State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China, and.
Department of Psychological Science, University of California, Irvine, California 92697.
J Neurosci. 2019 Jul 3;39(27):5351-5360. doi: 10.1523/JNEUROSCI.2741-18.2019. Epub 2019 Apr 29.
Spaced learning has been shown consistently to benefit memory compared with massed learning, yet the neural representations and processes underlying the spacing effect are still poorly understood. In particular, two influential models (i.e., the encoding variability hypothesis and the study-phase retrieval hypothesis) could both model behavioral performance very well, but they make opposite hypotheses regarding the spacing effect's neural mechanisms. The present study attempted to provide empirical neural evidence to adjudicate these competing hypotheses. Using spatiotemporal pattern similarity (STPS) analysis of EEG data, this study investigated whether and how repetition lags (massed/short-spaced/long-spaced) modulated the STPS's contribution to episodic memory encoding in male and female human participants. The results revealed that greater item-specific STPS in the right frontal electrodes at 543-727 ms after stimulus onset was associated with better memory performance. More importantly, this STPS was larger under the spaced-learning condition than the massed-learning condition and partially mediated the spacing effect on memory performance. In addition, we found that massed learning was associated with stronger repetition suppression in the N400 component that reflected momentary retrieval strength, but reduced activity in the late positive component that was associated with memory retrieval. These results suggest that spaced learning improves long-term memory by increasing retrieval effort and enhancing the pattern reinstatement of prior neural representations, which may be achieved by reducing the momentary retrieval strength as the extended repetition lags might help to eliminate the residual representation in working memory. As one of the most ubiquitous and fundamental phenomena in the history of memory research, the spacing effect provides an important window into understanding how enduring memory is formed in the brain and how different practice strategies could modulate these mechanisms to affect memory performance. By leveraging the neural representational analysis on scalp EEG data, the current study provides the first empirical data to show that spaced learning enhances memory by improving the spatiotemporal similarity that occurs at a late time window. Our results support the study-phase retrieval hypothesis but not the encoding variability hypothesis and emphasize the role of neural pattern reinstatement in strengthening memory via repeated study.
间隔学习相对于集中学习一直被证明可以提高记忆力，但间隔效应的神经表现和过程仍知之甚少。特别是，两个有影响力的模型（即编码变异性假说和学习阶段检索假说）都可以很好地模拟行为表现，但它们对间隔效应的神经机制提出了相反的假设。本研究试图提供经验性的神经证据来裁决这些竞争假说。本研究使用 EEG 数据的时空模式相似性（STPS）分析，研究了重复间隔（集中/短间隔/长间隔）是否以及如何调节 STPS 对男性和女性人类参与者情节记忆编码的贡献。结果表明，刺激后 543-727ms 右侧额电极的项目特异性 STPS 越大，记忆表现越好。更重要的是，与集中学习条件相比，间隔学习条件下的 STPS 更大，并且部分介导了记忆表现的间隔效应。此外，我们发现集中学习与 N400 成分中的更强的重复抑制相关，反映了瞬间检索强度，但减少了与记忆检索相关的晚正成分的活动。这些结果表明，间隔学习通过增加检索努力和增强先前神经表现的模式重新建立来提高长期记忆，这可能是通过降低瞬间检索强度来实现的，因为扩展的重复间隔可能有助于消除工作记忆中的残留表现。作为记忆研究历史上最普遍和最基本的现象之一，间隔效应为理解大脑中如何形成持久记忆以及不同的练习策略如何调节这些机制以影响记忆表现提供了一个重要窗口。通过对头皮 EEG 数据的神经表示分析，本研究提供了第一个经验数据，表明间隔学习通过提高在晚时间窗口发生的时空相似性来增强记忆。我们的结果支持学习阶段检索假说，但不支持编码变异性假说，并强调通过重复学习，神经模式重新建立在增强记忆中的作用。
