Computational Memory Lab, Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19104.
Department of Neuropsychology, Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum, 44780 Bochum, Germany.
J Neurosci. 2023 Jan 25;43(4):613-620. doi: 10.1523/JNEUROSCI.1045-22.2022. Epub 2022 Dec 8.
Computational models of rodent physiology implicate hippocampal theta as a key modulator of learning and memory (Buzsáki and Moser, 2013; Lisman and Jensen, 2013), yet human hippocampal recordings have shown divergent theta correlates of memory formation. Herweg et al. (2020) suggest that decreases in memory-related broadband power mask narrowband theta increases. Their survey also notes that the theta oscillations appear most prominently in contrasts that isolate memory retrieval processes and when aggregating signals across large brain regions. We evaluate these hypotheses by analyzing human hippocampal recordings captured as 162 neurosurgical patients ( = 86 female) performed a free recall task. Using the Irregular-Resampling Auto-Spectral Analysis (IRASA) to separate broad and narrowband components of the field potential, we show that (1) broadband and narrowband components of theta exhibit opposite effects, with broadband signals decreasing and narrowband theta increasing during successful encoding; (2) whereas low-frequency theta oscillations increase before successful recall, higher-frequency theta and alpha oscillations decrease, masking the positive effect of theta when aggregating across the full band; and (3) the effects of theta on memory encoding and retrieval do not differ between reference schemes that accentuate local signals (bipolar) and those that aggregate signals globally (whole-brain average). In line with computational models that ascribe a fundamental role for hippocampal theta in memory, our large-scale study of human hippocampal recordings shows that 3-4 Hz theta oscillations reliably increase during successful memory encoding and before spontaneous recall of previously studied items. Analyzing recordings from 162 participants, we resolve a long-standing question regarding the role of hippocampal theta oscillations in the formation and retrieval of episodic memories. We show that broadband spectral changes confound estimates of narrowband theta activity, thereby accounting for inconsistent results in the literature. After accounting for broadband effects, we find that increased theta activity marks successful encoding and retrieval of episodic memories, supporting rodent models that ascribe a key role for hippocampal theta in memory function.
啮齿动物生理学的计算模型表明，海马体θ波是学习和记忆的关键调制器（Buzsáki 和 Moser，2013；Lisman 和 Jensen，2013），然而，人类海马体记录显示记忆形成的θ波相关性存在差异。Herweg 等人（2020）认为，记忆相关宽带功率的降低掩盖了窄带θ波的增加。他们的调查还指出，θ 振荡在隔离记忆检索过程的对比中以及在跨大脑区域聚合信号时最为明显。我们通过分析 162 名接受神经外科手术的患者（=86 名女性）在执行自由回忆任务时捕获的人类海马体记录来评估这些假设。使用不规则重采样自谱分析（IRASA）分离场电位的宽带和窄带成分，我们表明：（1）宽带和窄带θ成分表现出相反的效果，在成功编码期间，宽带信号减少，窄带θ波增加；（2）虽然在成功回忆之前低频θ振荡增加，但高频θ和α振荡减少，从而掩盖了在整个频带中聚合时θ的正效应；（3）在强调局部信号（双极）的参考方案和全局聚合信号（全脑平均）之间，θ对记忆编码和检索的影响没有差异。与将海马体θ波归因于记忆的基本作用的计算模型一致，我们对人类海马体记录的大规模研究表明，在成功记忆编码期间以及在自发回忆之前学习过的项目时，3-4 Hzθ 振荡可靠地增加。通过分析 162 名参与者的记录，我们解决了一个关于海马体θ振荡在情节记忆形成和检索中的作用的长期存在的问题。我们表明，宽带谱变化混淆了窄带θ活动的估计，从而解释了文献中的不一致结果。在考虑宽带效应后，我们发现增加的θ活动标志着情节记忆的成功编码和检索，支持将海马体θ波归因于记忆功能的关键作用的啮齿动物模型。
