Distinct replay signatures for prospective decision-making and memory preservation

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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 decisionmaking (‘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 (MEG) 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. Our results provide new 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 on-going computational and task demands. Significance statement: The sequential neural reactivation of prior experience, known as replay, is considered to be an important mechanism for both future planning and preserving memories of the past. Whether, and how, replay supports both of these functions remains unknown. Here, in humans, we found that prior to a choice, rapid replay of potential future paths was enhanced when planning was more beneficial. By contrast, after choice feedback, when no future actions are imminent, we found evidence for a memory preservation signal evident in enhanced replay of paths that had been visited less in the recent past. The results demonstrate that distinct replay signatures, expressed at different times, relate to two dissociable cognitive functions.
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