Does proprioceptive acuity influence the extent of implicit sensorimotor adaptation in young and older adults?

2021 ◽  
Author(s):  
Koenraad Vandevoorde ◽  
Jean-Jacques Orban de Xivry
Keyword(s):  
Older Adults ◽  
Sensory Integration ◽  
Prediction Error ◽  
Motor Adaptation ◽  
Sensorimotor Adaptation ◽  
Proprioceptive Information ◽  
Age Related ◽  
Sensory Prediction

The ability to adjust movements to changes in the environment declines with aging. This age-related decline is caused by the decline of explicit adjustments. However, implicit adaptation remains intact and might even be increased with aging. Since proprioceptive information has been linked to implicit adaptation, it might well be that an age-related decline in proprioceptive acuity might be linked to the performance of older adults in implicit adaptation tasks. Indeed, age-related proprioceptive deficits could lead to altered sensory integration with an increased weighting of the visual sensory-prediction error. Another possibility is that reduced proprioceptive acuity results in an increased reliance on predicted sensory consequences of the movement. Both these explanations led to our preregistered hypothesis: we expected a relation between the decline of proprioception and the amount of implicit adaptation across ages. However, we failed to support this hypothesis. Our results question the existence of reliability-based integration of visual and proprioceptive signals during motor adaptation.

scholarly journals Does somatosensory acuity influence the extent of internal model recalibration in young and older adults?

2020 ◽  
Author(s):  
Koenraad Vandevoorde ◽  
Jean-Jacques Orban de Xivry
Keyword(s):  
Older Adults ◽  
Sensory Integration ◽  
Prediction Error ◽  
Internal Model ◽  
Sensory Feedback ◽  
Motor Adaptation ◽  
Age Related ◽  
Somatosensory Information ◽  
Implicit Motor ◽  
Sensory Prediction

AbstractThe ability to adjust movements to changes in the environment declines with aging. This age-related decline is caused by the decline of explicit adjustments. However, automatic adjustment of movement, or internal model recalibration, remains intact and might even be increased with aging. Since somatosensory information appears to be required for internal model recalibration, it might well be that an age-related decline in somatosensory acuity is linked to the increase of internal model recalibration. One possible explanation for an increased internal model recalibration is that age-related somatosensory deficits could lead to altered sensory integration with an increased weighting of the visual sensory-prediction error. Another possibility is that reduced somatosensory acuity results in an increased reliance on predicted sensory feedback. Both these explanations led to our preregistered hypothesis: we expect a relation between the decline of somatosensation and the increased internal model recalibration with aging. However, we failed to support this hypothesis. Our results question the existence of reliability-based integration of visual and somatosensory signals during motor adaptation.New & NoteworthyIs somatosensory acuity linked to implicit motor adaptation? The latter is larger in old compared to younger people? In light of reliability-based sensory integration, we hypothesized that this larger implicit adaptation was linked to an age-related lower reliability of somatosensation. Over two experiments and 130 participants, we failed to find any evidence for this. We discuss alternative explanations for the increase in implicit adaptation with age and the validity of our somatosensory assessment.

scholarly journals Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits?

Brain ◽  
2019 ◽  
Vol 142 (3) ◽  
pp. 662-673 ◽  
Author(s):  
Aaron L Wong ◽  
Cherie L Marvel ◽  
Jordan A Taylor ◽  
John W Krakauer
Keyword(s):  
Prediction Error ◽  
Poor Performance ◽  
Visuomotor Adaptation ◽  
Cerebellar Degeneration ◽  
Prediction Errors ◽  
Cerebellar Disease ◽  
Learning Mechanisms ◽  
Visuomotor Rotation ◽  
Age Related ◽  
Sensory Prediction

Abstract Systematic perturbations in motor adaptation tasks are primarily countered by learning from sensory-prediction errors, with secondary contributions from other learning processes. Despite the availability of these additional processes, particularly the use of explicit re-aiming to counteract observed target errors, patients with cerebellar degeneration are surprisingly unable to compensate for their sensory-prediction error deficits by spontaneously switching to another learning mechanism. We hypothesized that if the nature of the task was changed—by allowing vision of the hand, which eliminates sensory-prediction errors—patients could be induced to preferentially adopt aiming strategies to solve visuomotor rotations. To test this, we first developed a novel visuomotor rotation paradigm that provides participants with vision of their hand in addition to the cursor, effectively setting the sensory-prediction error signal to zero. We demonstrated in younger healthy control subjects that this promotes a switch to strategic re-aiming based on target errors. We then showed that with vision of the hand, patients with cerebellar degeneration could also switch to an aiming strategy in response to visuomotor rotations, performing similarly to age-matched participants (older controls). Moreover, patients could retrieve their learned aiming solution after vision of the hand was removed (although they could not improve beyond what they retrieved), and retain it for at least 1 year. Both patients and older controls, however, exhibited impaired overall adaptation performance compared to younger healthy controls (age 18–33 years), likely due to age-related reductions in spatial and working memory. Patients also failed to generalize, i.e. they were unable to adopt analogous aiming strategies in response to novel rotations. Hence, there appears to be an inescapable obligatory dependence on sensory-prediction error-based learning—even when this system is impaired in patients with cerebellar disease. The persistence of sensory-prediction error-based learning effectively suppresses a switch to target error-based learning, which perhaps explains the unexpectedly poor performance by patients with cerebellar degeneration in visuomotor adaptation tasks.

scholarly journals Older adults learn less, but still reduce metabolic cost, during motor adaptation

2014 ◽  
Vol 111 (1) ◽  
pp. 135-144 ◽  
Author(s):  
Helen J. Huang ◽  
Alaa A. Ahmed
Keyword(s):  
Older Adults ◽  
Young Adults ◽  
Muscle Activity ◽  
Motor Adaptation ◽  
Metabolic Cost ◽  
Gas Analysis ◽  
The Novel ◽  
Age Related ◽  
Expired Gas Analysis ◽  
Expired Gas

The ability to learn new movements and dynamics is important for maintaining independence with advancing age. Age-related sensorimotor changes and increased muscle coactivation likely alter the trial-and-error-based process of adapting to new movement demands (motor adaptation). Here, we asked, to what extent is motor adaptation to novel dynamics maintained in older adults (≥65 yr)? We hypothesized that older adults would adapt to the novel dynamics less well than young adults. Because older adults often use muscle coactivation, we expected older adults to use greater muscle coactivation during motor adaptation than young adults. Nevertheless, we predicted that older adults would reduce muscle activity and metabolic cost with motor adaptation, similar to young adults. Seated older ( n = 11, 73.8 ± 5.6 yr) and young ( n = 15, 23.8 ± 4.7 yr) adults made targeted reaching movements while grasping a robotic arm. We measured their metabolic rate continuously via expired gas analysis. A force field was used to add novel dynamics. Older adults had greater movement deviations and compensated for just 65% of the novel dynamics compared with 84% in young adults. As expected, older adults used greater muscle coactivation than young adults. Last, older adults reduced muscle activity with motor adaptation and had consistent reductions in metabolic cost later during motor adaptation, similar to young adults. These results suggest that despite increased muscle coactivation, older adults can adapt to the novel dynamics, albeit less accurately. These results also suggest that reductions in metabolic cost may be a fundamental feature of motor adaptation.

scholarly journals Both fast and slow learning processes contribute to savings following sensorimotor adaptation

2019 ◽  
Vol 121 (4) ◽  
pp. 1575-1583 ◽  
Author(s):  
Susan K. Coltman ◽  
Joshua G. A. Cashaback ◽  
Paul L. Gribble
Keyword(s):  
Force Field ◽  
Motor Adaptation ◽  
Retention Rates ◽  
Sensorimotor Adaptation ◽  
Prediction Errors ◽  
Fast Process ◽  
Learning Rates ◽  
History Of ◽  
Underlying Mechanisms ◽  
Sensory Prediction

Recent work suggests that the rate of learning in sensorimotor adaptation is likely not fixed, but rather can change based on previous experience. One example is savings, a commonly observed phenomenon whereby the relearning of a motor skill is faster than the initial learning. Sensorimotor adaptation is thought to be driven by sensory prediction errors, which are the result of a mismatch between predicted and actual sensory consequences. It has been proposed that during motor adaptation the generation of sensory prediction errors engages two processes (fast and slow) that differ in learning and retention rates. We tested the idea that a history of errors would influence both the fast and slow processes during savings. Participants were asked to perform the same force field adaptation task twice in succession. We found that adaptation to the force field a second time led to increases in estimated learning rates for both fast and slow processes. While it has been proposed that savings is explained by an increase in learning rate for the fast process, here we observed that the slow process also contributes to savings. Our work suggests that fast and slow adaptation processes are both responsive to a history of error and both contribute to savings. NEW & NOTEWORTHY We studied the underlying mechanisms of savings during motor adaptation. Using a two-state model to represent fast and slow processes that contribute to motor adaptation, we found that a history of error modulates performance in both processes. While previous research has attributed savings to only changes in the fast process, we demonstrated that an increase in both processes is needed to account for the measured behavioral data.

scholarly journals Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits?

2018 ◽  
Author(s):  
Aaron L. Wong ◽  
Cherie L. Marvel ◽  
Jordan A. Taylor ◽  
John W. Krakauer
Keyword(s):  
Spinocerebellar Ataxia ◽  
Prediction Error ◽  
Visuomotor Adaptation ◽  
Cerebellar Degeneration ◽  
Prediction Errors ◽  
Healthy Controls ◽  
Learning Mechanisms ◽  
Visuomotor Rotation ◽  
Age Related ◽  
Sensory Prediction

ABSTRACTSystematic perturbations in motor adaptation tasks are primarily countered by learning from sensory-prediction errors, with secondary contributions from other learning processes. Despite the availability of these additional processes, particularly the use of explicit re-aiming to counteract observed target errors, patients with cerebellar degeneration are surprisingly unable to compensate for their sensory-prediction-error deficits by spontaneously switching to another learning mechanism. We hypothesized that if the nature of the task was changed – by allowing vision of the hand, which eliminates sensory-prediction errors – patients could be induced to preferentially adopt aiming strategies to solve visuomotor rotations. To test this, we first developed a novel visuomotor rotation paradigm that provides participants with vision of their hand in addition to the cursor, effectively setting the sensory-prediction-error signal to zero. We demonstrated in younger healthy controls that this promotes a switch to strategic re-aiming based on target errors. We then showed that with vision of the hand, patients with spinocerebellar ataxia could also switch to an aiming strategy in response to visuomotor rotations, performing similarly to age-matched participants (older controls). Moreover, patients could retrieve their learned aiming solution after vision of the hand was removed, and retain it for at least one year. Both patients and older controls, however, exhibited impaired overall adaptation performance compared to younger healthy controls (age, 18-33), likely due to age-related reductions in spatial and working memory. Moreover, patients failed to generalize, i.e., they were unable to adopt analogous aiming strategies in response to novel rotations, nor could they further improve their performance without vision of the hand. Hence, there appears to be an inescapable obligatory dependence on sensory-prediction-error-based learning – even when this system is impaired in patients with cerebellar degeneration. The persistence of sensory-prediction-error-based learning effectively suppresses a switch to target-error-based learning, which perhaps explains the unexpectedly poor performance by patients with spinocerebellar ataxia in visuomotor adaptation tasks.

Individual differences in proprioception predict the extent of implicit sensorimotor adaptation

2020 ◽  
Author(s):  
Jonathan S. Tsay ◽  
Hyosub E. Kim ◽  
Darius E. Parvin ◽  
Alissa R. Stover ◽  
Richard B. Ivry
Keyword(s):  
Individual Differences ◽  
Upper Bound ◽  
Critical Role ◽  
Motor Adaptation ◽  
Proprioceptive Feedback ◽  
Hand Position ◽  
Sensorimotor Adaptation ◽  
Proprioceptive Information ◽  
Visual Perturbation

ABSTRACTRecent studies have revealed an upper bound in motor adaptation, beyond which other learning systems may be recruited. The factors determining this upper bound are poorly understood. The multisensory integration hypothesis states that this limit arises from opposing responses to visual and proprioceptive feedback. As individuals adapt to a visual perturbation, they experience an increasing proprioceptive error in the opposite direction, and the upper bound is the point where these two error signals reach an equilibrium. Assuming that visual and proprioceptive feedback are weighted according to their variability, there should be a correlation between proprioceptive variability and the limits of adaptation. Alternatively, the proprioceptive realignment hypothesis states that the upper bound arises when the (biased) sensed hand position realigns with the target. When a visuo-proprioceptive discrepancy is introduced, the sensed hand position is biased towards the visual cursor and the adaptive system nullifies this discrepancy by driving the hand away from the target. This hypothesis predicts a correlation between the size of the proprioceptive shift and the upper bound of adaptation. We tested these two hypotheses by considering natural variation in proprioception and motor adaptation across individuals. We observed a modest, yet reliable correlation between the upper bound of adaptation with both proprioceptive measures (variability and shift). While these results do not favor one hypothesis over the other, they underscore the critical role of proprioception in sensorimotor adaptation, and moreover, motivate a novel perspective on how these proprioceptive constraints drive implicit changes in motor behavior.SIGNIFICANCE STATEMENTWhile the sensorimotor system uses sensory feedback to remain properly calibrated, this learning process is constrained, limited in the maximum degree of plasticity. The factors determining this limit remain elusive. Guided by two hypotheses concerning how visual and proprioceptive information are integrated, we show that individual differences in the upper bound of adaptation in response to a visual perturbation can be predicted by the bias and variability in proprioception. These results underscore the critical, but often neglected role of proprioception in human motor learning.

Adaptation and Reintegration of Proprioceptive Information in Young and Older Adults' Postural Control

2010 ◽  
Vol 104 (4) ◽  
pp. 1969-1977 ◽  
Author(s):  
Michail Doumas ◽  
Ralf Th. Krampe
Keyword(s):  
Older Adults ◽  
Postural Control ◽  
Path Length ◽  
Reference Conditions ◽  
Age Groups ◽  
Linear Feedback ◽  
Body Sway ◽  
Support Surface ◽  
Proprioceptive Information ◽  
Age Related

We investigated age-related changes in adaptation and sensory reintegration in postural control without vision. In two sessions, participants adapted their posture to sway reference and to reverse sway reference conditions, the former reducing (near eliminating) and the latter enhancing (near doubling) proprioceptive information for posture by means of support-surface rotations in proportion to body sway. Participants stood on a stable platform for 3 min (baseline) followed by 18 min of sway reference or reverse sway reference (adaptation) and finally again on a stable platform for 3 min (reintegration). Results showed that when inaccurate proprioception was introduced, anterior-posterior (AP) sway path length increased in comparable levels in the two age groups. During adaptation, young and older adults reduced postural sway at the same rate. On restoration of the stable platform in the reintegration phase, a sizeable aftereffect of increased AP path length was observed in both groups, which was greater in magnitude and duration for older adults. In line with linear feedback models of postural control, spectral analyses showed that this aftereffect differed between the two platform conditions. In the sway-referenced condition, a switch from low- to high-frequency COP sway marked the transition from reduced to normal proprioceptive information. The opposite switch was observed in the reverse sway referenced condition. Our findings illustrate age-related slowing in participants' postural control adjustments to sudden changes in environmental conditions. Over and above differences in postural control, our results implicate sensory reweighting as a specific mechanism highly sensitive to age-related decline.

scholarly journals Corrective muscle activity reveals subject-specific sensorimotor recalibration

2018 ◽  
Author(s):  
Pablo A. Iturralde ◽  
Gelsy Torres-Oviedo
Keyword(s):  
Muscle Activity ◽  
Motor System ◽  
Environmental Changes ◽  
Prolonged Exposure ◽  
Temporal Dynamics ◽  
Motor Adaptation ◽  
Human Locomotion ◽  
Sensorimotor Adaptation ◽  
Motor Patterns ◽  
Age Related

AbstractRecent studies suggest that planned and corrective actions are recalibrated during some forms of motor adaptation. However, corrective (a.k.a., reactive) movements in human locomotion are thought to simply reflect sudden environmental changes independently from sensorimotor recalibration. Thus, we asked if corrective responses can indicate the motor system’s adapted state following prolonged exposure to a novel walking situation inducing sensorimotor adaptation. We recorded electromyographic signals bilaterally on 15 leg muscles before, during, and after split-belts walking (i.e., novel walking situation), in which the legs move at different speeds. We exploited the rapid temporal dynamics of corrective responses upon introduction or removal of an unexpected speed transition to isolate them from the overall motor output. We found that corrective muscle activity was structurally different following short vs. long exposures to split-belts walking. Only after a long exposure, removal of the novel environment elicited corrective muscle patterns that matched those expected in response to a perturbation opposite to the one originally experienced. This indicated that individuals who recalibrated their motor system adopted split-belts environment as their new “normal” and transitioning back to the original walking environment causes subjects to react as if it was novel to them. Interestingly, this learning declined with age, but steady state modulation of muscle activity during split-belts walking did not, suggesting potentially different neural mechanisms underlying these motor patterns. Taken together, our results show that corrective motor commands reflect the adapted state of the motor system, which is less flexible as we age.Significance statementWe showed that corrective muscle activity elicited by sudden environmental transitions is revealing of the underlying recalibration process during sensorimotor adaptation. This allowed us to identify age-related decline in motor learning that was not discernible from kinematic measures conventionally used in motor adaptation studies. These findings suggest that older populations may have limited potential to correct their movements through error-based protocols simply given their age. Moreover, we describe the distinct motor patterns recruited during and after the split condition, informing our understanding of the therapeutic effect of this task. Therefore, our detailed EMG characterization provides valuable normative data of muscle activity that could be reinforced with repeated exposure of split-belts walking.

scholarly journals The cerebellum does more than sensory-prediction-error-based learning in sensorimotor adaptation tasks

2017 ◽  
Author(s):  
Peter A. Butcher ◽  
Richard B. Ivry ◽  
Sheng-Han Kuo ◽  
David Rydz ◽  
John W. Krakauer ◽  
...  
Keyword(s):  
Implicit Learning ◽  
Prediction Error ◽  
Internal Model ◽  
Sensorimotor Adaptation ◽  
Prediction Errors ◽  
Cerebellar Dysfunction ◽  
Visuomotor Rotation ◽  
Cerebellar Damage ◽  
Internal Forward Model ◽  
Sensory Prediction

AbstractIndividuals with damage to the cerebellum perform poorly in sensorimotor adaptation paradigms. This deficit has been attributed to impairment in sensory-prediction-error-based updating of an internal forward model, a form of implicit learning. These individuals can, however, successfully counter a perturbation when instructed with an explicit aiming strategy. This successful use of an instructed aiming strategy presents a paradox: In adaptation tasks, why don’t individuals with cerebellar damage come up with an aiming solution on their own to compensate for their implicit learning deficit? To explore this question, we employed a variant of a visuomotor rotation task in which, prior to executing a movement on each trial, the participants verbally reported their intended aiming location. Compared to healthy controls, participants with spinocerebellar ataxia (SCA) displayed impairments in both implicit learning and aiming. This was observed when the visuomotor rotation was introduced abruptly (Exp. 1) or gradually (Exp. 2). This dual deficit does not appear to be related to the increased movement variance associated with ataxia: Healthy undergraduates showed little change in implicit learning or aiming when their movement feedback was artificially manipulated to produce similar levels of variability (Exp. 3). Taken together the results indicate that a consequence of cerebellar dysfunction is not only impaired sensory-prediction-error-based learning, but also a difficulty in developing and/or maintaining an aiming solution in response to a visuomotor perturbation. We suggest that this dual deficit can be explained by the cerebellum forming part of a network that learns and maintains action-outcome associations across trials.New and noteworthyIndividuals with cerebellar pathology are impaired in sensorimotor adaptation. This deficit has been attributed to an impairment in error-based learning, specifically, from a deficit in using sensory prediction errors to update an internal model. Here, we show that these individuals also have difficulty in discovering an aiming solution to overcome their adaptation deficit, suggesting a new role for the cerebellum in sensorimotor adaptation tasks.

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