Cross Zachariah R, Helfrich Randolph F, Corcoran Andrew W, Dede Adam J O, Kohler Mark J, Coussens Scott W, Zou-Williams Lena, Schlesewsky Matthias, Gaskell Gareth M, Knight Robert T, Bornkessel-Schlesewsky Ina
Cognitive Neuroscience Laboratory - Australian Research Centre for Interactive and Virtual Environments, University of South Australia, Adelaide, South Australia 5072, Australia
Department of Medical Social Sciences, Northwestern Feinberg School of Medicine, Northwestern University, Chicago, Illinois 60611.
J Neurosci. 2025 Jan 15;45(3):e2193232024. doi: 10.1523/JNEUROSCI.2193-23.2024.
Sentence comprehension involves the decoding of both semantic and grammatical information, a process fundamental to communication. As with other complex cognitive processes, language comprehension relies, in part, on long-term memory. However, the electrophysiological mechanisms underpinning the encoding and generalization of higher-order linguistic knowledge remain elusive, particularly from a sleep-based consolidation perspective. One candidate mechanism that may support the consolidation of higher-order language is the coordination of slow oscillations (SO) and sleep spindles during nonrapid eye movement sleep (NREM). To examine this hypothesis, we analyzed electroencephalographic (EEG) data recorded from 35 participants ( = 25.4; SD = 7.10; 16 males) during an artificial language learning task, contrasting performance between individuals who were given an 8 h nocturnal sleep period or an equivalent period of wake. We found that sleep relative to wake was associated with superior performance for sequence-based word order rules. Postsleep sequence-based word order processing was further associated with less task-related theta desynchronization, an electrophysiological signature of successful memory consolidation, as well as cognitive control and working memory. Frontal NREM SO-spindle coupling was also positively associated with behavioral sensitivity to sequence-based word order rules, as well as with task-related theta power. As such, theta activity during retrieval of previously learned information correlates with SO-spindle coupling, thus linking neural activity in the sleeping and waking brain. Taken together, this study presents converging behavioral and neurophysiological evidence for a role of NREM SO-spindle coupling and task-related theta activity as signatures of memory consolidation and retrieval in the context of higher-order language learning.
句子理解涉及语义和语法信息的解码，这是交流的基本过程。与其他复杂的认知过程一样，语言理解部分依赖于长期记忆。然而，支撑高阶语言知识编码和泛化的电生理机制仍然难以捉摸，特别是从基于睡眠的巩固角度来看。一种可能支持高阶语言巩固的候选机制是非快速眼动睡眠（NREM）期间慢振荡（SO）和睡眠纺锤波的协调。为了检验这一假设，我们分析了35名参与者（年龄 = 25.4岁；标准差 = 7.10；16名男性）在人工语言学习任务期间记录的脑电图（EEG）数据，对比了有8小时夜间睡眠时间或同等时长清醒时间的个体之间的表现。我们发现，相对于清醒状态，睡眠与基于序列的词序规则的更好表现相关。睡眠后基于序列的词序处理进一步与较少的任务相关θ去同步化相关，这是成功记忆巩固以及认知控制和工作记忆的电生理特征。额叶NREM期的SO-纺锤波耦合也与对基于序列的词序规则的行为敏感性以及任务相关的θ功率呈正相关。因此，在检索先前学习的信息时，θ活动与SO-纺锤波耦合相关，从而将睡眠和清醒大脑中的神经活动联系起来。综上所述，本研究提供了行为和神经生理学的综合证据，证明NREM期的SO-纺锤波耦合和任务相关的θ活动在高阶语言学习背景下作为记忆巩固和检索的标志所起的作用。
