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Distinct replay signatures for prospective decision-making and memory preservation

Theories of neural replay propose that it supports a range of functions, most prominently planning and memory consolidation. Here, we test the hypothesis that distinct signatures of replay in the same task are related to model-based decision-making (“planning”) and memory preservation. We designed a...

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Detalles Bibliográficos
Autores principales: Wimmer, G. Elliott, Liu, Yunzhe, McNamee, Daniel C., Dolan, Raymond J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9963918/
https://www.ncbi.nlm.nih.gov/pubmed/36719914
http://dx.doi.org/10.1073/pnas.2205211120
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author Wimmer, G. Elliott
Liu, Yunzhe
McNamee, Daniel C.
Dolan, Raymond J.
author_facet Wimmer, G. Elliott
Liu, Yunzhe
McNamee, Daniel C.
Dolan, Raymond J.
author_sort Wimmer, G. Elliott
collection PubMed
description Theories of neural replay propose that it supports a range of functions, most prominently planning and memory consolidation. Here, we test the hypothesis that distinct signatures of replay in the same task are related to model-based decision-making (“planning”) and memory preservation. We designed a reward learning task wherein participants utilized structure knowledge for model-based evaluation, while at the same time had to maintain knowledge of two independent and randomly alternating task environments. Using magnetoencephalography and multivariate analysis, we first identified temporally compressed sequential reactivation, or replay, both prior to choice and following reward feedback. Before choice, prospective replay strength was enhanced for the current task-relevant environment when a model-based planning strategy was beneficial. Following reward receipt, and consistent with a memory preservation role, replay for the alternative distal task environment was enhanced as a function of decreasing recency of experience with that environment. Critically, these planning and memory preservation relationships were selective to pre-choice and post-feedback periods, respectively. Our results provide support for key theoretical proposals regarding the functional role of replay and demonstrate that the relative strength of planning and memory-related signals are modulated by ongoing computational and task demands.
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spelling pubmed-99639182023-02-26 Distinct replay signatures for prospective decision-making and memory preservation Wimmer, G. Elliott Liu, Yunzhe McNamee, Daniel C. Dolan, Raymond J. Proc Natl Acad Sci U S A Social Sciences Theories of neural replay propose that it supports a range of functions, most prominently planning and memory consolidation. Here, we test the hypothesis that distinct signatures of replay in the same task are related to model-based decision-making (“planning”) and memory preservation. We designed a reward learning task wherein participants utilized structure knowledge for model-based evaluation, while at the same time had to maintain knowledge of two independent and randomly alternating task environments. Using magnetoencephalography and multivariate analysis, we first identified temporally compressed sequential reactivation, or replay, both prior to choice and following reward feedback. Before choice, prospective replay strength was enhanced for the current task-relevant environment when a model-based planning strategy was beneficial. Following reward receipt, and consistent with a memory preservation role, replay for the alternative distal task environment was enhanced as a function of decreasing recency of experience with that environment. Critically, these planning and memory preservation relationships were selective to pre-choice and post-feedback periods, respectively. Our results provide support for key theoretical proposals regarding the functional role of replay and demonstrate that the relative strength of planning and memory-related signals are modulated by ongoing computational and task demands. National Academy of Sciences 2023-01-31 2023-02-07 /pmc/articles/PMC9963918/ /pubmed/36719914 http://dx.doi.org/10.1073/pnas.2205211120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Social Sciences
Wimmer, G. Elliott
Liu, Yunzhe
McNamee, Daniel C.
Dolan, Raymond J.
Distinct replay signatures for prospective decision-making and memory preservation
title Distinct replay signatures for prospective decision-making and memory preservation
title_full Distinct replay signatures for prospective decision-making and memory preservation
title_fullStr Distinct replay signatures for prospective decision-making and memory preservation
title_full_unstemmed Distinct replay signatures for prospective decision-making and memory preservation
title_short Distinct replay signatures for prospective decision-making and memory preservation
title_sort distinct replay signatures for prospective decision-making and memory preservation
topic Social Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9963918/
https://www.ncbi.nlm.nih.gov/pubmed/36719914
http://dx.doi.org/10.1073/pnas.2205211120
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