Erin K. Cressman

Visuomotor adaptation and proprioceptive recalibration in older adults

Previous studies have shown that both young and older subjects adapt their reaches in response to a visuomotor distortion. It has been suggested that one’s continued ability to adapt to a visuomotor distortion with advancing age is due to the preservation of implicit learning mechanisms, where implicit learning mechanisms include processes that realign sensory inputs (i.e. shift one’s felt hand position to match the visual representation). The present study examined this proposal by determining if changes in sense of felt hand position (i.e. proprioceptive recalibration) follow visuomotor adaptation in older subjects. As well, we examined the influence of age on proprioceptive recalibration by comparing young and older subjects’ estimates of the position at which they felt their hand was aligned with a visual reference marker before and after aiming with a misaligned cursor that was gradually rotated 30° clockwise of the actual hand location. On estimation trials, subjects moved their hand along a robot-generated constrained pathway. At the end of the movement, a reference marker appeared and subjects indicated if their hand was left or right of the marker. Results indicated that all subjects adapted their reaches at a similar rate and to the same extent across the reaching trials. More importantly, we found that both young and older subjects recalibrated proprioception, such that they felt their hand was aligned with a reference marker when it was approximately 6° more left (or counterclockwise) of the marker following reaches with a rotated cursor. The leftward shift in both young and older subjects’ estimates was in the same direction and a third of the extent of adapted movement. Given that the changes in the estimate of felt hand position were only a fraction of the changes observed in the reaching movements, it is unlikely that sensory recalibration was the only source driving changes in reaches. Thus, we propose that proprioceptive recalibration combines with adapted sensorimotor mappings to produce changes in reaching movements. From the results of the present study, it is clear that changes in both sensory and motor systems are possible in older adults and could contribute to the preserved visuomotor adaptation.

Visuomotor Adaptation and Proprioceptive Recalibration

ABSTRACT Motor learning, in particular motor adaptation, is driven by information from multiple senses. For example, when arm control is faulty, vision, touch, and proprioception can all report on the arms movements and help guide the adjustments necessary for correcting motor error. In recent years we have learned a lot about how the brain integrates information from multiple senses for the purpose of perception. However, less is known about how multisensory data guide motor learning. Most models of, and studies on, motor learning focus almost exclusively on the ensuing changes in motor performance without exploring the implications on sensory plasticity. Nor do they consider how discrepancies in sensory information (e.g., vision and proprioception) related to hand position may affect motor learning. Here, we discuss research from our lab and others that shows how motor learning paradigms affect proprioceptive estimates of hand position, and how even the mere discrepancy between visual and proprioceptive feedback can affect learning and plasticity. Our results suggest that sensorimotor learning mechanisms do not exclusively rely on motor plasticity and motor memory, and that sensory plasticity, in particular proprioceptive recalibration, plays a unique and important role in motor learning.

On-line control of pointing is modified by unseen visual shapes

Shapes that are rendered invisible through backward masking are still able to influence motor responses: this is called masked priming. Yet it is unknown whether this influence is on the control of ongoing action, or whether it merely influences the initiation of an already-programmed action. We modified a masked priming procedure (Schmidt, 2002) such that the critical prime-mask sequence was displayed during the execution of an already-initiated goal-directed pointing movement. Psychophysical tests of prime visibility indicated that the identity of the prime shapes were not accessible to participants for conscious report. Yet detailed kinematic analysis of the finger in motion revealed that masked primes had an influence on the pointing trajectories within 277ms of their appearance, 56ms earlier than the trajectory deviations observed in response to the visible masks. These results indicate that subliminal shapes can indeed influence the control of ongoing motor activity.

Proprioceptive recalibration following prolonged training and increasing distortions in visuomotor adaptation

Reaching with misaligned visual feedback of the hand leads to reach adaptation (motor recalibration) and also results in partial sensory recalibration, where proprioceptive estimates of hand position are changed in a way that is consistent with the visual distortion. The goal of the present study was to explore the relationship between changes in sensory and motor systems by examining these processes following (1) prolonged reach training and (2) training with increasing visuomotor distortions. To examine proprioceptive recalibration, we determined the position at which subjects felt their hand was aligned with a reference marker after completing three blocks of reach training trials with a cursor that was rotated 30° clockwise (CW) for all blocks, or with a visuomotor distortion that was increased incrementally across the training blocks up to 70°CW relative to actual hand motion. On average, subjects adapted their reaches by 16° and recalibrated their sense of felt hand position by 7° leftwards following the first block of reach training trials in which they reached with a cursor that was rotated 30°CW relative to the hand, compared to baseline values. There was no change in these values for the 30° training group across subsequent training blocks. However, subjects training with increasing levels of visuomotor distortion showed increased reach adaptation (up to 34° leftward movement aftereffects) and sensory recalibration (up to 15° leftwards). Analysis of motor and sensory changes following each training block did not reveal any significant correlations, suggesting that the processes underlying motor adaptation and proprioceptive recalibration occur simultaneously yet independently of each other.

Assessing vestibular contributions during changes in gait trajectory.

Displacing prisms and galvanic stimulation were used to examine visual–vestibular interactions during target-directed gait. Participants walked towards a wall 6 m away. After taking four steps, a target on the wall, located directly in front or to the right of the participant, was illuminated. Participants continued walking towards the target. Galvanic vestibular stimulation was triggered at either gait initiation, a step before the potential turn, or at target illumination. Although the visual and vestibular perturbations significantly altered gait trajectory, the greatest interaction occurred when galvanic stimulation was triggered one step before the target appeared. This implies an increase in the weighting of vestibular inputs just before turning to prepare for the potential change in direction.

Proprioceptive recalibration in the right and left hands following abrupt visuomotor adaptation

Previous studies have demonstrated that after reaching with misaligned visual feedback of the hand, one adapts his or her reaches and partially recalibrates proprioception, such that sense of felt hand position is shifted to match the seen hand position. However, to date, this has only been demonstrated in the right (dominant) hand following reach training with a visuomotor distortion in which the rotated cursor distortion was introduced gradually. As reach adaptation has been shown to differ depending on how the distortion is introduced (gradual vs. abrupt), we sought to examine proprioceptive recalibration following reach training with a cursor that was abruptly rotated 30° clockwise relative to hand motion. Furthermore, because the left and right arms have demonstrated selective advantages when matching visual and proprioceptive targets, respectively, we assessed proprioceptive recalibration in right-handed subjects following training with either the right or the left hand. On average, we observed shifts in felt hand position of approximately 7.6° following training with misaligned visual feedback of the hand, which is consistent with our previous findings in which the distortion was introduced gradually. Moreover, no difference was observed in proprioceptive recalibration across the left and right hands. These findings suggest that proprioceptive recalibration is a robust process that arises symmetrically in the two hands following visuomotor adaptation regardless of the initial magnitude of the error signal.

Cognitive constraint on the 'automatic pilot' for the hand: Movement intention influences the hand's susceptibility to involuntary online corrections

Research suggests that the reaching hand automatically deviates toward a target that changes location (jumps) during the reach. In the current study, we investigated whether movement intention can influence the target jumps impact on the hand. We compared the degree of trajectory deviation to a jumped target under three instruction conditions: (1) GO, in which participants were told to go to the target if it jumped, (2) STOP, in which participants were told to immediately stop their movement if the target jumped, and (3) IGNORE, in which participants were told to ignore the target if it jumped and to continue to its initial location. We observed a reduced response to the jump in the IGNORE condition relative to the other conditions, suggesting that the response to the jump is contingent on the jump being a task-relevant event.

Intermanual transfer and proprioceptive recalibration following training with translated visual feedback of the hand

Reaching with visual feedback that is misaligned with respect to the actual hand’s location leads to changes in reach trajectories (i.e., visuomotor adaptation). Previous studies have also demonstrated that when training to reach with misaligned visual feedback of the hand, the opposite hand also partially adapts, providing evidence of intermanual transfer. Moreover, our laboratory has shown that visuomotor adaptation to a misaligned hand cursor, either translated or rotated relative to the hand, also leads to changes in felt hand position (what we call proprioceptive recalibration), such that subjects’ estimate of felt hand position relative to both visual and non-visual reference markers (e.g., body midline) shifts in the direction of the visuomotor distortion. In the present study, we first determined the extent that motor adaptation to a translated cursor leads to transfer to the opposite hand, and whether this transfer differs across the dominant and non-dominant hands. Second, we looked to establish whether changes in hand proprioception that occur with the trained hand following adaptation also transfer to the untrained hand. We found intermanual motor transfer to the left untrained (non-dominant) hand after subjects trained their right (dominant) hand to reach with translated visual feedback of their hand. Motor transfer from the left trained to the right untrained hand was not observed. Despite finding changes in felt hand position in both trained hands, we did not find similar evidence of proprioceptive recalibration in the right or left untrained hands. Taken together, our results suggest that unlike visuomotor adaptation, proprioceptive recalibration does not transfer between hands and is specific only to the arm exposed to the distortion.

Identifying visual–vestibular contributions during target-directed locomotion

The purpose of this experiment was to examine the potential interaction between visual and vestibular inputs as participants walked towards 1 of 3 targets located on a barrier 5m away. Visual and vestibular inputs were perturbed with displacing prisms and galvanic vestibular stimulation (GVS), respectively. For each target there were three vision conditions (no prisms, prisms left, and prisms right), and three GVS conditions (no GVS, anode left, and anode right). Participants were instructed to start with eyes closed, and to open the eyes at heel contact of the first step. GVS and target illumination were triggered by the first heel contact. This ensured that the upcoming visual condition and target were unknown and that both sensory perturbations occurred simultaneously. Lateral displacement was determined every 40 cm. Irrespective of target or direction, GVS or prism perturbation alone resulted in similar lateral deviations. When combined, the GVS and prism perturbations that had similar singular effects led to significantly larger deviations in the direction of the perturbations. The deviations were approximately equal to the sum of the single deviations indicating that the combined effects were additive. Conflicting GVS and prism perturbations led to significantly smaller deviations that were close to zero, indicating that opposite perturbations cancelled each other. These results show that when both visual and vestibular information remain important during task performance, the nervous system integrates the inputs equally.

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.