis, we found that the direction and final position errors of the first trial of movement, following opposite arm training, were always the same as those of naive performance. This was true whether the opposite arm was trained with the same or the opposing rotation. When trained with the same rotation, transfer of learning did not occur until the second trial. These findings suggest that the selective use of opposite arm information is dependent on the first trial to probe current movement conditions. Interestingly, the final extent of adaptation appeared to be reduced by opposite arm training of opposing rotations. Thus, the extent of adaptation, but not initial information transfer, appears obligatorily affected by prior opposite arm adaptation. According to our findings, it is plausible that the initiation and the final extent of adaptation involve two independent neural processes. Theoretical implications of these findings are discussed. Electronic Publication