Parkinson's disease differentially affects adaptation to gradual as compared to sudden visuomotor distortions

Patients with Parkinson’s disease (PD) have difficulties in movement adaptation to optimize performance in novel environmental contexts such as altered screen cursor-hand relationships. Prior studies have shown that the time course of the distortion differentially affects visuomotor adaptation to screen cursor rotations, suggesting separate mechanisms for gradual and sudden adaptation. Moreover, studies in human and non-human primates suggest that adaptation to sudden kinematic distortions may engage the basal ganglia, whereas adaptation to gradual kinematic distortions involves cerebellar structures. In the present studies, participants were patients with PD, who performed center-out pointing movements, using either a digitizer tablet and pen or a computer trackball, under normal or rotated screen cursor feedback conditions. The initial study tested patients with PD using a cross-over experimental design for adaptation to gradual as compared with sudden rotated hand-screen cursor relationships and revealed significant after-effects for the gradual adaptation task only. Consistent with these results, findings from a follow-up experiment using a trackball that required only small finger movements showed that patients with PD adapt better to gradual as against sudden perturbations, when compared to age-matched healthy controls. We conclude that Parkinson’s disease affects adaptation to sudden visuomotor distortions but spares adaptation to gradual distortions.     

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.     

Abrupt, but not gradual visuomotor distortion facilitates adaptation in children with developmental coordination disorder

A previous experiment investigating visuomotor adaptation in typically developing children and children with Developmental Coordination Disorder (DCD) suggested poor adaptation to an abruptly induced visuomotor perturbation. In the current study, using a similar center-out drawing task, but administering either an abrupt or a gradual perturbation, and twice as many adaptation trials, we show that typically developing children are well able to successfully update an existing internal model in response to a 60 degrees rotation of the visual feedback, independent of the perturbation condition. Children with DCD, however, updated their internal map more effectively during exposure to an abrupt visuomotor perturbation than to a gradual one. This may suggest that the adaptation process in children with DCD responds differently to small vs. large steps of visuomotor discrepancies. Given the known role of the cerebellum in providing an error signal necessary for updating the internal model in response to a gradual visuomotor distortion, the results of our study add to the growing body of evidence implicating compromised cerebellar function in DCD.     

Properties of intermodal transfer after dual visuo- and auditory-motor adaptation

Previous work documented that sensorimotor adaptation transfers between sensory modalities: When subjects adapt with one arm to a visuomotor distortion while responding to visual targets, they also appear to be adapted when they are subsequently tested with auditory targets. Vice versa, when they adapt to an auditory-motor distortion while pointing to auditory targets, they appear to be adapted when they are subsequently tested with visual targets. Therefore, it was concluded that visuomotor as well as auditory-motor adaptation use the same adaptation mechanism. Furthermore, it has been proposed that sensory information from the trained modality is weighted larger than sensory information from an untrained one, because transfer between sensory modalities is incomplete. The present study tested these hypotheses for dual arm adaptation. One arm adapted to an auditory-motor distortion and the other either to an opposite directed auditory-motor or visuomotor distortion. We found that both arms adapted significantly. However, compared to reference data on single arm adaptation, adaptation in the dominant arm was reduced indicating interference from the non-dominant to the dominant arm. We further found that arm-specific aftereffects of adaptation, which reflect recalibration of sensorimotor transformation rules, were stronger or equally strong when targets were presented in the previously adapted compared to the non-adapted sensory modality, even when one arm adapted visually and the other auditorily. The findings are discussed with respect to a recently published schematic model on sensorimotor adaptation.     

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.     

Adaptation to visuomotor rotations in younger and older adults

Adaptation to a visuomotor rotation is known to be impaired at older adult age. The authors examined whether the impairment is present already at preretirement age and whether it depends on the difficulty of the adaptation task. Moreover, the authors tested predictions of the hypothesis that the age-related impairment pertains primarily to strategic corrections and the explicit knowledge on which they are based but not to the acquisition of an (implicit) internal model of the novel visuomotor transformation. The authors found an age-related impairment of adaptation and explicit knowledge already at preretirement age but no age-related change of aftereffects. With an incremental simplification of the adaptation task, age-related changes were able to be eliminated. Individual differences of the quality of explicit knowledge were associated with differences of adaptation, but not of aftereffects. When age groups were matched by explicit knowledge, age-related impairments of adaptation largely disappeared. However, a reliable difference remained in one of the experiments, suggesting that other processes of adjustment to a visuomotor rotation might be affected by aging as well.     

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.     

Rapid adaptation to auditory-visual spatial disparity

The so-called ventriloquism aftereffect is a remarkable example of rapid adaptative changes in spatial localization caused by visual stimuli. After exposure to a consistent spatial disparity of auditory and visual stimuli, localization of sound sources is systematically shifted to correct for the deviation of the sound from visual positions during the previous adaptation period. In the present study, this aftereffect was induced by presenting, within 17 min, 1800 repetitive noise or pure-tone bursts in combination with synchronized, and 20° disparate flashing light spots, in total darkness. Post-adaptive sound localization, measured by a method of manual pointing, was significantly shifted 2.4° (noise), 3.1° (1 kHz tones), or 5.8° (4 kHz tones) compared with the pre-adaptation condition. There was no transfer across frequencies; that is, shifts in localization were insignificant when the frequencies used for adaptation and the post-adaptation localization test were different. It is hypothesized that these aftereffects may rely on shifts in neural representations of auditory space with respect to those of visual space, induced by intersensory spatial disparity, and may thus reflect a phenomenon of neural short-term plasticity.     

Interlimb differences in visuomotor and dynamic adaptation during targeted reaching in children

While a number of studies have focused on movement (a)symmetries between the arms in adults, less is known about movement asymmetries in typically developing children. The goal of this study was to examine interlimb differences in children when adapting to novel visuomotor and dynamic conditions while performing a center-out reaching task. We tested 13 right-handed children aged 9–11 years old. Prior to movement, one of eight targets arranged radially around the start position was randomly displayed. Movements were made either with the right (dominant) arm or the left (nondominant) arm. The children participated in two experiments separated by at least one week. In one experiment, subjects were exposed to a rotated visual display (30° about the start circle); and in the other, a 1 kg mass (attached eccentrically to the forearm axis). Each experiment consisted of three blocks: pre-exposure, exposure and post-exposure. Three measures of task performance were calculated from hand trajectory data: hand-path deviation from the straight target line, direction error at peak velocity and final position error. Results showed that during visuomotor adaptation, no interlimb differences were observed for any of the three measures. During dynamic adaptation, however, a significant difference between the arms was observed at the first cycle during dynamic adaptation. With regard to the aftereffects observed during the post-exposure block, direction error data indicate considerably large aftereffects for both arms during visuomotor adaptation; and there was a significant difference between the arms, resulting in substantially larger aftereffects for the right arm. Similarly, dynamic adaptation results also showed a significant difference between the arms; and post hoc analyses indicated that aftereffects were present only for the right arm. Collectively, these findings indicate that the dominant arm advantage for developing an internal model associated with a novel visuomotor or dynamic transform, as previously shown in young adults, may already be apparent at 9 to 11-year old children.     

Adaptive coordination and alignment of eye and hand

Under spatial misalignment of eye and hand induced by laterally displacing prisms (11.4 degrees in the rightward direction), subjects pointed 60 times (once every 3 s) at a visually implicit target (straight ahead of nose, Experiment 1) or a visually explicit target (an objectively straight-ahead target, Experiment 2). For different groups in each experiment, the hand became visible early in the sagittal pointing movement (early visual feedback). Adaptation to the optical misalignment during exposure (direct effects) was rapid, especially with early feedback; complete compensation for the misalignment was achieved within about 30 trials, and overcompensation occurred in later trials, especially with an explicit target. In contrast, adaptation measured with the misalignment removed and without visual feedback after blocks of 10 pointing trials (aftereffects) was slow to develop, especially with delayed feedback and an implicit target; at most, about 40% compensation for the misalignment occurred after 60 trials. This difference between direct effects and aftereffects is discussed in terms of separable adaptive mechanisms that are activated by different error signals. Adaptive coordination is activated by error feedback and involves centrally located, strategically flexible, short-latency processes to correct for sudden changes in operational precision that normally occur with short-term changes in coordination tasks. Adaptive alignment is activated automatically by spatial discordance between misaligned systems and involves distributed, long-latency processes to correct for slowly developing shifts in alignment among perceptual-motor components that normally occur with long-term drift. The sudden onset of misalignment in experimental situations activates both mechanisms in a complex and not always cooperative manner, which may produce overcompensatory behavior during exposure (i.e., direct effects) and which may limit long-term alignment (i.e., aftereffects).     

Prism adaptation in left-handers

Two experiments with left-handers examined the features of prism adaptation established by previous research with right-handers. Regardless of handedness, (1) rapid adaptation occurs in exposure pointing with developing error in the opposite direction after target achievement, especially with early visual feedback in target pointing; (2) proprioceptive or visual aftereffects are larger, depending on whether visual feedback is available early or late, respectively, in target pointing; (3) the sum of these aftereffects is equal to the total aftereffect for the eye-hand coordination loop; (4) intermanual transfer of visual aftereffects occurs only for the dominant hand; and (5) visual aftereffects are larger in left space when the dominant hand is exposed to leftward displacement. A notable handedness difference is that, while transfer of proprioceptive aftereffects only occurs to the nondominant hand in right-handers, transfer occurs in both directions for left-handers, but regardless of handedness, such transfer only occurs when the exposed hand is tested first after exposure. A discussion then focuses on the implications of these data for a theory of handedness.     

First-Trial Adaptation to Prism Exposure

Terminal target-pointing error on the 1st trial of exposure to optical displacement is usually less than that expected from the optical displacement magnitude. Such 1st trial adaptation was confirmed in 2 experiments (N = 48 students in each) comparing pointing toward optically displaced targets and toward equivalent physically displaced targets (no optical displacement), with visual feedback delayed until movement completion. First-trial performance could not be explained by ordinary target undershoot, online correction, or reverse optic flow information about true target position and was unrelated to realignment aftereffects. Such adaptation might be an artifact of the asymmetry of the structured visual field produced by optical displacement, which induces a felt head rotation opposite to the direction of the displacement, thereby reducing the effective optical displacement.     

Proprioception plays a different role for sensorimotor adaptation to different distortions

If proprioceptive feedback is degraded by agonist-antagonist muscle vibration, then adaptation to rotated vision remains intact while adaptation to a velocity-dependent force field worsens. Here we evaluate whether this differential effect of vibration is related to the physical nature of the distortion - visual versus mechanical - or to their kinematic coupling to the subjects’ hand - velocity versus position dependent. Subjects adapted to a velocity-dependent visual distortion, to a position-dependent force, or to a velocity-dependent force; one half of the subjects adapted with, and the other half without agonist-antagonist vibration at the wrist, elbow, and shoulder. We found, as before, that vibration slowed down adaptation to a velocity-dependent force. However, vibration did not modify adaptation to the other two distortions, nor did it influence the aftereffects of any distortion. From this we conclude that intact proprioception supports strategic compensatory processes when proprioceptive signals agree with visual ones, and provide relevant (dynamic) information not available to the visual system.     

Knowledge of Performance is Insufficient for Implicit Visuomotor Rotation Adaptation

The ability to adapt is a fundamental and vital characteristic of the motor system. The authors altered the visual environment and focused on the ability of humans to adapt to a rotated environment in a reaching task, in the absence of continuous visual information about their hand location. Subjects could not see their arm but were provided with post trial knowledge of performance depicting hand path from movement onset to final position. Subjects failed to adapt under these conditions. The authors sought to find out whether the lack of adaptation is related to the number of target directions presented in the task, and planned 2 protocols in which subjects were gradually exposed to 22.5° visuomotor rotation. These protocols differed only in the number of target directions: 8 and 4 targets. The authors found that subjects had difficulty adapting without the existence of continuous visual feedback of their performance regardless of the number of targets presented in task. In the 4-target protocol, some of the subjects noticed the rotation and explicitly aimed to the correct direction. The results suggest that real-time feedback is required for motor adaptation to visual rotation during reaching movements.     

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.     

Visuomotor error augmentation affects mediolateral head and trunk stabilization during walking

Prior work demonstrates that humans spontaneously synchronize their head and trunk kinematics to a broad range of driving frequencies of perceived mediolateral motion prescribed using optical flow. Using a closed-loop visuomotor error augmentation task in an immersive virtual environment, we sought to understand whether unifying visual with vestibular and somatosensory feedback is a control goal during human walking, at least in the context of head and trunk stabilization. We hypothesized that humans would minimize visual errors during walking – i.e., those between the visual perception of movement and actual movement of the trunk. We found that subjects did not minimize errors between the visual perception of movement and actual movement of the head and trunk. Rather, subjects increased mediolateral trunk range of motion in response to error-augmented optical flow with positive feedback gains. Our results are more consistent with our alternative hypothesis – that visual feedback can override other sensory modalities and independently compel adjustments in head and trunk position. Also, aftereffects following exposure to error-augmented optical flow included longer, narrower steps and reduced mediolateral postural sway, particularly in response to larger amplitude positive feedback gains. Our results allude to a recalibration of head and trunk stabilization toward more tightly regulated postural control following exposure to error-augmented visual feedback. Lasting reductions in mediolateral postural sway may have implications for using error-augmented optical flow to enhance the integrity of walking balance control through training, for example in older adults.     

Adaptation to displaced vision: Evidence for transfer of adaptation and long-lasting aftereffects

Aftereffects following a single exposure to visual rearrangement last for 48 h and longer. Following multiple spaced exposures to visual rearrangement, aftereffects persisted for at least 2 weeks. Over the course of the multiple exposures, subjects showed diminished scatter when pointing without sight of hand to visual targets but did not show diminished constant errors. Adaptation achieved in one visuomotor transferred nearly perfectly to a test situation involving somewhat different movement demands.     

Internally augmented displays: contingent aftereffects as performance aids

Previous research on visual contingent aftereffects has been concerned with examining the effects of various parameters (e.g., spatial frequency and luminance) on the adaptation to, and decay of, contingent aftereffects. The current study tested the viability of using visual contingent aftereffects in a display context. Using established characteristics of contingent aftereffects, a program of contingent aftereffect adaptation was designed. Studies were conducted to determine if subjects who were adapted to see visual contingent aftereffects invoked by a visual display could achieve more rapid or certain identification of a display under low luminance conditions. The results confirmed (a) that contingent aftereffects can improve performance on a visual discrimination task requiring information from a display and (b) that contingent aftereffects are more enhanced at low levels of illumination.     

Adaptation to a direction-dependent visuomotor gain in the young and elderly

Consistent with the widely accepted notion of separate specification of movement amplitude and direction, it has been argued that there is also a categorical difference between adaptation to novel visuomotor rotations and to novel visuomotor gains. In line with this view, ageing seems to affect rotation and gain adaptation differently in that age-related impairments are consistently found for the former, but not for the latter. In this study we ask whether the contrasting findings could also be ascribed to differences in the level of difficulty of gain and rotation adaptation tasks, respectively. In order to increase the difficulty of gain adaptation, younger and older participants had to adapt to a direction-dependent gain transformation. Results revealed direction-dependent adaptation in both groups. More importantly, we replicated the typical findings of age-related impairments of adaptation, but not of aftereffects, that were previously only reported for rotation adaptation. Younger participants also showed superior explicit knowledge regarding the novel visuomotor mapping as compared to the older participants. We show that this knowledge was used by younger participants to selectively augment adaptive shifts. Finally, our findings suggest that the difficulty of the novel visuomotor transformation and, related to this, the involvement of explicit knowledge in adaptation is critical for age-related changes to show up, but not the type of adaptation task, rotation and gain adaptation, respectively.