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Punishment Feedback Impairs Memory and Changes Cortical Feedback-Related Potentials During Motor Learning

Reward and punishment have demonstrated dissociable effects on motor learning and memory, which suggests that these reinforcers are differently processed by the brain. To test this possibility, we use electroencephalography to record cortical neural activity after the presentation of reward and puni...

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Autores principales: Hill, Christopher M., Stringer, Mason, Waddell, Dwight E., Del Arco, Alberto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7419689/
https://www.ncbi.nlm.nih.gov/pubmed/32848669
http://dx.doi.org/10.3389/fnhum.2020.00294
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author Hill, Christopher M.
Stringer, Mason
Waddell, Dwight E.
Del Arco, Alberto
author_facet Hill, Christopher M.
Stringer, Mason
Waddell, Dwight E.
Del Arco, Alberto
author_sort Hill, Christopher M.
collection PubMed
description Reward and punishment have demonstrated dissociable effects on motor learning and memory, which suggests that these reinforcers are differently processed by the brain. To test this possibility, we use electroencephalography to record cortical neural activity after the presentation of reward and punishment feedback during a visuomotor rotation task. Participants were randomly placed into Reward, Punishment, or Control groups and performed the task under different conditions to assess the adaptation (learning) and retention (memory) of the motor task. These conditions featured an incongruent position between the cursor and the target, with the cursor trajectory, rotated 30° counterclockwise, requiring the participant to adapt their movement to hit the target. Feedback based on error magnitude was provided during the Adaptation condition in the form of a positive number (Reward) or negative number (Punishment), each representing a monetary gain or loss, respectively. No reinforcement or visual feedback was provided during the No Vision condition (retention). Performance error and event-related potentials (ERPs) time-locked to feedback presentation were calculated for each participant during both conditions. Punishment feedback reduced performance error and promoted faster learning during the Adaptation condition. In contrast, punishment feedback increased performance error during the No Vision condition compared to Control and Reward groups, which suggests a diminished motor memory. Moreover, the Punishment group showed a significant decrease in the amplitude of ERPs during the No Vision condition compared to the Adaptation condition. The amplitude of ERPs did not change in the other two groups. These results suggest that punishment feedback impairs motor retention by altering the neural processing involved in memory encoding. This study provides a neurophysiological underpinning for the dissociative effects of punishment feedback on motor learning.
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spelling pubmed-74196892020-08-25 Punishment Feedback Impairs Memory and Changes Cortical Feedback-Related Potentials During Motor Learning Hill, Christopher M. Stringer, Mason Waddell, Dwight E. Del Arco, Alberto Front Hum Neurosci Human Neuroscience Reward and punishment have demonstrated dissociable effects on motor learning and memory, which suggests that these reinforcers are differently processed by the brain. To test this possibility, we use electroencephalography to record cortical neural activity after the presentation of reward and punishment feedback during a visuomotor rotation task. Participants were randomly placed into Reward, Punishment, or Control groups and performed the task under different conditions to assess the adaptation (learning) and retention (memory) of the motor task. These conditions featured an incongruent position between the cursor and the target, with the cursor trajectory, rotated 30° counterclockwise, requiring the participant to adapt their movement to hit the target. Feedback based on error magnitude was provided during the Adaptation condition in the form of a positive number (Reward) or negative number (Punishment), each representing a monetary gain or loss, respectively. No reinforcement or visual feedback was provided during the No Vision condition (retention). Performance error and event-related potentials (ERPs) time-locked to feedback presentation were calculated for each participant during both conditions. Punishment feedback reduced performance error and promoted faster learning during the Adaptation condition. In contrast, punishment feedback increased performance error during the No Vision condition compared to Control and Reward groups, which suggests a diminished motor memory. Moreover, the Punishment group showed a significant decrease in the amplitude of ERPs during the No Vision condition compared to the Adaptation condition. The amplitude of ERPs did not change in the other two groups. These results suggest that punishment feedback impairs motor retention by altering the neural processing involved in memory encoding. This study provides a neurophysiological underpinning for the dissociative effects of punishment feedback on motor learning. Frontiers Media S.A. 2020-08-05 /pmc/articles/PMC7419689/ /pubmed/32848669 http://dx.doi.org/10.3389/fnhum.2020.00294 Text en Copyright © 2020 Hill, Stringer, Waddell and Del Arco. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Human Neuroscience
Hill, Christopher M.
Stringer, Mason
Waddell, Dwight E.
Del Arco, Alberto
Punishment Feedback Impairs Memory and Changes Cortical Feedback-Related Potentials During Motor Learning
title Punishment Feedback Impairs Memory and Changes Cortical Feedback-Related Potentials During Motor Learning
title_full Punishment Feedback Impairs Memory and Changes Cortical Feedback-Related Potentials During Motor Learning
title_fullStr Punishment Feedback Impairs Memory and Changes Cortical Feedback-Related Potentials During Motor Learning
title_full_unstemmed Punishment Feedback Impairs Memory and Changes Cortical Feedback-Related Potentials During Motor Learning
title_short Punishment Feedback Impairs Memory and Changes Cortical Feedback-Related Potentials During Motor Learning
title_sort punishment feedback impairs memory and changes cortical feedback-related potentials during motor learning
topic Human Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7419689/
https://www.ncbi.nlm.nih.gov/pubmed/32848669
http://dx.doi.org/10.3389/fnhum.2020.00294
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