Visuomotor adaptation in normal aging

Visuomotor adaptation to a gradual or sudden screen cursor rotation was investigated in healthy young and elderly subjects. Both age groups were equally divided into two subgroups; one subgroup was exposed to 11.25° step increments of visual feedback rotation, every 45 trials (up to a total of 90°), whereas a second subgroup was subjected to 90° rotation from the onset of exposure. Participants performed discrete, horizontal hand movements to virtual targets in four randomized directions. Targets appeared on a computer screen in front of them, and a board prevented vision of the hand at all times. Differential effects of aging on visuomotor adaptation were found, depending on the time course of the visual distortion. In both age groups, early exposure to the sudden visual feedback distortion resulted in typical spiral-like trajectories, which became straighter by late exposure. However, the final adaptation level was reduced in the aged group, although the aftereffects were similar. When subjects were exposed to the gradual distortion, no statistically significant differences in measures of adaptation with advancing age were found. In this case, both age groups appeared to adapt equally. However, after removal of the distortion, elderly subjects showed reduced aftereffects as compared with the young group. These findings suggest differential effects of aging on adaptation to gradual versus sudden visual feedback distortions, and may help to explain the conflicting results obtained in previous visuomotor adaptation studies.     

Adaptation to direction-dependent visuo-motor rotations and its decay in younger and older adults

We studied adaptation to a direction-dependent visuo-motor rotation in adults of early and late working age. For hand movements to the right, visual motion of the cursor on a monitor was rotated clockwise, for forward movements rotation of the cursor motion was zero, and for directions in-between rotation was intermediate. In contrast to previous studies, in which adaptation was more difficult (larger visuo-motor rotation, larger number of targets during practice) and the older age group was of higher age, we found no age-related deficit of adaptation. However, consistent with previous studies we found an age-related impairment of explicit knowledge of the visuo-motor rotation and no age-related differences of aftereffects. Across periods of not performing the task for 24 h and of performing the task for a prolonged period of time without visual feedback, we observed a decay of adaptation which did not depend on age. The present findings cast doubts on the prevalent interpretation of age-related impairments of adaptation in the absence of age-related changes of aftereffects as resulting from intentional strategic corrections, which become less efficient at higher age.     

Alternating Adaptation of Eye and Hand Movements to Opposite Directed Double Steps

Eye and hand movements can adapt to a variety of sensorimotor discordances. Studies on adaptation of movement directions suggest that the oculomotor and the hand motor system access the same adaptive mechanism related to the polarity of a discordance, because concurrent adaptations to opposite directed discordances strongly interfere. The authors scrutinized whether participants adapt their hand and eye movements to opposite directions (clockwise/counterclockwise) when both motor systems are alternatingly exposed to opposite directed double steps, and whether such adaptation is influenced by the allocation of effector to adaptation direction. The results showed that hand and eye movements adapted to opposite directions, but adaptation was biased to the counterclockwise direction. Aftereffects emerged nearly unbiased and independently for both motor systems. The authors conclude that the oculomotor and the hand motor system use independent mechanisms when they adapt to opposite polarities, although they interact during adaptation or concurrent performance.     

Adaptation to a Nonlinear Visuomotor Amplitude Transformation With Continuous and Terminal Visual Feedback

The control of a cursor on a computer monitor offers a simple means of exploring the limits of the plasticity of human visuomotor coordination. The authors explored the boundary conditions for adaptation to nonlinear visuomotor amplitude transformations. The authors hypothesized that only with terminal visual feedback during practice, but not with continuous visual feedback, humans might develop an internal model of the nonlinear visuomotor amplitude transformation. Thus, 2 groups were engaged in a sensorimotor adaptation task receiving either continuous or terminal visual feedback during the practice phase. In contrast to expectations, adaptive shifts and aftereffects observed in visual open-loop tests were linearly related to target amplitudes for both groups. Although the 2 feedback groups did not differ with respect to adaptive shifts and aftereffects, terminal visual feedback resulted in stable visual open-loop performance for an extended period, whereas movement errors increased after continuous visual feedback during practice. The benefit of continuous visual feedback, on the other hand, was faster closed-loop performance, indicating an optimization of visual closed-loop control.     

Adaptation to a nonlinear visuomotor amplitude transformation with continuous and terminal visual feedback

The control of a cursor on a computer monitor offers a simple means of exploring the limits of the plasticity of human visuomotor coordination. The authors explored the boundary conditions for adaptation to nonlinear visuomotor amplitude transformations. The authors hypothesized that only with terminal visual feedback during practice, but not with continuous visual feedback, humans might develop an internal model of the nonlinear visuomotor amplitude transformation. Thus, 2 groups were engaged in a sensorimotor adaptation task receiving either continuous or terminal visual feedback during the practice phase. In contrast to expectations, adaptive shifts and aftereffects observed in visual open-loop tests were linearly related to target amplitudes for both groups. Although the 2 feedback groups did not differ with respect to adaptive shifts and aftereffects, terminal visual feedback resulted in stable visual open-loop performance for an extended period, whereas movement errors increased after continuous visual feedback during practice. The benefit of continuous visual feedback, on the other hand, was faster closed-loop performance, indicating an optimization of visual closed-loop control.     

First-trial adaptation to prism exposure: artifact of visual capture

Terminal target-pointing error on the 1st trial of exposure to optical displacement is usually less than is expected from the optical displacement magnitude. The authors confirmed 1st-trial adaptation in the task of pointing toward optically displaced targets while visual feedback was delayed until movement completion. Measurement of head-shoulder posture while participants (N = 24) viewed the optically displaced field revealed that their shoulders felt turned in the direction opposite to the displacement (visual capture), accounting for all but about 4% to 10% of 1st-trial adaptation. First-trial adaptation was unrelated to realignment aftereffects. First-trial adaptation is largely an artifact of the asymmetry of the structured visual field produced by optical displacement, which induces a felt body rotation, thereby reducing the effective optical displacement.     

Visual Information and Object Size in the Control of Reaching

The role of vision in the control of reaching and grasping was investigated by varying the available visual information. Adults (N = 7) reached in conditions that had full visual information, visual information about the target object but not the hand or surrounding environment, and no visual information. Four different object diameters were used. The results indicated that as visual information and object size decreased, subjects used longer movement times, had slower speeds, and more asymmetrical hand-speed profiles. Subjects matched grasp aperture to object diameter, but overcompensated with larger grasp apertures when visual information was reduced. Subjects also qualitatively differed in reach kinematics when challenged with reduced visual information or smaller object size. These results emphasize the importance of vision of the target in reaching and show that subjects do not simply scale a command template with task difficulty.     

The visual control of aimed hand movements to stationary and moving targets.

The present study attempted to determine if during short-duration movements visual feedback can be processed in order to make adjustments to changes in the environment. The effect that varying the importance of monitoring target position has on the relative importance of vision of hand and vision of target (Carlton 1981a; Whiting and Cockerill 1974) was also examined. Subjects performed short- (150 ms) and longer-duration (330 ms) aimed hand movements under four visual feedback conditions (lights-on/lights-off by target-on/target-off) to stationary and moving targets. For the lights-off and target-off conditions, the lights and target, respectively, were extinguished 50 ms after movement initiation. For all moving-target conditions, the target started to move as the movement was initiated. Subjects were able to process visual information in 165 ms, as movement endpoints were biased in the direction of target motion for movements of this duration. Removing visual feedback 50 ms after movement initiation did not alter this finding. Subjects performed equally well with target and lights on or off, independent of whether the target remained stationary or moved. Presumably, during the first 50 ms of the movement subjects received sufficient visual information to aid in movement control.     

Adaptive changes of opposite sign in the oculomotor systems of the two eyes

Subjects inspected their feet via base-out prisms for 3 min. Using binocular vision, subsequent reaching without prisms showed significant overestimation of distance. Monocular testing showed a lateral shift in pointing to targets in opposite directions for each eye. This indicates that registered, as opposed to actual, convergence is a factor in near distance perception, and that opposite adaptation occurs within the motor control system for each eye.     

Error processing in pointing at randomly feedback-induced double-step stimuli

Two experiments were conducted to determine the spatial and temporal organization of the arm trajectory in human subjects as they pointed to single- and double-step target displacements. Subjects pointed either without (Experiment 1) or with (Experiment 2) vision of their moving hand throughout the trial. In both experiments, target perturbation occurring in double-step trials was clearly perceived by the subjects and was randomly introduced either at the onset or at peak velocity of hand movement. Regardless of whether or not visual reafference from the pointing hand was available, subjects corrected the trajectory of their moving hand to accommodate the double-step. Moreover, asymmetrical velocity profiles were observed for responses to both types of target, with or without vision of the moving hand. The acceleration phase was a fixed pattern independent of the type of step stimulation. However, a clear dissociation, both in the deceleration phase and accuracy of responses to double-step targets, emerged according to the timing of target perturbation. When targets were perturbed at the onset of hand movement, subjects modulated the deceleration phase of their response to compensate for 88 to 100% of the second target displacement. In contrast, when targets were perturbed at peak velocity of hand movement, subjects were unable to modulate the deceleration phase adequately and compensated for only 20 to 40% of the perturbation. These results suggest that motor error is dynamically evaluated during the acceleration phase of a movement toward a perturbed target, allowing amendments to the trajectory to be performed during the deceleration phase. This main corrective process appears to be basically independent of visual reafference from the moving hand.     

On-line trajectory modifications of planar,goal-directed arm movements

Sometimes a goal-directed arm movement has to be modified en route due to an unforeseen perturbation such as a target displacement or a hand displacement by an external force. In this paper several aspects of that modification process are addressed. Subjects had to perform a point-to-point movement task on a computer screen using a mouse-coupled pointer as the representation of the hand position. Trajectory modifications were imposed by unexpectedly changing the position of the target or by changing the relation between mouse and screen pointer.In the first series of experiments, we examined how often a trajectory is updated. Here, trajectory modifications were imposed by unexpectedly changing the normal relation between mouse and pointer to a shear-like relation, where a percentage of the forward/backward position of the hand was added to the pointer position in the left/right direction. Withdrawal of visual feedback during the movement revealed that trajectories were updated at interval times shorter than 200 ms. From the similarity with experiments where the original relation between mouse and pointer was restored during the movements, we conclude that motor plans are updated on-line to move the hand from its current perceived position to the target.In a second series of experiments, we studied whether a continuous change in target position yields similar trajectory modifications as a continuous hand displacement. To mimic the latter perturbation, we used the above-mentioned distortion of the mouse-pointer relation. We found that the resulting hand paths did not differ for the two visual perturbations and conclude that the perturbed, goal-directed movements are modified in a consistent way, irrespective of whether the position of the target or hand was perturbed. Simulations of the experimental data with a kinematic reaching model support this conclusion.     

Experiencing the Cross-Sensory Error Signal During Movement Leads to Proprioceptive Recalibration

Abstract

Reaching to targets in a virtual reality environment with misaligned visual feedback of the hand results in changes in movements (visuomotor adaptation) and sense of felt hand position (proprioceptive recalibration). We asked if proprioceptive recalibration arises even when the misalignment between visual and proprioceptive estimates of hand position is only experienced during movement. Participants performed a “shooting task” through the targets with a cursor that was rotated 30° clockwise relative to hand motion. Results revealed that, following training on the shooting task, participants adapted their reaches to all targets by approximately 16° and recalibrated their sense of felt hand position by 8°. Thus, experiencing a sensory misalignment between visual and proprioceptive estimates of hand position during movement leads to proprioceptive recalibration.     

Influence of continual biofeedback on jaw pursuit-tracking in healthy adults and in adults with apraxia plus aphasia

Apraxia of speech (AOS) is a disorder of motor programming resulting from damage to premotor or anterior insula cortex. The authors used a pursuit visuomotor tracking task to test whether such a disorder interferes with development of motor programs or with modification of existing programs via integration of feedback. Healthy older adults (n = 15) and adults with AOS plus aphasia and nonverbal apraxia (n = 8) performed a jaw movement task with (a) continuous visual feedback of a target movement pattern and their jaw movement and (b) no feedback. Healthy speakers were more accurate and less variable with feedback, suggesting accurate development of a program and feedback integration. Apraxic individuals' performance accuracy and response to feedback suggested that the neurological damage impairs both development of new programs and efficient integration of feedback.     

A neural network model for development of reaching and pointing based on the interaction of forward and inverse transformations

Pointing is one of the communicative actions that infants acquire during their first year of life. Based on a hypothesis that early pointing is triggered by emergent reaching behavior toward objects placed at out‐of‐reach distances, we proposed a neural network model that acquires reaching without explicit representation of ‘targets’. The proposed model controls a two‐joint arm in a horizontal plane, and it learns a loop of internal forward and inverse transformations; the former predicts the visual feedback of hand position and the latter generates motor commands from the visual input through random generation of the motor commands. In the proposed model, the motor output and visual input were represented by broadly tuned neural units. Even though explicit ‘targets’ were not presented during learning, the simulation successfully generated reaching toward visually presented objects at within‐reach and out‐of‐reach distances.     

Children do not recalibrate motor‐sensory temporal order after exposure to delayed sensory feedback

Prolonged adaptation to delayed sensory feedback to a simple motor act (such as pressing a key) causes recalibration of sensory‐motor synchronization, so instantaneous feedback appears to precede the motor act that caused it (Stetson, Cui, Montague & Eagleman, 2006). We investigated whether similar recalibration occurs in school‐age children. Although plasticity may be expected to be even greater in children than in adults, we found no evidence of recalibration in children aged 8–11 years. Subjects adapted to delayed feedback for 100 trials, intermittently pressing a key that caused a tone to sound after a 200 ms delay. During the test phase, subjects responded to a visual cue by pressing a key, which triggered a tone to be played at variable intervals before or after the keypress. Subjects judged whether the tone preceded or followed the keypress, yielding psychometric functions estimating the delay when they perceived the tone to be synchronous with the action. The psychometric functions also gave an estimate of the precision of the temporal order judgment. In agreement with previous studies, adaptation caused a shift in perceived synchrony in adults, so the keypress appeared to trail behind the auditory feedback, implying sensory‐motor recalibration. However, school children of 8 to 11 years showed no measureable adaptation of perceived simultaneity, even after adaptation with 500 ms lags. Importantly, precision in the simultaneity task also improved with age, and this developmental trend correlated strongly with the magnitude of recalibration. This suggests that lack of recalibration of sensory‐motor simultaneity after adaptation in school‐age children is related to their poor precision in temporal order judgments. To test this idea we measured recalibration in adult subjects with auditory noise added to the stimuli (which hampered temporal precision). Under these conditions, recalibration was greatly reduced, with the magnitude of recalibration strongly correlating with temporal precision.     

Periodic change in phase relationship between target and hand motion during visuo-manual tracking task: Behavioral evidence for intermittent control

When one performs visuo-manual tracking tasks, velocity profile of hand movements shows discontinuous patterns even if the target moves smoothly. A crucial factor of this “intermittency” is considerable delay in the sensorimotor feedback loop, and several researchers have suggested that the cause is intermittent correction of motor commands. However, when and how the brain monitors task performance and updates motor commands in a continuous motor task is uncertain. We examined how tracking error was affected by the timing of target disappearance during a tracking task. Results showed that tracking error, defined as the average phase difference between target and hand, varied periodically in all conditions. Hand preceded target at one specific phase but followed it at another, implying that motor control was not performed in a temporally uniform manner. Tracking stability was evaluated by the variance in phase difference, and changed depending on the timing of target-removal. The variability was larger when target disappeared around turning points than that when it disappeared around the center of motion. This shows that visual information at turning points is more effectively exploited for motor control of sinusoidal target tracking, suggesting that our brain controls hand movements with intermittent reference to visual information.     

Vision and precision reaching in 15-month-old infants

Visual information about the location of the hand in space plays a key role in many theories of the development of reaching. Empirical data casts doubt on this assumption, although vision of the hand is clearly used by adults. The current study investigated the role of vision in 15-month-olds' reaching, manipulating both the precision demands of the task and the level of visual information available. Infants reached for both large and small objects, presented with visual feedback of the target and hand (full lighting), or with visual feedback of only the target object (glowing object in the dark). In contrast to findings with younger infants, 15-month-olds' reaches were sensitive to changes in precision demands and visual feedback, reflecting corrective movements that become necessary as reaching tasks become more challenging. Furthermore, these kinematic alterations are similar to those seen in adults, suggesting that visual guidance may become more important over the course of development, as infants engage in increasingly higher precision tasks.     

Influence of feedback modality on sensorimotor adaptation: contribution of visual, kinesthetic, and verbal cues

In 4 studies, the authors tested the contributions of visual, kinesthetic, and verbal knowledge of results to the adaptive control of reaching movements toward visual targets. The same apparatus was used in all experiments, but the procedures differed in the sensory modality of the feedback that participants (N s = 5, 5, 6, and 6, respectively, in Experiments 1, 2, 3, and 4) received about their performances. Using biased visual, proprioceptive, or verbal feedback, the authors introduced a 5 degrees shift in the visuomanual relationship. Results showed no significant difference in the final amount of adaptation to the mismatch: On average, participants adapted to 79% of the perturbation. That finding is consistent with the view that adaptation is a multisensory, highly flexible process whose efficiency does not depend on the sensory channel conveying the error signal.     

Performance of a visuomotor walking task in an augmented reality training setting

Visual cues can be used to train walking patterns. Here, we studied the performance and learning capacities of healthy subjects executing a high-precision visuomotor walking task, in an augmented reality training set-up. A beamer was used to project visual stepping targets on the walking surface of an instrumented treadmill. Two speeds were used to manipulate task difficulty. All participants (n = 20) had to change their step length to hit visual stepping targets with a specific part of their foot, while walking on a treadmill over seven consecutive training blocks, each block composed of 100 stepping targets. Distance between stepping targets was varied between short, medium and long steps. Training blocks could either be composed of random stepping targets (no fixed sequence was present in the distance between the stepping targets) or sequenced stepping targets (repeating fixed sequence was present). Random training blocks were used to measure non-specific learning and sequenced training blocks were used to measure sequence-specific learning. Primary outcome measures were performance (% of correct hits), and learning effects (increase in performance over the training blocks: both sequence-specific and non-specific). Secondary outcome measures were the performance and stepping-error in relation to the step length (distance between stepping target). Subjects were able to score 76% and 54% at first try for lower speed (2.3 km/h) and higher speed (3.3 km/h) trials, respectively. Performance scores did not increase over the course of the trials, nor did the subjects show the ability to learn a sequenced walking task. Subjects were better able to hit targets while increasing their step length, compared to shortening it. In conclusion, augmented reality training by use of the current set-up was intuitive for the user. Suboptimal feedback presentation might have limited the learning effects of the subjects.     

Gait symmetric adaptation: Comparing effects of implicit visual distortion versus split-belt treadmill on aftereffects of adapted step length symmetry

Understanding gait adaptation is essential for rehabilitation, and visual feedback can be used during gait rehabilitation to develop effective gait training. We have previously shown that subjects can adapt spatial aspects of walking to an implicitly imposed distortion of visual feedback of step length. To further investigate the storage benefit of an implicit process engaged in visual feedback distortion, we compared the robustness of aftereffects acquired by visual feedback distortion, versus split-belt treadmill walking. For the visual distortion trial, we implicitly distorted the visual representation of subjects’ gait symmetry, whereas for the split-belt trial, the speed ratio of the two belts was gradually adjusted without visual feedback. After adaptation, the visual feedback or the split-belt perturbation was removed while subjects continued walking, and aftereffects of preserved asymmetric pattern were assessed. We found that subjects trained with visual distortion trial retained aftereffects longest. In response to the larger speed ratio of split-belt walking, the subjects showed an increase in the size of aftereffects compared to the smaller speed ratio, but it steeply decreased over time in all the speed ratios tested. In contrast, the visual distortion group showed much slower decreasing rate of aftereffects, which was evidence of longer storage of an adapted gait pattern. Visual distortion adaptation may involve the interaction and integration of the change in motor strategy and implicit process in sensorimotor adaptation. Although it should be clarified more clearly through further studies, the findings of this study suggest that gait control employs distinct adaptive processes during the visual distortion and split-belt walking and also the level of reliance of an implicit process may be greater in the visual distortion adaptation than the split-belt walking adaptation.