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Distinct replay signatures for prospective decision-making and memory preservation

Wimmer, G Elliott; Liu, Yunzhe; McNamee, Daniel C; Dolan, Raymond J; (2023) Distinct replay signatures for prospective decision-making and memory preservation. Proceedings of the National Academy of Sciences , 120 (6) , Article e2205211120. 10.1073/pnas.2205211120. Green open access

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Abstract

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.

Type: Article
Title: Distinct replay signatures for prospective decision-making and memory preservation
Open access status: An open access version is available from UCL Discovery
DOI: 10.1073/pnas.2205211120
Publisher version: https://doi.org/10.1073/pnas.2205211120
Language: English
Additional information: Copyright © 2023 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).
Keywords: planning, memory, replay, hippocampus, decision-making
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology > Imaging Neuroscience
URI: https://discovery.ucl.ac.uk/id/eprint/10164234
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