Human hippocampal replay during rest prioritizes weakly-learned information and predicts memory performance

There is now extensive evidence that the hippocampus replays experiences during
quiet rest periods, and that this replay benefits subsequent memory. A critical open
question is how memories are prioritized for replay during these offline periods. We
addressed this question in an experiment in which participants learned the features of 15
objects and then underwent fMRI scanning to track item-level replay in the hippocampus
using pattern analysis during a rest period. Objects that were remembered less well were
replayed more during the subsequent rest period, suggesting a prioritization process in
which weaker memories—memories most vulnerable to forgetting—are selected for
wake replay. Participants came back for a second session, either after a night of sleep or a
day awake, and underwent another scanned rest period followed by a second memory
test. In the second session, more hippocampal replay of a satellite during the rest period
predicted better subsequent memory for that satellite. Only in the group with intervening
sleep did rest replay predict improvement from the first to second session. Our results
provide the first evidence that replay of individual memories occurs during rest in the
human hippocampus and that this replay prioritizes weakly learned information, predicts
subsequent memory performance, and relates to memory improvement across a delay
with sleep.

现有大量研究证据表明，海马体（hippocampus）会在安静休息时段回放过往经历，且该回放过程可改善后续记忆表现。目前学界尚未明确的核心问题之一是：在这类离线休息时段中，记忆该如何被优先遴选以进行回放。本研究通过一项实验针对该问题展开探究：受试者首先学习15种物品的特征，随后进入休息阶段，期间借助模式分析技术，通过功能磁共振成像（fMRI）追踪海马体中单个物品的回放活动。实验结果显示，记忆识别表现较差的物品，其在后续休息时段的回放频次更高，这提示存在一套记忆优先级调控机制：最易受遗忘影响的弱记忆会被挑选出来进行回放。受试者随后分为两组，分别经过一晚睡眠或一日清醒状态后返回参与第二阶段实验：期间再次开展带扫描的休息阶段，随后完成第二次记忆测试。在第二阶段实验中，休息时段内海马体对某颗卫星的回放频次越高，该卫星后续的记忆识别表现就越好。仅在经历睡眠间隔的组别中，休息时段的回放活动能够预测受试者从第一阶段到第二阶段的记忆提升幅度。本研究结果首次提供直接证据表明：人类海马体在休息时段会对单个记忆进行回放，且该回放过程会优先选择学习程度较弱的信息，能够有效预测后续记忆表现，并与睡眠间隔期内的记忆提升存在显著关联。