Choi Kyuwan, Bagen Lisa, Robinson Linley, Umbach Gray, Rugg Michael, Lega Bradley
Department of Neurosurgery, University of Texas Southwestern, Dallas, TX 75390, USA.
Center for Vital Longevity, University of Texas at Dallas, Dallas, TX 75235, USA.
Cereb Cortex Commun. 2020;1(1):tgaa010. doi: 10.1093/texcom/tgaa010. Epub 2020 Apr 14.
The question of longitudinal hippocampal functional specialization is critical to human episodic memory because an accurate understanding of this phenomenon would impact theories of mnemonic function and entail practical consequences for the clinical management of patients undergoing temporal lobe surgery. The implementation of the robotically assisted stereo electroencephalography technique for seizure mapping has provided our group with the opportunity to obtain recordings simultaneously from the anterior and posterior human hippocampus, allowing us to create an unparalleled data set of human subjects with simultaneous anterior and posterior hippocampal recordings along with several cortical regions. Using these data, we address several key questions governing functional hippocampal connectivity in human memory. First, we ask whether functional networks during episodic memory encoding and retrieval are significantly different for the anterior versus posterior hippocampus (PH). We also examine how connections differ across the 2-5 Hz versus 4-9 Hz theta frequency ranges, directly addressing the relative contribution of each of these separate bands in hippocampal-cortical interactions. While we report some overlapping connections, we observe evidence of distinct anterior versus posterior hippocampal networks during memory encoding related to frontal and parietal connectivity as well as hemispheric differences in aggregate connectivity. We frame these findings in light of the proposed AT/PM memory systems. We also observe distinct encoding versus retrieval connectivity patterns between anterior and posterior hippocampal networks, we find that overall connectivity is greater for the PH in the right hemisphere, and further that these networks significantly differ in terms of frontal and parietal connectivity. We place these findings in the context of existing theoretical treatments of human memory systems, especially the proposed AT/PM system. During memory retrieval, we observe significant differences between slow-theta (2-5 Hz) and fast-theta (4-9 Hz) connectivity between the cortex and hippocampus. Finally, we test how these distinct theta frequency oscillations propagate within the hippocampus, using phase slope index to estimate the direction slow-theta and fast-theta oscillations travel during encoding and retrieval. We uncover evidence that 2-5 Hz oscillations travel in the posterior-to-anterior direction, while 5-9 Hz oscillations travel from anterior-to-posterior. Taken together, our findings describe mnemonically relevant functional connectivity differences along the longitudinal axis of the human hippocampus that will inform interpretation of models of hippocampal function that seek to integrate rodent and human data.
海马体纵向功能特化问题对于人类情景记忆至关重要，因为准确理解这一现象将影响记忆功能理论，并对接受颞叶手术患者的临床管理产生实际影响。机器人辅助立体脑电图技术用于癫痫发作定位，为我们团队提供了同时从人类海马体前部和后部进行记录的机会，使我们能够创建一个无与伦比的数据集，该数据集包含人类受试者同时进行的海马体前部和后部记录以及几个皮质区域。利用这些数据，我们解决了几个关于人类记忆中海马体功能连接的关键问题。首先，我们询问情景记忆编码和检索过程中，海马体前部与后部（PH）的功能网络是否存在显著差异。我们还研究了在2 - 5赫兹与4 - 9赫兹θ频率范围内连接如何不同，直接探讨这些不同频段在海马体 - 皮质相互作用中的相对贡献。虽然我们报告了一些重叠连接，但我们观察到在与额叶和顶叶连接相关的记忆编码过程中，海马体前部与后部网络存在明显差异，以及整体连接中的半球差异。我们根据提出的AT/PM记忆系统来阐述这些发现。我们还观察到海马体前部和后部网络之间编码与检索连接模式不同，我们发现右半球的PH整体连接性更强，并且这些网络在额叶和顶叶连接方面存在显著差异。我们将这些发现置于人类记忆系统现有理论处理的背景下，特别是提出的AT/PM系统。在记忆检索过程中，我们观察到皮质与海马体之间慢θ（2 - 5赫兹）和快θ（4 - 9赫兹）连接存在显著差异。最后，我们使用相位斜率指数来估计编码和检索过程中慢θ和快θ振荡传播的方向，测试这些不同的θ频率振荡如何在海马体内传播。我们发现有证据表明2 - 5赫兹振荡从后向前传播，而5 - 9赫兹振荡从前向后传播。综上所述，我们的发现描述了人类海马体纵轴上与记忆相关的功能连接差异，这将为旨在整合啮齿动物和人类数据的海马体功能模型的解释提供信息。
