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     

The extent of interlimb transfer following adaptation to a novel visuomotor condition does not depend on awareness of the condition

There is a controversy in the literature as to whether transfer of motor learning across the arms occurs because of an individual's cognitive awareness of the learned condition. The purpose of this study was to test whether the extent of interlimb transfer following adaptation to a novel visuomotor rotation with one arm, as well as the rate of learning acquired by the other arm, would vary depending on the subjects' awareness of the rotation condition. Awareness of the condition was varied by employing three experimental conditions. In one condition, visual rotation of the display up to 32° was gradually introduced to minimize the subjects' awareness of the rotation during targeted reaching movement. In another condition, the 32° rotation was abruptly introduced from the beginning of the adaptation session. Finally, the subjects were informed regarding the rotation prior to the adaptation session. After adaptation with the left arm under the three conditions, subjects performed reaching movement with the right arm under the same 32° rotation condition. Our results showed that the amount of initial transfer, and also the changes in performance with the right arm, did not vary significantly across the three conditions. This finding suggests that interlimb transfer of visuomotor adaptation does not occur based on an individual's awareness of the manipulation, but rather as a result of implicit generalization of the obtained visuomotor transformation across the arms.     

视觉动作适应中的学习、巩固和迁移

视觉动作适应是一种特殊形式的动作学习,是视觉目标与动作目标发生分离时大脑进行视觉动作转换从而完成动作执行的过程。类似于一般的动作学习,视觉动作适应中也有典型的动作学习、动作巩固和动作迁移现象,但表现机制更为复杂。视觉动作适应的学习是在视觉目标与动作目标不匹配时,被试在连续或阻断的视觉反馈的指导下,通过形成新的视觉动作地图完成动作任务的过程。排除任务间的顺行干扰,动作视觉适应巩固就随着时间的增强而增强。在双手之间和效应器之间都可以发生视觉动作适应的迁移。     

Trial-by-trial analysis of intermanual transfer during visuomotor adaptation

Studies of intermanual transfer have been used to probe representations formed during skill acquisition. We employ a new method that provides a continuous assay of intermanual transfer, intermixing right- and left-hand trials while limiting visual feedback to right-hand movements. We manipulated the degree of awareness of the visuomotor rotation, introducing a 22.5° perturbation in either an abrupt single step or gradually in ～1° increments every 10 trials. Intermanual transfer was observed with the direction of left-hand movements shifting in the opposite direction of the rotation over the course of training. The transfer on left-hand trials was less than that observed in the right hand. Moreover, the magnitude of transfer was larger in our mixed-limb design compared with the standard blocked design in which transfer is only probed at the end of training. Transfer was similar in the abrupt and gradual groups, suggesting that awareness of the perturbation has little effect on intermanual transfer. In a final experiment, participants were provided with a strategy to offset an abrupt rotation, a method that has been shown to increase error over the course of training due to the operation of sensorimotor adaptation. This deterioration was also observed on left-hand probe trials, providing further support that awareness has little effect on intermanual transfer. These results indicate that intermanual transfer is not dependent on the implementation of cognitively assisted strategies that participants might adopt when they become aware that the visuomotor mapping has been perturbed. Rather, the results indicate that the information available to processes involved in adaptation entails some degree of effector independence.     

Asymmetric interlimb transfer of concurrent adaptation to opposing dynamic forces

Interlimb transfer of a novel dynamic force has been well documented. It has also been shown that unimanual adaptation to opposing novel environments is possible if they are associated with different workspaces. The main aim of this study was to test if adaptation to opposing velocity dependent viscous forces with one arm could improve the initial performance of the other arm. The study also examined whether this interlimb transfer occurred across an extrinsic, spatial, coordinative system or an intrinsic, joint based, coordinative system. Subjects initially adapted to opposing viscous forces separated by target location. Our measure of performance was the correlation between the speed profiles of each movement within a force condition and an ‘average’ trajectory within null force conditions. Adaptation to the opposing forces was seen during initial acquisition with a significantly improved coefficient in epoch eight compared to epoch one. We then tested interlimb transfer from the dominant to non-dominant arm (D → ND) and vice-versa (ND → D) across either an extrinsic or intrinsic coordinative system. Interlimb transfer was only seen from the dominant to the non-dominant limb across an intrinsic coordinative system. These results support previous studies involving adaptation to a single dynamic force but also indicate that interlimb transfer of multiple opposing states is possible. This suggests that the information available at the level of representation allowing interlimb transfer can be more intricate than a general movement goal or a single perceived directional error.     

Body-centered visuomotor adaptation

Previous research has shown that humans generalize distortions of visuomotor feedback in terms of egocentric rotations. We examined whether these rotations are linked to the orientation of the eyes or of the shoulder of the arm that was used. Subjects moved a hand-held cube between target locations in a sequence of adaptation and test phases. During adaptation phases, subjects received either veridical or distorted visual feedback about the location of the cube. The distortions were changes in azimuth either relative to the eyes or to the shoulder. During test phases subjects received no visual feedback. Test phases were performed either with the arm that was exposed to the distorted feedback or with the unexposed arm. We compared test movement endpoints after distorted feedback with ones after veridical feedback. For the exposed arm, the spatial layout of the changes in endpoints clearly reflected the small differences between a rotation around the shoulder and around the eyes. For the unexposed arm, the changes in endpoints were smaller for both types of distortions and were less consistent with the distortions. Thus although the adaptation closely matches the imposed distortion, it does not appear to be directly linked to the orientation of the eyes or of the exposed arm.     

Effects of Parkinson's disease on visuomotor adaptation

Visuomotor adaptation to a kinematic distortion was investigated in Parkinson's disease (PD) patients and age-matched controls. Participants performed pointing movements in which the visual feedback of hand movement, displayed as a screen cursor, was normal (pre-exposure condition) or rotated by 90° counterclockwise (exposure condition). Aftereffects were assessed in a post-exposure condition in which the visual feedback of hand movement was set back to normal. In pre- and early-exposure trials, both groups showed similar initial directional error (IDE) and movement straightness (RMSE, root mean square error), but the PD group showed reduced movement smoothness (normalized jerk, NJ) and primary submovement to total movement distance ratios (PTR). During late-exposure the PD subjects, compared with controls, showed larger IDE, RMSE, NJ, and smaller PTR scores. Moreover, PD patients showed smaller aftereffects than the controls during the post-exposure condition. Overall, the PD group showed both slower and reduced adaptation compared with the control group. These results are discussed in terms of reduced signal-to-noise ratio in feedback signals related to increased movement variability and/or disordered kinesthesia, deficits in movement initiation, impaired selection of initial movement direction, and deficits in internal model formation in PD patients. We conclude that Parkinson's disease impairs visuomotor adaptation. Electronic Publication     

Effect of visuomotor-map uncertainty on visuomotor adaptation

Vision and proprioception contribute to generating hand movement. If a conflict between the visual and proprioceptive feedback of hand position is given, reaching movement is disturbed initially but recovers after training. Although previous studies have predominantly investigated the adaptive change in the motor output, it is unclear whether the contributions of visual and proprioceptive feedback controls to the reaching movement are modified by visuomotor adaptation. To investigate this, we focused on the change in proprioceptive feedback control associated with visuomotor adaptation. After the adaptation to gradually introduce visuomotor rotation, the hand reached the shifted position of the visual target to move the cursor to the visual target correctly. When the cursor feedback was occasionally eliminated (probe trial), the end point of the hand movement was biased in the visual-target direction, while the movement was initiated in the adapted direction, suggesting the incomplete adaptation of proprioceptive feedback control. Moreover, after the learning of uncertain visuomotor rotation, in which the rotation angle was randomly fluctuated on a trial-by-trial basis, the end-point bias in the probe trial increased, but the initial movement direction was not affected, suggesting a reduction in the adaptation level of proprioceptive feedback control. These results suggest that the change in the relative contribution of visual and proprioceptive feedback controls to the reaching movement in response to the visuomotor-map uncertainty is involved in visuomotor adaptation, whereas feedforward control might adapt in a manner different from that of the feedback control.     

Changes in motor cortical activity during visuomotor adaptation

We examined neuronal activity in three motor cortical areas while a rhesus monkey adapted to novel visuomotor transforms. The monkey moved a joystick that controlled a cursor on a video screen. Each trial began with the joystick centered. Next, the cursor appeared in one of eight positions, arranged in a circle around a target stimulus at the center of the screen. To receive reinforcement, the monkey moved the joystick so that the cursor contacted the target continuously for 1s. The video monitor provided continuous visual feedback of both cursor and target position. With those elements of the task constant, we modified the transform between joystick movement and that of the cursor at the beginning of a block of trials. Neuronal activity was studied as the monkey adapted to these novel joystick-cursor transforms. Some novel tasks included spatial transforms such as single-axis inversions, asymmetric double-axis inversions and angular deviations (also known as rotations). Other tasks involved changes in the spatiotemporal pattern and magnitude of joystick movement. As the monkey adapted to various visuomotor tasks, 209 task-related neurons (selected for stable background activity) showed significant changes in their task-related activity: 88 neurons in the primary motor cortex (M1), 32 in the supplementary motor cortex (M2), and 89 in the caudal part of the dorsal premotor cortex (PMdc). Slightly more than half of the sample in each area showed significant changes in the magnitude of activity modulation during adaptation, with the number of increases approximately equaling the number of decreases. These data support the prediction that changes in task-related neuronal activity can be observed in M1 during motor adaptation, but fail to support the hypothesis that M1 and PMdc differ in this regard. When viewed in population averages, motor cortex continued to change its activity for at least dozens of trials after performance reached a plateau. This slow, apparently continuing change in the pattern and magnitude of task-related activity may reflect the initial phases of consolidating the motor memory for preparing and executing visuomotor skills.     

The role of the cross-sensory error signal in visuomotor adaptation

Reaching to targets with misaligned visual feedback of the hand leads to changes in proprioceptive estimates of hand position and reach aftereffects. In such tasks, subjects are able to make use of two error signals: the discrepancy between the desired and actual movement, known as the sensorimotor error signal, and the discrepancy between visual and proprioceptive estimates of hand position, which we refer to as the cross-sensory error signal. We have recently shown that mere exposure to a sensory discrepancy in the absence of goal-directed movement (i.e. no sensorimotor error signal) is sufficient to produce similar changes in felt hand position and reach aftereffects. Here, we sought to determine the extent that this cross-sensory error signal can contribute to proprioceptive recalibration and movement aftereffects by manipulating the magnitude of this signal in the absence of volitional aiming movements. Subjects pushed their hand out along a robot-generated linear path that was gradually rotated clockwise relative to the path of a cursor. On all trials, subjects viewed a cursor that headed directly towards a remembered target while their hand moved out synchronously. After exposure to a 30° rotated hand-cursor distortion, subjects recalibrated their sense of felt hand position and adapted their reaches. However, no additional increases in recalibration or aftereffects were observed following further increases in the cross-sensory error signal (e.g. up to 70°). This is in contrast to our previous study where subjects freely reached to targets with misaligned visual hand position feedback, hence experiencing both sensorimotor and cross-sensory errors, and the distortion magnitude systematically predicted increases in proprioceptive recalibration and reach aftereffects. Given these findings, we suggest that the cross-sensory error signal results in changes to felt hand position which drive partial reach aftereffects, while larger aftereffects that are produced after visuomotor adaptation (and that vary with the size of distortion) are related to the sensorimotor error signal.     

The role of proprioception and attention in a visuomotor adaptation task

The role of proprioception in the control and adaptation of visuomotor relationships is still unclear. We have studied a deafferented subject, IW, and control subjects in a task in which they used single joint elbow extension to move to a visual target, with visual feedback of the terminal position provided by a cursor displayed in the plane of their movements. We report the differences in movement accuracy between the deafferented subject and controls in the normal task and when challenged with a cognitive load, counting backwards. All subjects were less accurate when counting; this was a small effect for the controls (<10% change) but much greater for the deafferented subject (>60% change). We also examined changes in movement kinematics when the instructed amplitude was altered via a changed gain between final arm position and presentation of the feedback cursor. The deafferented subject maintained temporal movement parameters stable and altered amplitude by scaling force (i.e. changed peak velocity), whereas the controls scaled both movement velocity and duration. Finally, we compared the subjects' adaptation of movement amplitude after a period of exposure to the changed visuomotor gain. The deafferented subject was able to adapt, but his adaptation was severely impaired by the counting task. These results suggest that proprioception is not an absolute requirement for adaptation to occur. Instead, proprioception has a more subtle role to play in the adjustment to visuomotor perturbations. It has an important role in the control of reaching movements, while in the absence of proprioception, attention appears necessary to monitor movements.     

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.     

Straight ahead acts as a reference for visuomotor adaptation

One can adapt movement planning to compensate for a mismatch between vision and action. Previous research with prismatic lenses has shown this adaptation to be accompanied with a shift in the evaluation of one’s body midline, suggesting an important role of this reference for successful adaptation. This interpretation leads to the prediction that rotation adaptation could be more difficult to learn for some directions than others. Specifically, we hypothesized that targets seen to the right of the body midline but for which a rotation imposes a movement to its left would generate a conflict leading to a bias in movement planning. As expected, we observed different movement planning biases across movement directions. The same pattern of biases was observed in a second experiment in which the starting position was translated 15 cm to the right of the participants’ midline. This indicates that the “straight ahead” direction, not one’s midline, serves as an important reference for movement planning during rotation adaptation.

Saccadic-like visuomotor adaptation involves little if any perceptual effects

Studies on visuomotor adaptation provide crucial clues on the functional properties of the human motor system. The widely studied saccadic adaptation paradigm is a major example of such a fruitful field of investigation. Magescas and Prablanc (J Cogn Neurosci 18(1):75–83, 2006) proposed a transposition of this protocol to arm pointing behavior, by designing an experiment in which the informational context of the upper limb visuomotor system is comparable to that of the saccadic system. Subjects were given terminal only visual feedback in a hand pointing task, assumed to produce a purely terminal visual error signal. Importantly, this paradigm has been shown to induce no saccadic adaptation. Although the saccadic adaptation paradigm is known to induce a predominantly motor adaptation with minor sensory effects, the lack of sensory changes has not been tested in its transposition to pointing. The present study was a partial replication of Magescas and Prablanc’s (J Cogn Neurosci 18(1):75–83, 2006) study with additional control tests. A first experiment searched for a possible change in the static visual-to-proprioceptive congruency. A second experiment, based on an anti-pointing task, aimed at separating the sensory and motor effects of the adaptation in a dynamic condition. Consistent with most results on saccadic adaptation, we found a predominant adaptation of the motor components, with little if any involvement of the sensory components. Results are interpreted by proposing a causal relationship between the type of error signal and its adaptive effects.     

Absence of after-effects for observers after watching a visuomotor adaptation

We tested whether observational practice would elicit after-effects in a normal environment following observation of an actor performing in a perturbed visuomotor environment. Two actor groups (with and without vision of the hand) practised reaching to visual targets with the cursor rotated 30° to the actual hand movement. An observer group viewed this adaptation. Observers demonstrated significant learning when they subsequently performed the aiming task in the perturbed environment. However, different from both actor groups, observers did not show after-effects in the normal visuomotor condition. Our findings imply that there is a qualitative difference in the processes between observational and physical practice and suggest that physical exposure is required to update an internal model of the visuomotor environment.     

Cerebellar regions involved in adaptation to force field and visuomotor perturbation

Studies with patients and functional magnetic resonance imaging investigations have demonstrated that the cerebellum plays an essential role in adaptation to visuomotor rotation and force field perturbation. To identify cerebellar structures involved in the two tasks, we studied 19 patients with focal lesions after cerebellar infarction. Focal lesions were manually traced on magnetic resonance images and normalized using a new spatially unbiased template of the cerebellum. In addition, we reanalyzed data from 14 patients with cerebellar degeneration using voxel-based morphometry. We found that adjacent regions with only little overlap in the anterior arm area (lobules IV to VI) are important for adaptation in both tasks. Although adaptation to the force field task lay more anteriorly (lobules IV and V), lobule VI was more important for the visuomotor task. In addition, regions in the posterolateral cerebellum (Crus I and II) contributed to both tasks. No consistent involvement of the posterior arm region (lobule VIII) was found. Independence of the two kinds of adaptation is further supported by findings that performance in one task did not correlate to performance in the other task. Our results show that the anterior arm area of the cerebellum is functionally divided into a more posterior part of lobule VI, extending into lobule V, related to visuomotor adaption, and a more anterior part including lobules IV and V, related to force field adaption. The posterolateral cerebellum may process common aspects of both tasks.     

Interlimb transfer of visuomotor rotations depends on handedness

We previously reported that opposite arm adaptation to visuomotor rotations improved the initial direction of right arm movements in right-handers, whereas it only improved the final position accuracy of their left arm movements. We now investigate the pattern of interlimb transfer following adaptation to 30° visuomotor rotations in left-handers to determine whether the direction of transfer depends on handedness. Our results indicate unambiguous transfer across the arms. In terms of final position accuracy, the direction of transfer is opposite to that observed in right-handers, such that transfer only occurred from the left to the right arm movements. Directional accuracy also showed the opposite pattern of transfer to that of right-handers: initial movement direction, calculated at peak tangential acceleration, transferred only from right to left arms. When movement direction was measured later in the movement, at peak tangential velocity, asymmetrical transfer also occurred, such that greater transfer occurred from right to left arms. However, a small, but significant influence of opposite arm adaptation also occurred for the left arm, which might reflect differences in the use of the nondominant arm between left- and right-handers. Overall, our results indicate that left-handers show a mirror-imaged pattern of interlimb transfer in visuomotor adaptation to that previously reported for right-handers. This pattern of transfer is consistent with the hypothesis that asymmetry in interlimb transfer is dependent on differential specialization of the dominant and nondominant hemisphere/limb systems for trajectory and positional control, respectively.