The origins of anterograde interference in visuomotor adaptation

Lerner, Gonzalo; Albert, Scott T.; Caffaro, Pedro Alejandro; Villalta, Jorge I.; Jacobacci, Florencia; Shadmehr, Reza; Della‐Maggiore, Valeria

doi:10.1101/593996

Cited by 6 publications

(4 citation statements)

References 39 publications

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“…While many studies have shown that one's rate of learning 58,59 can be altered in numerous contexts such as savings 7,29,31,32,34,48,49 , meta-learning 31,48 , and anterograde interference 60 , we know comparatively little about how the brain controls the total amount of adaptation achieved with prolonged exposures to a perturbation. State-space models of learning 27,61 predict that asymptotic levels of performance are set by the balancing of learning and forgetting 17,62 .…”

Section: The Extent Of Adaptation Is Altered By a Decaying Memory Of ...mentioning

confidence: 99%

An implicit memory of errors limits human sensorimotor adaptation

et al. 2021

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After extended practice, motor adaptation reaches a limit in which learning appears to stop, despite the fact that residual errors persist. What prevents the brain from eliminating the residual errors? Here we found that the adaptation limit was causally dependent on the second order statistics of the perturbation; when variance was high, learning was impaired and large residual errors persisted. However, when learning relied solely on explicit strategy, both the adaptation limit and its dependence on perturbation variability disappeared. In contrast, when learning depended entirely, or in part on implicit learning, residual errors developed. Residual errors in implicit performance were caused by variance-dependent modifications to error sensitivity, not forgetting. These observations are consisted with a model of learning in which the implicit system becomes more sensitive to error when errors are consistent, but forgets this memory of errors over time. Thus, residual errors in motor adaptation are a signature of the implicit learning system, caused by an error sensitivity that depends on the history of past errors. Introduction During motor adaptation, perturbations alter the sensory consequences of motor commands, yielding sensory prediction errors. In humans and other animals, the brain learns from these errors and adjusts its motor commands on subsequent attempts. Over many trials, the adjustments accumulate, but surprisingly, adaptation often remains incomplete; even after extended periods of practice, residual errors persist in many behaviors including reaching 1-4 , saccades 5,6 , and walking 7 . Why does learning appear to stop despite the fact that errors remain?Current models suggest that adaptation is supported by distinct learning systems: one implicit 8 , and the other explicit [9][10][11] . It is thought that the implicit system contributes little to modulation of asymptotic performance; when challenged with fixed errors, the implicit system appears to saturate at identical levels 12,13 . In contrast, explicit strategy provides greater flexibility; its asymptotic behavior is altered as people age [14][15][16] , under different types of feedback 17 , and with the time allotted for the preparation of a movement 18 . Therefore, current evidence suggests that the explicit system alone modifies the asymptotic state of learning.Here we tested this view using stochastic perturbations that affected reaching movements. We found that when perturbation variability was high, residual errors increased [19][20][21] . Furthermore, when perturbation variability was increased mid-experiment, the asymptotic performance decreased, causing participants to lose what they had already learned. Thus, the asymptote of adaptation was not a hard limit, but a dynamic variable that depended on the second order statistics of the perturbation. Which adaptive system was responsible for limiting the adaptation process?To answer this question we isolated implicit and explicit components of adaptation using several methodologies inc...

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Section: The Extent Of Adaptation Is Altered By a Decaying Memory Of ...mentioning

confidence: 99%

An implicit memory of errors limits human sensorimotor adaptation

et al. 2021

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“…Earlier studies that documented modulation of error sensitivity focused on understanding the rate of 355 motor adaptation 16,42 in the context of savings 7,13,26,27,[43][44][45] , meta-learning 26,45 , and anterograde 356 interference 46 . Here we describe yet another feature of adaptation that appears to be controlled 357 through error sensitivity: the total extent of motor adaptation.…”

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An implicit memory of errors limits human sensorimotor adaptation

Albert

Jang

Sheahan

et al. 2019

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22In many forms of motor adaptation, performance approaches a limit at which point learning stops, 23 despite the fact that errors remain. What causes this adaptation limit? Here we found that while reach 24 adaptation exhibited an asymptotic limit, this limit was not fixed: when the variance of the perturbation 25 decreased, the adaptation limit increased, and performance improved. Moreover, the limit could be 26 altered in real-time by changing perturbation variance. The same was true at low reaction times, 27indicating that implicit processes influenced the adaptation limit. Using a mathematical model that 28describes adaptation as a balance between learning and forgetting, we found that participants altered 29 their adaptation limit by changing their sensitivity to reaching errors. Changes in error sensitivity were 30 linked to the consistency of past errors. These observations suggest that during adaptation, time-varying 31 error sensitivities compete with constant forgetting, setting the boundary conditions that produce an 32 apparent limit in total adaptation. 33

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“…While the session order (3° or 30°) was fully counterbalanced across participants, one potential concern in a withinparticipant design of learning is that there may be an effect of transfer or interference between sessions (Avraham et al, 2021;Krakauer et al, 2005;Lerner et al, 2020). For instance, experiencing a 30° clamped feedback in the first session may interfere with learning in the second session, resulting in attenuated learning.…”

Section: Experiments 1: the Impact Of Low Vision On Implicit Motor Adaptation For Small And Large Errorsmentioning

confidence: 99%

“…We thus analyzed the data of 52 unique participants with low vision: 12 participants completed only Experiment 1 (two sessions), 32 participants completed only Experiment 2 (one session), and 8 participants completed both experiments (three sessions). Sessions were spaced at least 24 hours apart to minimize any savings or interference (Avraham et al, 2021;Krakauer et al, 2005;Lerner et al, 2020).…”

Section: Participantsmentioning

confidence: 99%

Low vision impairs implicit sensorimotor adaptation in response to small errors, but not large errors

Tan

Chu

Ivry

et al. 2022

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Successful goal-directed actions require constant fine-tuning in response to errors introduced by changes in the body and environment. This implicit adaptive process has been assumed to operate in a statistically optimal fashion, reducing its sensitivity to errors when sensory uncertainty is high. However, recent work has shown that visual uncertainty attenuates implicit adaptation for small errors, but not large errors, a result that is at odds with an optimal integration hypothesis. This error size interaction has motivated a new hypothesis that sensory uncertainty impacts the distribution of the perceived error locations but not the system's sensitivity to errors. To examine these competing hypotheses, previous studies have experimentally manipulated uncertainty. But it is unknown which hypothesis best describes motor adaptation to sensory uncertainty experienced during daily life. To address this question, we recruited individuals with low vision due to diverse clinical conditions impacting visual uncertainty and matched controls. The groups were tested on visuomotor tasks designed to isolate implicit adaptation and maintain tight control over the error size. In two experiments, low vision was associated with attenuated implicit adaptation only for small errors, but not for large errors. Taken together with prior work in which visual uncertainty was experimentally manipulated, these results support the notion that increasing sensory uncertainty increases the likelihood that errors are mis-localized but does not affect error sensitivity, offering a novel account for the motor learning deficits seen in low vision.

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The origins of anterograde interference in visuomotor adaptation

Cited by 6 publications

References 39 publications

An implicit memory of errors limits human sensorimotor adaptation

An implicit memory of errors limits human sensorimotor adaptation

An implicit memory of errors limits human sensorimotor adaptation

Low vision impairs implicit sensorimotor adaptation in response to small errors, but not large errors

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