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Single-trial modeling separates multiple overlapping prediction errors during reward processing in human EEG

Learning signals during reinforcement learning and cognitive control rely on valenced reward prediction errors (RPEs) and non-valenced salience prediction errors (PEs) driven by surprise magnitude. A core debate in reward learning focuses on whether valenced and non-valenced PEs can be isolated in t...

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Autores principales: Hoy, Colin W., Steiner, Sheila C., Knight, Robert T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8302587/
https://www.ncbi.nlm.nih.gov/pubmed/34302057
http://dx.doi.org/10.1038/s42003-021-02426-1
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author Hoy, Colin W.
Steiner, Sheila C.
Knight, Robert T.
author_facet Hoy, Colin W.
Steiner, Sheila C.
Knight, Robert T.
author_sort Hoy, Colin W.
collection PubMed
description Learning signals during reinforcement learning and cognitive control rely on valenced reward prediction errors (RPEs) and non-valenced salience prediction errors (PEs) driven by surprise magnitude. A core debate in reward learning focuses on whether valenced and non-valenced PEs can be isolated in the human electroencephalogram (EEG). We combine behavioral modeling and single-trial EEG regression to disentangle sequential PEs in an interval timing task dissociating outcome valence, magnitude, and probability. Multiple regression across temporal, spatial, and frequency dimensions characterized a spatio-tempo-spectral cascade from early valenced RPE value to non-valenced RPE magnitude, followed by outcome probability indexed by a late frontal positivity. Separating negative and positive outcomes revealed the valenced RPE value effect is an artifact of overlap between two non-valenced RPE magnitude responses: frontal theta feedback-related negativity on losses and posterior delta reward positivity on wins. These results reconcile longstanding debates on the sequence of components representing reward and salience PEs in the human EEG.
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spelling pubmed-83025872021-08-12 Single-trial modeling separates multiple overlapping prediction errors during reward processing in human EEG Hoy, Colin W. Steiner, Sheila C. Knight, Robert T. Commun Biol Article Learning signals during reinforcement learning and cognitive control rely on valenced reward prediction errors (RPEs) and non-valenced salience prediction errors (PEs) driven by surprise magnitude. A core debate in reward learning focuses on whether valenced and non-valenced PEs can be isolated in the human electroencephalogram (EEG). We combine behavioral modeling and single-trial EEG regression to disentangle sequential PEs in an interval timing task dissociating outcome valence, magnitude, and probability. Multiple regression across temporal, spatial, and frequency dimensions characterized a spatio-tempo-spectral cascade from early valenced RPE value to non-valenced RPE magnitude, followed by outcome probability indexed by a late frontal positivity. Separating negative and positive outcomes revealed the valenced RPE value effect is an artifact of overlap between two non-valenced RPE magnitude responses: frontal theta feedback-related negativity on losses and posterior delta reward positivity on wins. These results reconcile longstanding debates on the sequence of components representing reward and salience PEs in the human EEG. Nature Publishing Group UK 2021-07-23 /pmc/articles/PMC8302587/ /pubmed/34302057 http://dx.doi.org/10.1038/s42003-021-02426-1 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Hoy, Colin W.
Steiner, Sheila C.
Knight, Robert T.
Single-trial modeling separates multiple overlapping prediction errors during reward processing in human EEG
title Single-trial modeling separates multiple overlapping prediction errors during reward processing in human EEG
title_full Single-trial modeling separates multiple overlapping prediction errors during reward processing in human EEG
title_fullStr Single-trial modeling separates multiple overlapping prediction errors during reward processing in human EEG
title_full_unstemmed Single-trial modeling separates multiple overlapping prediction errors during reward processing in human EEG
title_short Single-trial modeling separates multiple overlapping prediction errors during reward processing in human EEG
title_sort single-trial modeling separates multiple overlapping prediction errors during reward processing in human eeg
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8302587/
https://www.ncbi.nlm.nih.gov/pubmed/34302057
http://dx.doi.org/10.1038/s42003-021-02426-1
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