Sensorimotor Adaptation Research Articles

Prism adaptation during balance standing enhances the transfer after-effect on standing postural displacement

Prism adaptation (PA) is a sensorimotor adaptation paradigm that induces after-effects of adapted tasks and transfer after-effects of non-adapted tasks. Previous studies showed inconsistent results of transfer after-effects of adaptation to a leftward prismatic shift on the center-of-pressure (COP) displacement during eyes-closed standing. Challenging balance during PA increases the generalization of the internal model to untrained movements, resulting in increased transfer after-effects. The present study aimed to investigate the transfer after-effects of PA with challenging balance on standing postural displacement. Thirty healthy young adults were grouped into floor standing and balance-disc standing groups during leftward PA and pointed to targets while adapting to a leftward visual shift (30 diopters) for 20 min. After leftward PA, both groups had a significant rightward displacement of straight-ahead pointing with eyes closed. However, the COP position during eyes-closed standing with feet-closed was significantly displaced rightward only in the balance-disc standing group after leftward PA. These results show that challenging balance might increase the somatosensory and proprioceptive information for standing postural control, resulting in increased transfer after-effects of leftward PA on rightward standing postural displacement.

Effects of an Acute High Intensity Exercise Bout on Retention of Explicit, Strategic Locomotor Learning in Individuals With Chronic Stroke

Background Exercise priming, pairing high intensity exercise with a motor learning task, improves retention of upper extremity tasks in individuals after stroke, but has shown no benefit to locomotor learning. This difference may relate to the type of learning studied. Upper extremity studies used explicit, strategic tasks; locomotor studies used implicit sensorimotor adaptation (split-belt treadmill). Since walking is an important rehabilitation goal, it is crucial to understand under which circumstances exercise priming may improve retention of a newly learned walking pattern. Objective Determine the impact of exercise priming on explicit, strategic locomotor learning task retention in chronic stroke survivors. Methods Chronic stroke survivors (>6 months) performed 2 treadmill walking sessions. Visual feedback was used to train increased step length. Participants were assigned to control group (no exercise), continuous exercise (5 minutes high intensity), or long-interval exercise (15 minutes high/moderate intervals). After day 1 learning, participants either rested or performed exercise. On day 2, retention of the learned walking pattern was tested. Results All groups learned on day 1 (P < .001). The 2 priming groups showed significant changes in blood lactate and heart rate after exercise priming, the resting control group did not (P < .001). On day 2, there was no significant between-group difference in cued or un-cued task retention (P = .963 and .287, respectively). Conclusions Exercise priming did not affect retention of an explicit locomotor task in chronic stroke survivors. Further work should explore subgroups of individuals for whom priming may have selective clinical benefit to locomotor learning. ClinicalTrials.gov Identifier: NCT03726047

Sensorimotor adaptation reveals systematic biases of 3D estimates for reach-to-grasp actions.

Sensorimotor adaptation reveals systematic biases of 3D estimates for reach-to-grasp actions.

Mechanisms of sensorimotor adaptation in a hierarchical state feedback control model of speech.

Upon perceiving sensory errors during movements, the human sensorimotor system updates future movements to compensate for the errors, a phenomenon called sensorimotor adaptation. One component of this adaptation is thought to be driven by sensory prediction errors-discrepancies between predicted and actual sensory feedback. However, the mechanisms by which prediction errors drive adaptation remain unclear. Here, auditory prediction error-based mechanisms involved in speech auditory-motor adaptation were examined via the feedback aware control of tasks in speech (FACTS) model. Consistent with theoretical perspectives in both non-speech and speech motor control, the hierarchical architecture of FACTS relies on both the higher-level task (vocal tract constrictions) as well as lower-level articulatory state representations. Importantly, FACTS also computes sensory prediction errors as a part of its state feedback control mechanism, a well-established framework in the field of motor control. We explored potential adaptation mechanisms and found that adaptive behavior was present only when prediction errors updated the articulatory-to-task state transformation. In contrast, designs in which prediction errors updated forward sensory prediction models alone did not generate adaptation. Thus, FACTS demonstrated that 1) prediction errors can drive adaptation through task-level updates, and 2) adaptation is likely driven by updates to task-level control rather than (only) to forward predictive models. Additionally, simulating adaptation with FACTS generated a number of important hypotheses regarding previously reported phenomena such as identifying the source(s) of incomplete adaptation and driving factor(s) for changes in the second formant frequency during adaptation to the first formant perturbation. The proposed model design paves the way for a hierarchical state feedback control framework to be examined in the context of sensorimotor adaptation in both speech and non-speech effector systems.

Contribution of implicit memory to adaptation of movement extent during reaching against unpredictable spring-like loads: insensitivity to intentional suppression of kinematic performance.

We examined the extent to which intentionally underperforming a goal-directed reaching task impacts how memories of recent performance contribute to sensorimotor adaptation. Healthy human subjects performed computerized cognition testing and an assessment of sensorimotor adaptation, wherein they grasped the handle of a horizontal planar robot while making goal-directed out-and-back reaching movements. The robot exerted forces that resisted hand motion with a spring-like load that changed unpredictably between movements. The robotic test assessed how implicit and explicit memories of sensorimotor performance contribute to the compensation for the unpredictable changes in the hand-held load. After each movement, subjects were to recall and report how far the hand moved on the previous trial (peak extent of the out-and-back movement). Subjects performed the tests under two counter-balanced conditions: one where they performed with their best effort, and one where they intentionally sabotaged (i.e., suppressed) kinematic performance. Results from the computerized cognition tests confirmed that subjects understood and complied with task instructions. When suppressing performance during the robotic assessment, subjects demonstrated marked changes in reach precision, time to capture the target, and reaction time. We fit a set of limited memory models to the data to identify how subjects used implicit and explicit memories of recent performance to compensate for the changing loads. In both sessions, subjects used implicit, but not explicit, memories from the most recent trial to adapt reaches to unpredictable spring-like loads. Subjects did not "give up" on large errors, nor did they discount small errors deemed "good enough". Although subjects clearly suppressed kinematic performance (response timing, movement variability, and self-reporting of reach error), the relative contributions of sensorimotor memories to trial-by-trial variations in task performance did not differ significantly between the two testing conditions. We conclude that intentional performance suppression had minimal impact on how implicit sensorimotor memories contribute to adaptation of unpredictable mechanical loads applied to the hand.

Modeling orientation perception adaptation to altered gravity environments with memory of past sensorimotor states.

Transitioning between gravitational environments results in a central reinterpretation of sensory information, producing an adapted sensorimotor state suitable for motor actions and perceptions in the new environment. Critically, this central adaptation is not instantaneous, and complete adaptation may require weeks of prolonged exposure to novel environments. To mitigate risks associated with the lagging time course of adaptation (e.g., spatial orientation misperceptions, alterations in locomotor and postural control, and motion sickness), it is critical that we better understand sensorimotor states during adaptation. Recently, efforts have emerged to model human perception of orientation and self-motion during sensorimotor adaptation to new gravity stimuli. While these nascent computational frameworks are well suited for modeling exposure to novel gravitational stimuli, they have yet to distinguish how the central nervous system (CNS) reinterprets sensory information from familiar environmental stimuli (i.e., readaptation). Here, we present a theoretical framework and resulting computational model of vestibular adaptation to gravity transitions which captures the role of implicit memory. This advancement enables faster readaptation to familiar gravitational stimuli, which has been observed in repeat flyers, by considering vestibular signals dependent on the new gravity environment, through Bayesian inference. The evolution and weighting of hypotheses considered by the CNS is modeled via a Rao-Blackwellized particle filter algorithm. Sensorimotor adaptation learning is facilitated by retaining a memory of past harmonious states, represented by a conditional state transition probability density function, which allows the model to consider previously experienced gravity levels (while also dynamically learning new states) when formulating new alternative hypotheses of gravity. In order to demonstrate our theoretical framework and motivate future experiments, we perform a variety of simulations. These simulations demonstrate the effectiveness of this model and its potential to advance our understanding of transitory states during which central reinterpretation occurs, ultimately mitigating the risks associated with the lagging time course of adaptation to gravitational environments.

Implicit Sensorimotor Adaptation Proceeds in Absence of Movement Execution.

In implicit sensorimotor adaptation, a mismatch between the predicted and actual sensory feedback results in a sensory prediction error (SPE). Sensory predictions have long been thought to be linked to descending motor commands, implying a necessary contribution of movement execution to adaptation. However, recent work has shown that mere motor imagery (MI) also engages predictive mechanisms, opening up the possibility that MI might be sufficient to drive implicit adaptation. In a within-subject design in humans (n = 30), implicit adaptation was assessed in a center-out reaching task, following a single exposure to a visuomotor rotation. It was hypothesized that performing MI of a reaching movement while being provided with an animation of rotated visual feedback (MI condition) would lead to postrotation biases (PRBs) similar to those observed when the movement is executed (Execution condition). Results revealed that both the MI and Execution conditions led to significant directional biases following rotated trials. Yet the magnitude of these biases was significantly larger in the Execution condition. To further probe the contribution of MI to adaptation, a Control condition was conducted in which participants were presented with the same rotated visual animation as in the MI condition, but in which they were prevented from performing MI. Surprisingly, significant biases were also observed in the Control condition, suggesting that MI per se may not have accounted for adaptation. Overall, these results suggest that implicit adaptation can be partially supported by processes other than those that strictly pertain to generating motor commands, although movement execution does potentiate it.

Sensory prediction error drives subconscious motor learning outside of the laboratory.

Sensorimotor adaptation is supported by at least two parallel learning systems: an intentionally controlled explicit strategy and an involuntary implicit learning system. Past work focused on constrained reaches or finger movements in laboratory environments has shown subconscious learning systems to be driven in part by sensory prediction error (SPE), i.e., the mismatch between the realized and expected outcome of an action. We designed a ball rolling task to explore whether SPEs can drive implicit motor adaptation during complex whole body movements that impart physical motion on external objects. After applying a visual shift, participants rapidly adapted their rolling angles to reduce the error between the ball and the target. We removed all visual feedback and told participants to aim their throw directly toward the primary target, revealing an unintentional 5.06° implicit adjustment to reach angles that decayed over time. To determine whether this implicit adaptation was driven by SPE, we gave participants a second aiming target that would "solve" the visual shift, as in the study by Mazzoni and Krakauer (Mazzoni P, Krakauer JW. J Neurosci 26: 3642-3645, 2006). Remarkably, after rapidly reducing ball-rolling error to zero (due to enhancements in strategic aiming), the additional aiming target caused rolling angles to deviate beyond the primary target by 3.15°. This involuntary overcompensation, which worsened task performance, is a hallmark of SPE-driven implicit learning. These results show that SPE-driven implicit processes, previously observed within simplified finger or planar reaching movements, actively contribute to motor adaptation in more complex naturalistic skill-based tasks.NEW & NOTEWORTHY Implicit and explicit learning systems have been detected using simple, constrained movements inside the laboratory. How these systems impact movements during complex whole body, skill-based tasks has not been established. Here, we demonstrate that sensory prediction errors significantly impact how a person updates their movements, replicating findings from the laboratory in an unconstrained ball-rolling task. This real-world validation is an important step toward explaining how subconscious learning helps humans execute common motor skills in dynamic environments.

Updating of Implicit Adaptation Processes through Erroneous Numeric Feedback

There is debate about how implicit and explicit processes interact in sensorimotor adaptation, implicating how error signals drive learning. Target error information is thought to primarily influence explicit processes, therefore manipulations to the veracity of this information should impact adaptation but not implicit recalibration (i.e. after-effects). Thirty participants across three groups initially adapted to rotated cursor feedback. Then we manipulated numeric target error through knowledge of results (KR) feedback, where groups practised with correct or incorrect (+/-15°) numeric KR. Participants adapted to erroneous KR, but only the KR + 15 group showed augmented implicit recalibration, evidenced by larger after-effects than before KR exposure. In the presence of sensory prediction errors, target errors modulated after-effects, suggesting an interaction between implicit and explicit processes.

Cognitive Impairments After Stroke Do Not Attenuate Explicit Visuomotor Adaptation in Reaching and Savings With the Unaffected Arm

Background Accumulating evidence suggests that motor performance is affected by the cognitive control abilities of the subject. Performance in motor tasks in populations with cognitive deficits such as older adults and subjects with stroke is therefore expected to deteriorate. The goal of this study is to investigate the relationship between cognitive impairments and motor control and learning impairments in a visuomotor adaptation task in subjects with stroke. Methods Twenty-seven post-stroke, 31 age matched controls, and 30 young control subjects completed a sensorimotor adaptation task composed of 2 adaptation blocks separated by a washout block. Explicit learning was assessed by cueing subjects to suppress their strategy. Cognitive assessment was conducted using the Montreal Cognitive Assessment (MoCA) and a verbal learning test. Subjects with stroke performed the task with their unaffected arm. Results Despite the cognitive deterioration, the adaptation and savings of the stroke group and age matched controls were comparable. Adaptation and savings were smaller with respect to the young subjects. Savings was associated with a significant improvement in the explicit component across blocks. Finally, the explicit enhancement between blocks was significantly correlated with the MoCA scores in the stroke group and with the results of the verbal learning test in the young controls. Conclusion The lack of stroke-induced attenuation on adaptation, despite a correlation between cognitive abilities and explicit learning in adaptation, suggests that subjects with stroke have enough cognitive resources to support sensorimotor adaptation. The availability of cognitive resources for motor learning following brain damage could be utilized in the rehabilitation process.

A reliable and efficient adaptive Bayesian method to assess static lower limb position sense

BackgroundLower limb proprioception is critical for maintaining stability during gait and may impact how individuals modify their movements in response to changes in the environment and body state, a process termed “sensorimotor adaptation”. However, the connection between lower limb proprioception and sensorimotor adaptation during human gait has not been established. We suspect this gap is due in part to the lack of reliable, efficient methods to assess global lower limb proprioception in an ecologically valid context. New MethodWe assessed static lower limb proprioception using an alternative forced choice task, administered twice to determine test-retest reliability. Participants stood on a dual-belt treadmill which passively moved one limb to stimulus locations selected by a Bayesian adaptive algorithm. At the stimulus locations, participants judged relative foot positions and the algorithm estimated the point of subjective equality (PSE) and the uncertainty of lower limb proprioception. ResultsUsing the Bland-Altman method, combined with Bayesian statistics, we found that both the PSE and uncertainty estimates had good reliability. Comparison with existing method(s)Current methods assessing static lower limb proprioception do so within a single joint, in non-weight bearing positions, and rely heavily on memory. One exception assessed static lower limb proprioception in standing but did not measure reliability and contained confounds impacting participants’ judgments, which we experimentally controlled here. ConclusionsThis efficient and reliable method assessing lower limb proprioception will aid future mechanistic understanding of locomotor adaptation and serve as a useful tool for basic and clinical researchers studying balance and falls.

Daily artificial gravity is associated with greater neural efficiency during sensorimotor adaptation.

Altered vestibular signaling and body unloading in microgravity results in sensory reweighting and adaptation. Microgravity effects are well-replicated in head-down tilt bed rest (HDBR). Artificial gravity (AG) is a potential countermeasure to mitigate the effects of microgravity on human physiology and performance. We examined the effectiveness of daily AG for mitigating brain and/or behavioral changes in 60days of HDBR. One group received AG for 30minutes daily (AG; n = 16) and a control group spent the same time in HDBR but received no AG (CTRL; n = 8). All participants performed a sensorimotor adaptation task five times during fMRI scanning: twice prior to HDBR, twice during HDBR, and once following HDBR. The AG group showed similar behavioral adaptation effects compared with the CTRLs. We identified decreased brain activation in the AG group from pre to late HDBR in the cerebellum for the task baseline portion and in the thalamus, calcarine, cuneus, premotor cortices, and superior frontal gyrus in the AG group during the early adaptation phase. The two groups also exhibited differential brain-behavior correlations. Together, these results suggest that AG may result in a reduced recruitment of brain activity for basic motor processes and sensorimotor adaptation. These effects may stem from the somatosensory and vestibular stimulation that occur with AG.

Event-related (de)synchronization and potential in whole vs. part sensorimotor learning.

There are different ways to learn a sensorimotor task. This research focuses on whole versus part learning in a complex video game that involves sensorimotor adaptations and skill learning. The primary aim of this research is to compare the changes in (1) event-related potentials (ERP) and (2) Alpha and Beta event-related desynchronization/synchronization [ERD(S)] of EEG between whole and part practice protocols. 18 Healthy young participants practiced for 5 days a video game with distorted kinematic (advancing skill) and dynamic features (shooting skill) to test the ability to combine sensorimotor skill components learned modularly (part learning, 9 participants) or combined (whole practice, 9 participants). We examined ERP and ERD(S) in EEG channels in the baseline test (day 1) and the retention test (day 5), dissociating epochs with advancing or shooting. We focus the analysis on the main activity of ERP or ERD(S) in different time windows. In the advancing epochs (distorted kinematic), both groups showed a decrease in time for ERP and an increase in Beta ERD activity in central and posterior channels. In the shooting epochs (distorted dynamic), the Whole group showed a decrease in time for ERPs in anterior and central-posterior channels. Additionally, the shooting ERS in the Beta band decreases within sessions in central channels, particularly for the Part group. Neural correlates of kinematic and dynamic control [ERP and ERD(S)] were modulated by sensorimotor learning, which reflects the effect of the type of practice on the execution and the evaluation of the action. These results can be linked with our previous report, where the simultaneous practice of kinematic and dynamic distortions takes advantage of the motor performance on retention tests, indicating a more automatic control for the whole practice group.

Signatures of contextual interference in implicit sensorimotor adaptation.

Contextual interference refers to the phenomenon whereby a blocked practice schedule results in faster acquisition but poorer retention of new motor skills compared to a random practice schedule. While contextual interference has been observed under a broad range of tasks, it remains unclear if this effect generalizes to the implicit and automatic recalibration of an overlearned motor skill. To address this question, we compared blocked and random practice schedules in a visuomotor rotation task that isolates implicit adaptation. In experiment 1, we found robust signatures of contextual interference in implicit adaptation: compared to participants tested under a blocked training schedule, participants tested under a random training schedule exhibited a reduced rate of learning during the training phase but better retention during a subsequent no-feedback assessment phase. In experiment 2, we again observed an advantage in retention following random practice and showed that this result was not due to a change in context between the training and assessment phases (e.g. a blocked training schedule followed by a random assessment schedule). Taken together, these results indicate that contextual interference is not limited to the acquisition of new motor skills but also applies to the implicit adaptation of established motor skills.

Developmental and age differences in visuomotor adaptation across the lifespan

In the present cross-sectional study, we examined age and sex differences in sensorimotor adaptation. We tested 253 individuals at a local science museum (NEMO Science Museum, Amsterdam). Participants spanned a wide age range (8–70 years old; 54% male), allowing us to examine effects of both development and healthy aging within a single study. Participants performed a visuomotor adaptation task in which they had to adapt manual joystick movements to rotated visual feedback. We assessed the rate of adaptation following the introduction of the visual perturbation (both for early and later stages of adaptation), and the rate of de-adaptation following its removal. Results showed reliable adaptation patterns which did not differ by sex. We observed a quadratic relationship between age and both early adaptation and de-adaptation rates, with younger and older adults exhibiting the fasted adaptation rates. Our findings suggest that both younger and older age are associated with poorer strategic, cognitive processes involved in adaptation. We propose that developmental and age differences in cognitive functions and brain properties may underlie these effects on sensorimotor functioning.

Inter-Task Transfer of Prism Adaptation through Motor Imagery.

Prism adaptation (PA) is a useful method to investigate short-term sensorimotor plasticity. Following active exposure to prisms, individuals show consistent after-effects, probing that they have adapted to the perturbation. Whether after-effects are transferable to another task or remain specific to the task performed under exposure, represents a crucial interest to understand the adaptive processes at work. Motor imagery (MI, i.e., the mental representation of an action without any concomitant execution) offers an original opportunity to investigate the role of cognitive aspects of motor command preparation disregarding actual sensory and motor information related to its execution. The aim of the study was to test whether prism adaptation through MI led to transferable after-effects. Forty-four healthy volunteers were exposed to a rightward prismatic deviation while performing actual (Active group) versus imagined (MI group) pointing movements, or while being inactive (inactive group). Upon prisms removal, in the MI group, only participants with the highest MI abilities (MI+ group) showed consistent after-effects on pointing and, crucially, a significant transfer to throwing. This was not observed in participants with lower MI abilities and in the inactive group. However, a direct comparison of pointing after-effects and transfer to throwing between MI+ and the control inactive group did not show any significant difference. Although this interpretation requires caution, these findings suggest that exposure to intersensory conflict might be responsible for sensory realignment during prism adaptation which could be transferred to another task. This study paves the way for further investigations into MI's potential to develop robust sensorimotor adaptation.

Minified Augmented Reality as a Terrestrial Analog for G-Transitions Effects in Lunar and Interplanetary Spaceflight

Brief periods of extreme gravitational transition are anticipated during interplanetary spaceflight, including transitions between microgravity, hypogravity, and hypergravity. Rapid sensorimotor adaptation will occur following these G-transitions which may affect astronaut performance including gaze control and dynamic visual acuity. Significant decrements in dynamic visual acuity could lead to mission compromise or failure (e.g., impairing mission critical tasks or spacecraft maneuvering). It is crucial to provide astronauts with the training necessary to overcome these physiological barriers they are bound to encounter during spaceflight missions. Minifying lenses in augmented reality may serve as an easily applicable, low-cost, method to simulate vestibulo-ocular dysfunction that occurs during gravitational transitions. In this paper, we review the effects of G-transitions on the vestibulo-ocular system and report on the novel development of minified augmented reality as a potential simulator and training tool for future spaceflight. We also report the results from an early validation study with a mean decrease in DVA (0.370 LogMAR) with 80% minifying effect, as well as a mean increase of DVA post-minifying (0.030 LogMAR). These early results suggest that minified augmented reality may serve as an accessible terrestrial analog for G-transitions, thus having potential for pre-mission training, particularly for lunar and interplanetary spaceflight.

Effects of Different Feedback Conditions on Sensorimotor Adaptation Revealed in a Mirror Reversal Paradigm

Effects of Different Feedback Conditions on Sensorimotor Adaptation Revealed in a Mirror Reversal Paradigm

Distinct patterns of cortical manifold expansion and contraction underlie human sensorimotor adaptation

Sensorimotor learning is a dynamic, systems-level process that involves the combined action of multiple neural systems distributed across the brain. Although much is known about the specialized cortical systems that support specific components of action (such as reaching), we know less about how cortical systems function in a coordinated manner to facilitate adaptive behavior. To address this gap, our study measured human brain activity using functional MRI (fMRI) while participants performed a classic sensorimotor adaptation task and used a manifold learning approach to describe how behavioral changes during adaptation relate to changes in the landscape of cortical activity. During early adaptation, areas in the parietal and premotor cortices exhibited significant contraction along the cortical manifold, which was associated with their increased covariance with regions in the higher-order association cortex, including both the default mode and fronto-parietal networks. By contrast, during Late adaptation, when visuomotor errors had been largely reduced, a significant expansion of the visual cortex along the cortical manifold was associated with its reduced covariance with the association cortex and its increased intraconnectivity. Lastly, individuals who learned more rapidly exhibited greater covariance between regions in the sensorimotor and association cortices during early adaptation. These findings are consistent with a view that sensorimotor adaptation depends on changes in the integration and segregation of neural activity across more specialized regions of the unimodal cortex with regions in the association cortex implicated in higher-order processes. More generally, they lend support to an emerging line of evidence implicating regions of the default mode network (DMN) in task-based performance.

Sensorimotor adaptation and its transfer to motor command is altered in high autistic tendency

Sensorimotor adaptation and its transfer to motor command is altered in high autistic tendency