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.

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 Distinct Processing of Sensory Prediction Error and Task Error during Motor Learning

2021 ◽  
Author(s):  
Jonathan Tsay ◽  
Adrian Haith ◽  
Richard B Ivry ◽  
Hyosub E Kim
Keyword(s):  
Prediction Error ◽  
Sensory Feedback ◽  
Displacement Method ◽  
Visuomotor Learning ◽  
Primary Signal ◽  
Implicit Motor ◽  
Feedback Method ◽  
The Difference ◽  
Sensory Prediction ◽  
And Task

While sensory-prediction error (SPE), the difference between predicted and actual sensory feedback, is recognized as the primary signal that drives implicit motor recalibration, recent studies have shown that task error (TE), the difference between sensory feedback and the movement goal, also plays a modulatory role. To systematically examine how SPE and TE collectively shape implicit recalibration, we performed a series of visuomotor learning experiments, introducing perturbations that varied the size of TE using a popular target displacement method and the size of SPE using a clamped visual feedback method. In Experiments 1 & 2, we observed robust sign-dependent changes in hand angle in response to perturbations with both SPE and TE but failed to observe changes in hand angle in response to TE-only perturbations. Yet in Experiments 3 & 4, the magnitude of TE modulated implicit recalibration in the presence of a fixed SPE. Taken together, these results underscore that implicit recalibration is driven by both SPE and TE (Kim, Parvin, & Ivry, 2019), while specifying unappreciated interactions between these two error-based processes. First, TE only impacts implicit calibration when SPE is present. Second, transient changes occurring when the target is displaced to manipulate TE has an attenuating effect on implicit recalibration, perhaps due to attention being directed away from the sensory feedback.

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 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.

scholarly journals Learning from the path not taken: Sensory prediction errors are sufficient for implicit adaptation of withheld movements

2021 ◽  
Author(s):  
Olivia A Kim ◽  
Alexander D Forrence ◽  
Samuel D McDougle
Keyword(s):  
Sensory Feedback ◽  
Prediction Errors ◽  
Learning Networks ◽  
Model Framework ◽  
Forward Models ◽  
Implicit Motor Learning ◽  
Computer Mouse ◽  
Implicit Motor ◽  
Human Participants ◽  
Sensory Prediction

Current theories of motor control emphasize forward models as a critical component of the brain's motor execution and learning networks. These internal models are thought to predict the consequences of movement before sensory feedback from these movements can reach the brain, allowing for smooth, continuous online motor performance and for the computation of prediction errors that drive implicit motor learning. Taking this framework to its logical extreme, we tested the hypothesis that movements are not necessary for the generation of predictions, the computation of prediction errors, and implicit motor adaptation. Human participants were cued to move a computer mouse to a visually displayed target and were subsequently cued to withhold those movements on a subset of trials. Visual errors displayed on both trials with and without movements to the target induced single-trial learning. Furthermore, learning on trials without movements persisted when accompanying movement trials were never paired with errors and when movement and sensory feedback trajectories were decoupled. These data provide compelling evidence supporting an internal model framework in which forward models generate sensory predictions independent of the generation of movements.

scholarly journals Internal model recalibration does not deteriorate with age while motor adaptation does

2018 ◽  
Author(s):  
Koenraad Vandevoorde ◽  
Jean-Jacques Orban de Xivry
Keyword(s):  
Older People ◽  
Older Women ◽  
Internal Model ◽  
Motor Adaptation ◽  
Cerebellar Degeneration ◽  
Motor Memory ◽  
Cognitive Component ◽  
Age Related ◽  
Wide Range ◽  
Interesting Possibility

AbstractA wide range of motor function declines with aging. Motor adaptation, which occurs when participants learn to reach accurately to a target despite a perturbation, does not deviate from this rule. There are currently three major hypotheses that have been put forward to explain this age-related decline in adaptation: deterioration of internal model recalibration due to age-related cerebellar degeneration, impairment of the cognitive component of motor adaptation, and deficit in the retention of the learned movement. In the present study, we systematically investigated these three hypotheses in a large sample of older women and men. We demonstrate that age-related deficits in motor adaptation are not due to impaired internal model recalibration or impaired retention of motor memory. Rather, we found that the cognitive component was reduced in older people. Therefore, our study suggests the interesting possibility that cerebellar-based mechanisms do not deteriorate with age despite cerebellar degeneration. In contrast, internal model recalibration appears to compensate for deficits in the cognitive component of this type of learning.

scholarly journals Increased upper-limb sensory attenuation with age

2021 ◽  
Author(s):  
Manasa Parthasharathy ◽  
Dante Mantini ◽  
Jean-Jacques Orban de Xivry
Keyword(s):  
Older Adults ◽  
Upper Limb ◽  
Internal Model ◽  
The Body ◽  
The Self ◽  
Model Function ◽  
Force Matching ◽  
External Agent ◽  
Age Related ◽  
Sensory Attenuation

The pressure of our own finger on the arm feels differently than the same pressure exerted by an external agent: the latter involves just touch, whereas the former involves a combination of touch and predictive output from the internal model of the body. This internal model predicts the movement of our own finger and hence the intensity of the sensation of the finger press is decreased. A decrease in intensity of the self-produced stimulus is called sensory attenuation. It has been reported that, due to decreased proprioception with age and an increased reliance on the prediction of the internal model, sensory attenuation is increased in older adults. In this study, we used a force-matching paradigm to test if sensory attenuation is also present over the arm and if aging increases sensory attenuation. We demonstrated that, while both young and older adults overestimate a self-produced force, older adults overestimate it even more showing an increased sensory attenuation. In addition, we also found that both younger and older adults self-produce higher forces when activating the homologous muscles of the upper limb. While this is traditionally viewed as evidence for an increased reliance on internal model function in older adults because of decreased proprioception, proprioception appeared unimpaired in our older participants. This begs the question of whether an age-related decrease in proprioception is really responsible for the increased sensory attenuation observed in older people.

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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