Motor adaptation does not differ when a perturbation is introduced abruptly or gradually.

People continuously adapt their movements to ever-changing circumstances, and particularly in skills training and rehabilitation, it is crucial that we understand how to optimize implicit adaptation in order for these processes to require as little conscious effort as possible. Although it is generally assumed that the way to do this is by introducing perturbations gradually, the literature is ambivalent on the effectiveness of this approach. Here, we tested whether there are differences in motor performance when adapting to an abrupt compared to a ramped visuomotor rotation. Using a within-subjects design, we tested this question under 3 different rotation sizes: 30-degrees, 45-degrees, and 60-degrees, as well as in 3 different populations: younger adults, older adults, and patients with mild cerebellar ataxia. We find no significant differences in either the behavioural outcomes, or model fits, between abrupt and gradual learning across any of the different conditions. Neither age, nor cerebellar ataxia had any significant effect on error-sensitivity either. These findings together indicate that error-sensitivity is not modulated by introducing a perturbation abruptly compared to gradually, and is also unaffected by age or mild cerebellar ataxia.

Reduced feedback barely slows down proprioceptive recalibration.

Introducing altered visual feedback of the hand produces quick adaptation of reaching movements. Our lab has shown that the associated shifts in estimates of the felt position of the hand saturate within a few training trials. The current study investigates whether the rapid changes in felt hand position that occur during classic visuomotor adaptation are diminished or slowed when training feedback is reduced. We reduced feedback by either providing visual feedback only at the end of the reach (terminal feedback) or constraining hand movements to reduce motor adaptation-related error signals such as sensory prediction errors and task errors (exposure). We measured changes as participants completed reaches with a 30° rotation, a -30° rotation, and clamped visual feedback, with these two "impoverished" training conditions, along with classic visuomotor adaptation training, while continuously estimating their felt hand position. Training with terminal feedback slightly reduced the initial rate of change in overall adaptation. However, the rate of change in hand localization, as well as the asymptote of hand localization shifts in both the terminal feedback group and the exposure training group was not noticeably different from those in the classic training group. Taken together, shifts in felt hand position are rapid and robust responses to sensory mismatches and are at best slightly modulated when feedback is reduced. This suggests that given the speed and invariance to the quality of feedback of proprioceptive recalibration, it could immediately contribute to all kinds of reach adaptation.NEW & NOTEWORTHY Reaching to targets with altered visual feedback about hand position leads to adaptation of movements as well as shifts in estimates of felt hand position. Felt hand position can shift in as little as one trial, and here we show that there is no noticeable reduction in speed when the feedback about movements is impoverished, indicating the robustness of the process of recalibrating felt hand position.

Measuring the double-drift illusion and its resets with hand trajectories.

If a Gabor pattern drifts in one direction while its internal texture drifts in the orthogonal direction, its perceived position deviates further and further away from its true path. We first evaluated the illusion using manual tracking. Participants followed the Gabor with a stylus on a drawing tablet that coincided optically with the horizontal monitor surface. Their hand and the stylus were not visible during the tracking. The magnitude of the tracking illusion corresponded closely to previous perceptual and pointing measures indicating that manual tracking is a valid measure for the illusion. This allowed us to use it in a second experiment to capture the behavior of the illusion as it eventually degrades and breaks down in single trials. Specifically, the deviation of the Gabor stops accumulating at some point and either stays at a fixed offset or resets toward the veridical position. To report the perceived trajectory of the Gabor, participants drew it after the Gabor was removed from the monitor. Resets were detected and analyzed and their distribution matches neither a temporal nor a spatial limit, but rather a broad gamma distribution over time. This suggests that resets are triggered randomly, about once per 1.3 seconds, possible by extraneous distractions or eye movements.

Proprioceptive recalibration following implicit visuomotor adaptation is preserved in Parkinson's disease.

Individuals with Parkinson's disease (PD) and healthy adults demonstrate similar levels of visuomotor adaptation provided that the distortion is small or introduced gradually, and hence, implicit processes are engaged. Recently, implicit processes underlying visuomotor adaptation in healthy individuals have been proposed to include proprioceptive recalibration (i.e., shifts in one's proprioceptive sense of felt hand position to match the visual estimate of their hand experienced during reaches with altered visual feedback of the hand). In the current study, we asked if proprioceptive recalibration is preserved in PD patients. PD patients tested during their "off" and "on" medication states and age-matched healthy controls reached to visual targets, while visual feedback of their unseen hand was gradually rotated 30° clockwise or translated 4 cm rightwards of their actual hand trajectory. As expected, PD patients and controls produced significant reach aftereffects, indicating visuomotor adaptation after reaching with the gradually introduced visuomotor distortions. More importantly, following visuomotor adaptation, both patients and controls showed recalibration in hand position estimates, and the magnitude of this recalibration was comparable between PD patients and controls. No differences for any measures assessed were observed across medication status (i.e., PD off vs PD on). Results reveal that patients are able to adjust their sensorimotor mappings and recalibrate proprioception following adaptation to a gradually introduced visuomotor distortion, and that dopaminergic intervention does not affect this proprioceptive recalibration. These results suggest that proprioceptive recalibration does not involve striatal dopaminergic pathways and may contribute to the preserved visuomotor adaptation that arises implicitly in PD patients.

Modeling inter-trial variability of pointing movements during visuomotor adaptation.

Trial-to-trial variability during visuomotor adaptation is usually explained as the result of two different sources, planning noise and execution noise. The estimation of the underlying variance parameters from observations involving varying feedback conditions cannot be achieved by standard techniques (Kalman filter) because they do not account for recursive noise propagation in a closed-loop system. We therefore developed a method to compute the exact likelihood of the output of a time-discrete and linear adaptation system as has been used to model visuomotor adaptation (Smith et al. in PLoS Biol 4(6):e179, 2006), observed under closed-loop and error-clamp conditions. We identified the variance parameters by maximizing this likelihood and compared the model prediction of the time course of variance and autocovariance with empiric data. The observed increase in variability during the early training phase could not be explained by planning noise and execution noise with constant variances. Extending the model by signal-dependent components of either execution noise or planning noise showed that the observed temporal changes of the trial-to-trial variability can be modeled by signal-dependent planning noise rather than signal-dependent execution noise. Comparing the variance time course between different training schedules showed that the signal-dependent increase of planning variance was specific for the fast adapting mechanism, whereas the assumption of constant planning variance was sufficient for the slow adapting mechanisms.

Sensing hand position in Ehlers-Danlos syndrome.

PURPOSE: To explore the effect of joint hypermobility on acuity, and precision, of hand proprioception. MATERIALS AND METHODS: We compared proprioceptive acuity, and precision, between EDS patients and controls. We then measured any changes in their estimates of hand position after participants adapted their reaches in response to altered visual feedback of their hand. The Beighton Scale was used to quantify the magnitude of joint hypermobility. RESULTS: There were no differences between the groups in the accuracy of estimates of hand location, nor in the visually induced changes in hand location. However, EDS patients' estimates were less precise when based purely on proprioception and could be partially predicted by Beighton score. CONCLUSIONS: EDS patients are less precise at estimating their hand's location when only afferent information is available, but the presence of efferent signalling may reduce this imprecision. Those who are more hypermobile are more likely to be imprecise.

Three-dimensional transformations for goal-directed action.

Much of the central nervous system is involved in visuomotor transformations for goal-directed gaze and reach movements. These transformations are often described in terms of stimulus location, gaze fixation, and reach endpoints, as viewed through the lens of translational geometry. Here, we argue that the intrinsic (primarily rotational) 3-D geometry of the eye-head-reach systems determines the spatial relationship between extrinsic goals and effector commands, and therefore the required transformations. This approach provides a common theoretical framework for understanding both gaze and reach control. Combined with an assessment of the behavioral, neurophysiological, imaging, and neuropsychological literature, this framework leads us to conclude that (a) the internal representation and updating of visual goals are dominated by gaze-centered mechanisms, but (b) these representations must then be transformed as a function of eye and head orientation signals into effector-specific 3-D movement commands.

Proprioceptive recalibration arises slowly compared to reach adaptation.

When subjects reach in a novel visuomotor environment (e.g. while viewing a cursor representing their hand that is rotated from their hand's actual position), they typically adjust their movements (i.e. bring the cursor to the target), thus reducing reaching errors. Additionally, research has shown that reaching with altered visual feedback of the hand results in sensory changes, such that proprioceptive estimates of hand position are shifted in the direction of the visual feedback experienced (Cressman and Henriques in J Neurophysiol 102:3505-3518, 2009). This study looked to establish the time course of these sensory changes. Additionally, the time courses of implicit sensory and motor changes were compared. Subjects reached to a single visual target while seeing a cursor that was either aligned with their hand position (50 trials) or rotated 30° clockwise relative to their hand (150 trials). Reach errors and proprioceptive estimates of felt hand position were assessed following the aligned reach training trials and at seven different times during the rotated reach training trials by having subjects reach to the target without visual feedback, and provide estimates of their hand relative to a visual reference marker, respectively. Results revealed a shift in proprioceptive estimates throughout the rotated reach training trials; however, significant sensory changes were not observed until after 70 trials. In contrast, results showed a greater change in reaches after a limited number of reach training trials with the rotated cursor. These findings suggest that proprioceptive recalibration arises more slowly than reach adaptation.

Allocentric versus egocentric representation of remembered reach targets in human cortex.

The location of a remembered reach target can be encoded in egocentric and/or allocentric reference frames. Cortical mechanisms for egocentric reach are relatively well described, but the corresponding allocentric representations are essentially unknown. Here, we used an event-related fMRI design to distinguish human brain areas involved in these two types of representation. Our paradigm consisted of three tasks with identical stimulus display but different instructions: egocentric reach (remember absolute target location), allocentric reach (remember target location relative to a visual landmark), and a nonspatial control, color report (report color of target). During the delay phase (when only target location was specified), the egocentric and allocentric tasks elicited widely overlapping regions of cortical activity (relative to the control), but with higher activation in parietofrontal cortex for egocentric task and higher activation in early visual cortex for allocentric tasks. In addition, egocentric directional selectivity (target relative to gaze) was observed in the superior occipital gyrus and the inferior occipital gyrus, whereas allocentric directional selectivity (target relative to a visual landmark) was observed in the inferior temporal gyrus and inferior occipital gyrus. During the response phase (after movement direction had been specified either by reappearance of the visual landmark or a pro-/anti-reach instruction), the parietofrontal network resumed egocentric directional selectivity, showing higher activation for contralateral than ipsilateral reaches. These results show that allocentric and egocentric reach mechanisms use partially overlapping but different cortical substrates and that directional specification is different for target memory versus reach response.

Generalization patterns for reach adaptation and proprioceptive recalibration differ after visuomotor learning.

Visuomotor learning results in changes in both motor and sensory systems (Cressman EK, Henriques DY. J Neurophysiol 102: 3505-3518, 2009), such that reaches are adapted and sense of felt hand position recalibrated after reaching with altered visual feedback of the hand. Moreover, visuomotor learning has been shown to generalize such that reach adaptation achieved at a trained target location can influence reaches to novel target directions (Krakauer JW, Pine ZM, Ghilardi MF, Ghez C. J Neurosci 20: 8916-8924, 2000). We looked to determine whether proprioceptive recalibration also generalizes to novel locations. Moreover, we looked to establish the relationship between reach adaptation and changes in sense of felt hand position by determining whether proprioceptive recalibration generalizes to novel targets in a similar manner as reach adaptation. On training trials, subjects reached to a single target with aligned or misaligned cursor-hand feedback, in which the cursor was either rotated or scaled in extent relative to hand movement. After reach training, subjects reached to the training target and novel targets (including targets from a second start position) without visual feedback to assess generalization of reach adaptation. Subjects then performed a proprioceptive estimation task, in which they indicated the position of their hand relative to visual reference markers placed at similar locations as the trained and novel reach targets. Results indicated that shifts in hand position generalized across novel locations, independent of reach adaptation. Thus these distinct sensory and motor generalization patterns suggest that reach adaptation and proprioceptive recalibration arise from independent error signals and that changes in one system cannot guide adjustments in the other.

No effect of delay on the spatial representation of serial reach targets.

When reaching for remembered target locations, it has been argued that the brain primarily relies on egocentric metrics and especially target position relative to gaze when reaches are immediate, but that the visuo-motor system relies stronger on allocentric (i.e., object-centered) metrics when a reach is delayed. However, previous reports from our group have shown that reaches to single remembered targets are represented relative to gaze, even when static visual landmarks are available and reaches are delayed by up to 12 s. Based on previous findings which showed a stronger contribution of allocentric coding in serial reach planning, the present study aimed to determine whether delay influences the use of a gaze-dependent reference frame when reaching to two remembered targets in a sequence after a delay of 0, 5 or 12 s. Gaze was varied relative to the first and second target and shifted away from the target before each reach. We found that participants used egocentric and allocentric reference frames in combination with a stronger reliance on allocentric information regardless of whether reaches were executed immediately or after a delay. Our results suggest that the relative contributions of egocentric and allocentric reference frames for spatial coding and updating of sequential reach targets do not change with a memory delay between target presentation and reaching.

Retention of proprioceptive recalibration following visuomotor adaptation.

We have recently shown that visuomotor adaptation following reaches with a misaligned cursor not only induces changes in an individual's motor output, but their proprioceptive sense of hand position as well. Long-term changes are seen in motor adaptation; however, very little is known about the retention of changes in felt hand position. We sought to evaluate whether this recalibration in proprioception, following visuomotor adaptation, is sufficiently robust to be retained the following day (~24 h later), and if so, to determine its extent. Visuomotor adaptation was induced by having subjects perform reaches to visual targets using a cursor representing their unseen hand, which had been gradually rotated 45° counterclockwise. Motor adaptation and proprioceptive recalibration were determined by assessing subjects' reach aftereffects and changes in hand bias, respectively. We found that subjects adapted their reaches and recalibrated their sense of hand position following training with a misaligned cursor, as shown in Cressman and Henriques (J Neurophysiol 102:3505-3518, 2009). More importantly, subjects who showed proprioceptive recalibration in the direction of motor adaptation on Day 1 did retain changes in felt hand position and motor adaptation on Day 2. These findings suggest that in addition to motor changes, individuals are capable of retaining sensory changes in proprioception up to 24 h later.

Concurrent adaptation to opposing visuomotor rotations by varying hand and body postures.

When reaching towards objects, the human central nervous system (CNS) can actively compensate for two different perturbations simultaneously (dual adaptation), though this does not simply occur upon presentation. Dual adaptation is made more difficult when the desired trajectories and targets are identical and hence do not cue the impending perturbation. In cases like these, the CNS requires contextual cues in order to predict the dynamics of the environment. Not all cues are effective at facilitating dual adaptation. In two experiments, we investigated the efficacy of two contextual cues that are intrinsic to the CNS, namely hand as well as body posture in concurrently adapting to two opposing visuomotor rotations. For the hand posture experiment, we also look at the role of extended training. Participants reached manually to visual targets with their unseen hand represented by a cursor that was rotated either 30° clockwise or counterclockwise, determined randomly on each reach. Each rotation was associated with a distinct hand posture (a precision or power grip, respectively) in one experiment and a distinct body rotation (10° leftward or rightward turn of the seat, respectively, while fixating straight) in the second experiment. Critically, the targets (and thus, the required cursor trajectories) were identical in both rotations. We found that how people held the tool or oriented their body while reaching is sufficient for concurrently adapting separate visuomotor mappings such that over time, reach errors significantly decrease. Extended practice did not lead to further benefits though. These findings suggest that when the required cursor movements are identical for different visuomotor mappings, dual adaptation is still possible given sufficient intrinsic contextual cues.

Generalization of reach adaptation and proprioceptive recalibration at different distances in the workspace.

Studies have shown that adapting one's reaches in one location in the workspace can generalize to other novel locations. Generalization of this visuomotor adaptation is influenced by the location of novel targets relative to the trained location such that reaches made to novel targets that are located far from the trained target direction (i.e., ~22.5°; Krakauer et al. in J Neurosci 20:8916-8924, 2000) show very little generalization compared to those that are closer to the trained direction. However, generalization is much broader when reaching to novel targets in the same direction but at different distances from the trained target. In this study, we investigated whether changes in hand proprioception (proprioceptive recalibration), like reach adaptation, generalize to different distances of the workspace. Subjects adapted their reaches with a rotated cursor to two target locations at a distance of 13 cm from the home position. We then compared changes in open-loop reaches and felt hand position at these trained locations to novel targets located in the same direction as the trained targets but either at a closer (10 cm) or at a farther distance (15 cm) from the home position. We found reach adaptation generalized to novel closer and farther targets to the same extent as observed at the trained target distance. In contrast, while changes in felt hand position were significant across the two novel distances, this recalibration was smaller for the novel-far locations compared to the trained location. Given that reach adaptation completely generalized across the novel distances but proprioceptive recalibration generalized to a lesser extent for farther distances, we suggest that proprioceptive recalibration may arise independently of motor adaptation and vice versa.

Functional magnetic resonance imaging adaptation reveals the cortical networks for processing grasp-relevant object properties.

Grasping behaviors require the selection of grasp-relevant object dimensions, independent of overall object size. Previous neuroimaging studies found that the intraparietal cortex processes object size, but it is unknown whether the graspable dimension (i.e., grasp axis between selected points on the object) or the overall size of objects triggers activation in that region. We used functional magnetic resonance imaging adaptation to investigate human brain areas involved in processing the grasp-relevant dimension of real 3-dimensional objects in grasping and viewing tasks. Trials consisted of 2 sequential stimuli in which the object's grasp-relevant dimension, its global size, or both were novel or repeated. We found that calcarine and extrastriate visual areas adapted to object size regardless of the grasp-relevant dimension during viewing tasks. In contrast, the superior parietal occipital cortex (SPOC) and lateral occipital complex of the left hemisphere adapted to the grasp-relevant dimension regardless of object size and task. Finally, the dorsal premotor cortex adapted to the grasp-relevant dimension in grasping, but not in viewing, tasks, suggesting that motor processing was complete at this stage. Taken together, our results provide a complete cortical circuit for progressive transformation of general object properties into grasp-related responses.

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.

The effect of visuomotor adaptation on proprioceptive localization: the contributions of perceptual and motor changes.

Reaching movements are rapidly adapted following training with rotated visual feedback of the hand (motor recalibration). Our laboratory has also found that visuomotor adaptation results in changes in estimates of felt hand position (proprioceptive recalibration) in the direction of the visuomotor distortion (Cressman and Henriques 2009, 2010; Cressman et al. 2010). In the present study, we included an additional method for measuring hand proprioception [specifically, proprioceptive-guided reaches of the unadapted (left) hand to the robot-guided adapted (right) hand-target] and compared this with our original perceptual task (estimating the felt hand position of the adapted hand relative to visual reference markers/the body midline), as well as to no-cursor reaches with the adapted hand (reaching to visual and midline-targets), to better identify whether changes in reaching following adaptation to a 50° rightward-rotated cursor reflect sensory or motor processes. Results for the proprioceptive estimation task were consistent with previous findings; subjects felt their hand to be aligned with a reference marker when it was shifted approximately 4° more in the direction of the visuomotor distortion following adaptation compared with baseline conditions. Moreover, we found similar changes in the proprioceptive-guided reaching task such that subjects misreached 5° in the direction of the cursor rotation. However, these results were true only for proprioceptive-guided reaches to the adapted hand, as reaches to the body midline were not affected by adaptation. This suggests that proprioceptive recalibration is restricted to the adapted hand and does not generalize to the rest of the body; this truly reflects a change in the sensory representation of the hand rather than changes in the motor program. This is in contrast to no-cursor reaches made with the adapted hand, which show reach after-effects for both visual targets and the midline, suggesting that reaches with the adapted hand reflect more of a change in the motor system. Our results also shed light on previous studies that may have misattributed these sensory and motor changes.

Movement-goal relevant object shape properties act as poor but viable cues for the attribution of motor errors to external objects.

When a context change is detected during motor learning, motor memories-internal models for executing movements within some context-may be created or existing motor memories may be activated and modified. Assigning credit to plausible causes of errors can allow for fast retrieval and activation of a motor memory, or a combination of motor memories, when the presence of such causes is detected. Features of the movement-context intrinsic to the movement dynamics, such as posture of the end effector, are often effective cues for detecting context change whereas features extrinsic to the movement dynamics, such as the colour of an object being moved, are often not. These extrinsic cues are typically not relevant to the motor task at hand and can be safely ignored by the motor system. We conducted two experiments testing if extrinsic but movement-goal relevant object-shape cues during an object-transport task can act as viable contextual cues for error assignment to the object, and the creation of new, object-shape-associated motor memories. In the first experiment we find that despite the object-shape cues, errors are primarily attributed to the hand transporting the object. In a second experiment, we find participants can execute differing movements cued by the object shape in a dual adaptation task, but the extent of adaptation is small, suggesting that movement-goal relevant object-shape properties are poor but viable cues for creating context specific motor memories.

Distinct learning, retention, and generalization patterns in de novo learning versus motor adaptation.

People correct for movement errors when acquiring new motor skills (de novo learning) or adapting well-known movements (motor adaptation). While de novo learning establishes new control policies, adaptation modifies existing ones, and previous work have distinguished behavioral and underlying brain mechanisms for each motor learning type. However, it is still unclear whether learning in each type interferes with the other. In study 1, we use a within-subjects design where participants train with both 30° visuomotor rotation and mirror reversal perturbations, to compare adaptation and de novo learning respectively. We find no perturbation order effects, and find no evidence for differences in learning rates and asymptotes for both perturbations. Explicit instructions also provide an advantage during early learning in both perturbations. However, mirror reversal learning shows larger inter-participant variability and slower movement initiation. Furthermore, we only observe reach aftereffects following rotation training. In study 2, we incorporate the mirror reversal in a browser-based task, to investigate under-studied de novo learning mechanisms like retention and generalization. Learning persists across three or more days, substantially transfers to the untrained hand, and to targets on both sides of the mirror axis. Our results extend insights for distinguishing motor skill acquisition from adapting well-known movements.

Visuomotor adaptation across the lifespan.

Being able to adapt our movements to changing circumstances allows people to maintain performance across a wide range of tasks throughout life, but it is unclear whether visuomotor learning abilities are fully developed in young children and, if so, whether they remain stable in the elderly. There is limited evidence of changes in motor adaptation ability throughout life, and the findings are inconsistent. Therefore, our goal was to compare visuomotor learning abilities throughout the lifespan. We used a shorter, gamified experimental task and collected data from participants in 5 age groups. Young children (M = 7 years), older children (M = 11 years), young adults (M = 20 years), adults (M = 40 years) and older adults (M = 67 years) adapted to a 45° visuomotor rotation in a centre-out reaching task. Across measures of rate of adaptation, extent of learning, rate of unlearning, generalization, and savings, we found that all groups performed similarly. That is, at least for short bouts of gamified learning, children and older adults perform just as well as young adults.