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A Single-Rate Context-Dependent Learning Process Underlies Rapid Adaptation to Familiar Object Dynamics

Motor learning has been extensively studied using dynamic (force-field) perturbations. These induce movement errors that result in adaptive changes to the motor commands. Several state-space models have been developed to explain how trial-by-trial errors drive the progressive adaptation observed in...

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Autores principales: Ingram, James N., Howard, Ian S., Flanagan, J. Randall, Wolpert, Daniel M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3182866/
https://www.ncbi.nlm.nih.gov/pubmed/21980277
http://dx.doi.org/10.1371/journal.pcbi.1002196
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author Ingram, James N.
Howard, Ian S.
Flanagan, J. Randall
Wolpert, Daniel M.
author_facet Ingram, James N.
Howard, Ian S.
Flanagan, J. Randall
Wolpert, Daniel M.
author_sort Ingram, James N.
collection PubMed
description Motor learning has been extensively studied using dynamic (force-field) perturbations. These induce movement errors that result in adaptive changes to the motor commands. Several state-space models have been developed to explain how trial-by-trial errors drive the progressive adaptation observed in such studies. These models have been applied to adaptation involving novel dynamics, which typically occurs over tens to hundreds of trials, and which appears to be mediated by a dual-rate adaptation process. In contrast, when manipulating objects with familiar dynamics, subjects adapt rapidly within a few trials. Here, we apply state-space models to familiar dynamics, asking whether adaptation is mediated by a single-rate or dual-rate process. Previously, we reported a task in which subjects rotate an object with known dynamics. By presenting the object at different visual orientations, adaptation was shown to be context-specific, with limited generalization to novel orientations. Here we show that a multiple-context state-space model, with a generalization function tuned to visual object orientation, can reproduce the time-course of adaptation and de-adaptation as well as the observed context-dependent behavior. In contrast to the dual-rate process associated with novel dynamics, we show that a single-rate process mediates adaptation to familiar object dynamics. The model predicts that during exposure to the object across multiple orientations, there will be a degree of independence for adaptation and de-adaptation within each context, and that the states associated with all contexts will slowly de-adapt during exposure in one particular context. We confirm these predictions in two new experiments. Results of the current study thus highlight similarities and differences in the processes engaged during exposure to novel versus familiar dynamics. In both cases, adaptation is mediated by multiple context-specific representations. In the case of familiar object dynamics, however, the representations can be engaged based on visual context, and are updated by a single-rate process.
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spelling pubmed-31828662011-10-06 A Single-Rate Context-Dependent Learning Process Underlies Rapid Adaptation to Familiar Object Dynamics Ingram, James N. Howard, Ian S. Flanagan, J. Randall Wolpert, Daniel M. PLoS Comput Biol Research Article Motor learning has been extensively studied using dynamic (force-field) perturbations. These induce movement errors that result in adaptive changes to the motor commands. Several state-space models have been developed to explain how trial-by-trial errors drive the progressive adaptation observed in such studies. These models have been applied to adaptation involving novel dynamics, which typically occurs over tens to hundreds of trials, and which appears to be mediated by a dual-rate adaptation process. In contrast, when manipulating objects with familiar dynamics, subjects adapt rapidly within a few trials. Here, we apply state-space models to familiar dynamics, asking whether adaptation is mediated by a single-rate or dual-rate process. Previously, we reported a task in which subjects rotate an object with known dynamics. By presenting the object at different visual orientations, adaptation was shown to be context-specific, with limited generalization to novel orientations. Here we show that a multiple-context state-space model, with a generalization function tuned to visual object orientation, can reproduce the time-course of adaptation and de-adaptation as well as the observed context-dependent behavior. In contrast to the dual-rate process associated with novel dynamics, we show that a single-rate process mediates adaptation to familiar object dynamics. The model predicts that during exposure to the object across multiple orientations, there will be a degree of independence for adaptation and de-adaptation within each context, and that the states associated with all contexts will slowly de-adapt during exposure in one particular context. We confirm these predictions in two new experiments. Results of the current study thus highlight similarities and differences in the processes engaged during exposure to novel versus familiar dynamics. In both cases, adaptation is mediated by multiple context-specific representations. In the case of familiar object dynamics, however, the representations can be engaged based on visual context, and are updated by a single-rate process. Public Library of Science 2011-09-29 /pmc/articles/PMC3182866/ /pubmed/21980277 http://dx.doi.org/10.1371/journal.pcbi.1002196 Text en Ingram et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Ingram, James N.
Howard, Ian S.
Flanagan, J. Randall
Wolpert, Daniel M.
A Single-Rate Context-Dependent Learning Process Underlies Rapid Adaptation to Familiar Object Dynamics
title A Single-Rate Context-Dependent Learning Process Underlies Rapid Adaptation to Familiar Object Dynamics
title_full A Single-Rate Context-Dependent Learning Process Underlies Rapid Adaptation to Familiar Object Dynamics
title_fullStr A Single-Rate Context-Dependent Learning Process Underlies Rapid Adaptation to Familiar Object Dynamics
title_full_unstemmed A Single-Rate Context-Dependent Learning Process Underlies Rapid Adaptation to Familiar Object Dynamics
title_short A Single-Rate Context-Dependent Learning Process Underlies Rapid Adaptation to Familiar Object Dynamics
title_sort single-rate context-dependent learning process underlies rapid adaptation to familiar object dynamics
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3182866/
https://www.ncbi.nlm.nih.gov/pubmed/21980277
http://dx.doi.org/10.1371/journal.pcbi.1002196
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