Cargando…

Rapid Visuomotor Responses Reflect Value-Based Decisions

Cognitive decision-making is known to be sensitive to the values of potential options, which are the probability and size of rewards associated with different choices. Here, we examine whether rapid motor responses to perturbations of visual feedback about movement, which mediate low-level and invol...

Descripción completa

Detalles Bibliográficos
Autores principales: Carroll, Timothy J., McNamee, Daniel, Ingram, James N., Wolpert, Daniel M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6520503/
https://www.ncbi.nlm.nih.gov/pubmed/30850511
http://dx.doi.org/10.1523/JNEUROSCI.1934-18.2019
_version_ 1783418752336920576
author Carroll, Timothy J.
McNamee, Daniel
Ingram, James N.
Wolpert, Daniel M.
author_facet Carroll, Timothy J.
McNamee, Daniel
Ingram, James N.
Wolpert, Daniel M.
author_sort Carroll, Timothy J.
collection PubMed
description Cognitive decision-making is known to be sensitive to the values of potential options, which are the probability and size of rewards associated with different choices. Here, we examine whether rapid motor responses to perturbations of visual feedback about movement, which mediate low-level and involuntary feedback control loops, reflect computations associated with high-level value-based decision-making. In three experiments involving human participants, we varied the value associated with different potential targets for reaching movements by controlling the distributions of rewards across the targets (Experiment 1), the probability with which each target could be specified (Experiment 2), or both (Experiment 3). We found that the size of rapid and involuntary feedback responses to movement perturbations was strongly influenced by the relative value between targets. A statistical model of relative value that includes a term for risk sensitivity provided the best fit to the visuomotor response data, illustrating that feedback control policies are biased to favor more frequent task success at the expense of the overall extrinsic reward accumulated through movement. Importantly however, the regulation of rapid feedback responses was associated with successful pursuit of high-value task outcomes. This implies that when we move, the brain specifies a set of feedback control gains that enable low-level motor areas not only to generate efficient and accurate movement, but also to rapidly and adaptively respond to evolving sensory information in a manner consistent with value-based decision-making. SIGNIFICANCE STATEMENT Current theories of sensorimotor control suggest that, rather than selecting and planning the details of movements in advance, the role of the brain is to set time-varying feedback gains that continuously transform sensory information into motor commands by feedback control. Here, we examine whether the fastest motor responses to perturbations of movement, which mediate low-level and involuntary feedback control loops (i.e., reflexes), reflect computations associated with high-level, value-based decision-making. We find that rapid feedback responses during reaching reflect the relative probabilities and rewards associated with target options. This suggests that low-order components of the sensorimotor control hierarchy, which generate rapid and automatic responses, can continuously evaluate evolving sensory evidence and initiate responses according to the prospect of reward.
format Online
Article
Text
id pubmed-6520503
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Society for Neuroscience
record_format MEDLINE/PubMed
spelling pubmed-65205032019-05-17 Rapid Visuomotor Responses Reflect Value-Based Decisions Carroll, Timothy J. McNamee, Daniel Ingram, James N. Wolpert, Daniel M. J Neurosci Research Articles Cognitive decision-making is known to be sensitive to the values of potential options, which are the probability and size of rewards associated with different choices. Here, we examine whether rapid motor responses to perturbations of visual feedback about movement, which mediate low-level and involuntary feedback control loops, reflect computations associated with high-level value-based decision-making. In three experiments involving human participants, we varied the value associated with different potential targets for reaching movements by controlling the distributions of rewards across the targets (Experiment 1), the probability with which each target could be specified (Experiment 2), or both (Experiment 3). We found that the size of rapid and involuntary feedback responses to movement perturbations was strongly influenced by the relative value between targets. A statistical model of relative value that includes a term for risk sensitivity provided the best fit to the visuomotor response data, illustrating that feedback control policies are biased to favor more frequent task success at the expense of the overall extrinsic reward accumulated through movement. Importantly however, the regulation of rapid feedback responses was associated with successful pursuit of high-value task outcomes. This implies that when we move, the brain specifies a set of feedback control gains that enable low-level motor areas not only to generate efficient and accurate movement, but also to rapidly and adaptively respond to evolving sensory information in a manner consistent with value-based decision-making. SIGNIFICANCE STATEMENT Current theories of sensorimotor control suggest that, rather than selecting and planning the details of movements in advance, the role of the brain is to set time-varying feedback gains that continuously transform sensory information into motor commands by feedback control. Here, we examine whether the fastest motor responses to perturbations of movement, which mediate low-level and involuntary feedback control loops (i.e., reflexes), reflect computations associated with high-level, value-based decision-making. We find that rapid feedback responses during reaching reflect the relative probabilities and rewards associated with target options. This suggests that low-order components of the sensorimotor control hierarchy, which generate rapid and automatic responses, can continuously evaluate evolving sensory evidence and initiate responses according to the prospect of reward. Society for Neuroscience 2019-05-15 /pmc/articles/PMC6520503/ /pubmed/30850511 http://dx.doi.org/10.1523/JNEUROSCI.1934-18.2019 Text en Copyright © 2019 Carroll et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Carroll, Timothy J.
McNamee, Daniel
Ingram, James N.
Wolpert, Daniel M.
Rapid Visuomotor Responses Reflect Value-Based Decisions
title Rapid Visuomotor Responses Reflect Value-Based Decisions
title_full Rapid Visuomotor Responses Reflect Value-Based Decisions
title_fullStr Rapid Visuomotor Responses Reflect Value-Based Decisions
title_full_unstemmed Rapid Visuomotor Responses Reflect Value-Based Decisions
title_short Rapid Visuomotor Responses Reflect Value-Based Decisions
title_sort rapid visuomotor responses reflect value-based decisions
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6520503/
https://www.ncbi.nlm.nih.gov/pubmed/30850511
http://dx.doi.org/10.1523/JNEUROSCI.1934-18.2019
work_keys_str_mv AT carrolltimothyj rapidvisuomotorresponsesreflectvaluebaseddecisions
AT mcnameedaniel rapidvisuomotorresponsesreflectvaluebaseddecisions
AT ingramjamesn rapidvisuomotorresponsesreflectvaluebaseddecisions
AT wolpertdanielm rapidvisuomotorresponsesreflectvaluebaseddecisions