前额叶−海马−内侧隔核环路的theta-gamma相位幅值耦合: 跨脑区协同与工作记忆调控机制

doi:10.3724/SP.J.1042.2026.0499

摘要/Abstract

摘要：

工作记忆作为高级认知功能的核心, 依赖于前额叶−海马−内侧隔核神经环路的动态协同, 其中theta-gamma相位幅值耦合(TG-PAC)是跨脑区信息整合的关键机制。本文系统阐述了前额叶−海马−内侧隔核神经环路中theta-gamma相位幅值耦合在工作记忆中的核心调控作用。研究表明, 前额叶通过持续性神经活动维持工作记忆中的信息表征, 其theta振荡(4~8 Hz)通过相位调制gamma活动(30~80 Hz)形成认知控制的神经时间窗。海马作为空间信息处理的枢纽, 通过theta-gamma嵌套编码实现空间导航与工作记忆绑定, 其局部gamma振荡与theta振荡的耦合强度可预测记忆容量与行为表现。前额叶theta相位与海马gamma幅值的跨脑区耦合, 构成了认知控制与记忆存储的动态交互界面, 确保工作记忆任务的精准执行。内侧隔核作为关键中继节点, 其胆碱能、GABA能神经元通过调控海马theta振荡, 影响海马theta-gamma相位幅值耦合的强度与时空特性, 进而调节工作记忆效能。此外, TG-PAC异常与精神分裂症、阿尔茨海默病等认知功能障碍密切相关, 提示其作为潜在生物标志物和神经调控靶点的临床价值。本文创新性整合前额叶−海马−内侧隔核三节点环路之间的theta-gamma相位幅值耦合, 并展望未来研究需结合多模态成像、细胞特异性调控与计算建模, 以推动基于神经振荡耦合的认知障碍干预新策略。

关键词: 工作记忆, theta-gamma相位幅值耦合, 交叉节律耦合, 前额叶, 海马, 内侧隔核

Abstract:

Working memory, as a core component of higher-order cognitive functions, its neural basis involves the dynamic coordination mechanisms among distributed neural networks. Although the functions of the prefrontal cortex (PFC) and hippocampus in working memory have been intensively investigated, the neural mechanisms underlying cross-brain region information integration, especially the role of key sub-cortical structures in this process, still await systematic elucidation. This review aims to address a crucial scientific question: As a key hub between the PFC and hippocampus, how does the medial septal nucleus (MS) regulate working memory through the theta-gamma phase-amplitude coupling mechanism and thus mediate the information transmission process in the PFC-hippocampal-MS three-node circuit? Based on this, we propose and elaborate on an innovative “three-node coordination model”. This model systematically integrates the MS into the classical PFC-hippocampus working memory framework for the first time and identifies theta-gamma phase-amplitude coupling as the core electrophysiological mechanism for achieving cross-brain region coordination.

By integrating evidence from neuroanatomical and functional studies, this research has established that the MS is not merely a simple information relay station but an active regulatory hub within the working memory circuit. In terms of neural connectivity architecture, the MS has direct synaptic connections with both the PFC and hippocampus. This unique neural connectivity enables the MS with an irreplaceable role in coordinating the activities of the PFC and hippocampus. At the functional mechanism level, GABAergic neurons in the MS exhibit distinct theta-frequency burst firing characteristics and are considered the pacemaker source of the hippocampal theta rhythm. Applying “theta rhythm stimulation” to the MS using optogenetic techniques can effectively enhance the power of hippocampal theta oscillations and significantly improve the behavioral performance of spatial working memory. These causal findings comprehensively demonstrate the indispensability of the MS in working memory information processing.

Theta-gamma phase-amplitude coupling serves as the fundamental neural coding mechanism for information integration in the three-node circuit. Specifically, theta oscillations provide a global temporal reference framework for cross-brain region information transmission, while gamma oscillations act as local information representation units nested within specific theta phases. There is a complex bidirectional theta-gamma phase-amplitude regulatory process between the PFC and hippocampal circuits. During the information encoding stage of working memory, the hippocampus transmits environmental information to the PFC. During the working memory decision-making stage, the PFC exerts top-down executive control over the hippocampus. Both of these processes are mediated by theta-gamma coupling. The MS profoundly influences the strength and spatio-temporal characteristics of hippocampal theta-gamma coupling by regulating the hippocampal theta rhythm. Meanwhile, the feedback loop of somatostatin-positive interneurons in the hippocampus enables dynamic fine-tuning to prevent excessive network synchronization. This multi-level regulatory mechanism solidifies the central position of the MS in neural information integration. Moreover, abnormal theta-gamma coupling in the PFC-hippocampal-MS circuit is closely associated with cognitive deficits in various neuropsychiatric disorders.

In summary, this study has established the critical regulatory role of the MS during the maintenance phase of working memory, clarified its mechanism of controlling the hippocampal theta rhythm via the GABAergic pathway; revealed the neural pathway through which the MS, as a theta oscillation regulatory hub, influences local hippocampal activity and thereby regulates overall working memory efficiency; and constructed a “PFC-hippocampal-MS three-node circuit model”, which for the first time systematically incorporates the MS into the working memory theoretical framework. Future research should combine multimodal neuroimaging, cell-specific regulation, and computational modeling approaches to delve deeper into the functional connectivity between the PFC and MS and the dynamic characteristics of theta-gamma coupling, providing a theoretical foundation for promoting intervention strategies for cognitive impairments based on neural oscillations.

Key words: working memory, θ-γ phase amplitude coupling, cross-frequency coupling, prefrontal cortex, hippocampus, medial Septal neural

中图分类号:

B845

张秋霞, 陈伟海. (2026). 前额叶−海马−内侧隔核环路的theta-gamma相位幅值耦合: 跨脑区协同与工作记忆调控机制. 心理科学进展 , 34(3), 499-514.

ZHANG Qiuxia, CHEN Weihai. (2026). Theta-gamma phase-amplitude coupling in the prefrontal-hippocampal- medial septal circuit: Mechanisms of cross-regional coordination and working memory regulation. Advances in Psychological Science, 34(3), 499-514.

图/表 3

图1 神经振荡的交叉节律耦合示意图。(A)相位−相位耦合(PPC); (B)幅值−幅值耦合(AAC); (C)相位−幅值耦合(PAC)。

图2 gamma振荡周期中的全局性抑制如何决定哪些神经元放电。图片中三种不同灰度的直线分别代表了一个gamma周期内兴奋性由强到弱的三种神经元, 浅灰代表最兴奋的神经元, 中灰代表中等兴奋的神经元, 黑色的则代表低等兴奋神经元。在一个gamma周期中, 伴随着中间神经元对周围神经元抑制的衰减(由抑制性突触后电位的时间常数tau决定), 最兴奋的神经元最先放电, 一旦某个神经元放电, 它会通过快速抑制性中间神经元触发全局反馈抑制, 阻止其他神经元继续放电, 然而, 由于反馈抑制的传递存在延迟(d), 在这个延迟期窗口内, 兴奋性略低于最兴奋神经元的其他神经元(中等强度的神经元)也有机会放电。

图3 低频振荡(如theta振荡)相位和gamma功率之间的耦合可以促进跨区域之间信息的同频协调。(A)脑区A和C中的神经元进行通信时, 它们通过低频(如theta振荡)波段进行连贯的同频振荡, 通常gamma振荡嵌套在theta振荡中, 即TG-PAC。因此脑区A中的gamma活动将能够传递到C区中的神经元, A和C中的gamma振荡将保持同频。在脑区B则作为脑区C低频振荡的外部重要驱动源, 间接影响脑区A和脑区C之间的TG-PAC。(B)图中三角形、圆形和正方形分别代表谷氨酸能神经元、GABA能神经元和胆碱能神经元, 图中显示了前额叶、内侧隔核和海马三者之间的神经联系, 其中内侧隔核内部三种神经元局部相互连接, 形成密集的局部网络, 内侧隔核的GABA能神经元和谷氨酸能神经元主要终止于海马CA1区的GABA能神经元; 海马CA1的谷氨酸能神经元投射至前额叶区域; 前额叶则与内侧隔核和外侧隔核均有突触联系。前额叶与海马、内侧隔核与海马之间存在的theta-gamma相位幅值耦合也以波形的方式在三个脑区之间标出。

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