Declarative memory encompasses episodic and semantic divisions. Episodic memory captures singular events with specific spatiotemporal relationships, whereas semantic memory houses context-independent knowledge. Behavioural and functional neuroimaging studies have revealed common and distinct neural substrates of both memory systems, implicating mesiotemporal lobe (MTL) regions such as the hippocampus and distributed neocortices. Here, we explored declarative memory system reorganization in patients with unilateral temporal lobe epilepsy (TLE) as a human disease model to test the impact of variable degrees of MTL pathology on memory function. Our cohort included 31 patients with TLE and 60 age- and sex-matched healthy controls, and all participants underwent episodic and semantic retrieval tasks during a multimodal MRI session. The functional MRI tasks were closely matched in terms of stimuli and trial design. Capitalizing on non-linear connectome gradient-mapping techniques, we derived task-based functional topographies during episodic and semantic memory states, in both the MTL and neocortical networks. Comparing neocortical and hippocampal functional gradients between TLE patients and healthy controls, we observed a marked topographic reorganization of both neocortical and MTL systems during episodic memory states. Neocortical alterations were characterized by reduced functional differentiation in TLE across lateral temporal and midline parietal cortices in both hemispheres. In the MTL, in contrast, patients presented with a more marked functional differentiation of posterior and anterior hippocampal segments ipsilateral to the seizure focus and pathological core, indicating perturbed intrahippocampal connectivity. Semantic memory reorganization was also found in bilateral lateral temporal and ipsilateral angular regions, whereas hippocampal functional topographies were unaffected. Furthermore, leveraging MRI proxies of MTL pathology, we observed alterations in hippocampal microstructure and morphology that were associated with TLE-related functional reorganization during episodic memory. Moreover, correlation analysis and statistical mediation models revealed that these functional alterations contributed to behavioural deficits in episodic memory, but again not in semantic memory in patients. Altogether, our findings suggest that semantic processes rely on distributed neocortical networks, whereas episodic processes are supported by a network involving both the hippocampus and the neocortex. Alterations of such networks can provide a compact signature of state-dependent reorganization in conditions associated with MTL damage, such as TLE.

中文翻译：

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癫痫相关近颞叶病理中情景记忆系统和语义记忆系统的差异重组


陈述性记忆包括情景和语义划分。情景记忆捕捉具有特定时空关系的单一事件，而语义记忆则包含独立于上下文的知识。行为和功能神经影像学研究揭示了两种记忆系统共同和不同的神经基质，涉及近颞叶 （MTL） 区域，例如海马体和分布的新皮层。在这里，我们探讨了单侧颞叶癫痫 （TLE） 患者的陈述性记忆系统重组作为人类疾病模型，以测试不同程度的 MTL 病理对记忆功能的影响。我们的队列包括 31 名 TLE 患者和 60 名年龄和性别匹配的健康对照者，所有参与者在多模态 MRI 会议期间都接受了情景和语义检索任务。功能性 MRI 任务在刺激和试验设计方面密切相关。利用非线性连接组梯度映射技术，我们在 MTL 和新皮层网络中衍生了情景和语义记忆状态下基于任务的功能拓扑图。比较 TLE 患者和健康对照者的新皮层和海马功能梯度，我们观察到情景记忆状态下新皮层和 MTL 系统都有明显的地形重组。新皮层改变的特征是两个半球外侧颞叶和中线顶叶皮层的 TLE 功能分化减少。相比之下，在 MTL 中，患者在癫痫病灶和病理核心同侧的后、前节段功能分化更明显，表明海马内连接性受干扰。 在双侧外侧颞区和同侧角区也发现了语义记忆重组，而海马功能地形不受影响。此外，利用 MTL 病理学的 MRI 代理，我们观察到海马微观结构和形态的变化，这些变化与情景记忆期间 TLE 相关的功能重组有关。此外，相关性分析和统计中介模型显示，这些功能改变导致了情景记忆的行为缺陷，但同样不是患者语义记忆的行为缺陷。总而言之，我们的研究结果表明，语义过程依赖于分布式新皮层网络，而情景过程则由涉及海马体和新皮层的网络支持。这种网络的改变可以在与 MTL 损伤相关的条件下提供状态依赖性重组的紧凑特征，例如 TLE。