Disorganization of language and working memory systems in frontal versus temporal lobe epilepsy.

Disorganization of language and working memory systems in frontal versus temporal lobe epilepsy.
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DOI:
10.1093/brain/awac150
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发表时间:
2023-03-01
期刊:
影响因子:
5.6
通讯作者:
Bernhardt, B. C.
Bernhardt, B. C.
中科院分区:
医学1区
文献类型:
--
作者:
Caciagli, L.;Paquola, C.;He, X.;Vollmar, C.;Centeno, M.;Wandschneider, B.;Braun, U.;Trimmel, K.;Vos, S. B.;Sidhu, M. K.;Thompson, P. J.;Baxendale, S.;Winston, G. P.;Duncan, J. S.;Bassett, D. S.;Koepp, M. J.;Bernhardt, B. C.

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认知障碍是癫痫的常见合并症,对额叶(FLE)和颞叶(TLE)癫痫患者产生不利影响。虽然它的神经底物已被广泛研究在TLE,功能成像研究在FLE是稀缺的。在这项研究中,我们描绘了FLE认知障碍的神经过程,并直接比较了FLE和TLE,以建立共同点和差异。我们调查了172名成年参与者(56名FLE,64名TLE和52名对照),使用神经心理学测试和四项功能性MRI任务探测表达性语言(言语流畅性,动词生成)和工作记忆(言语和视觉空间)。患者组在病程和抗癫痫药物负荷方面具有可比性。我们设计了一个多尺度的方法来映射大脑激活和失活过程中的认知和跟踪重组FLE和TLE。以体素为基础的分析与任务效应的分析相辅相成,这些任务效应跨越了大脑功能组织的既定模式:(i)典型的静息态功能系统;(ii)主要的功能连接梯度,它编码了区域连接轮廓的连续过渡,将较低水平的感觉和跨模态大脑区域锚定在频谱的两端。我们发现,FLE中的认知障碍与注意力和执行系统的激活减少以及默认模式系统的失活减少有关,这表明任务相关招聘的大规模混乱。FLE功能障碍的成像特征与TLE功能障碍的成像特征大致相似,但某些模式具有症状特异性:FLE的默认模式失活改变更为突出,而TLE在语义需求任务期间后部语言区的招募受损更为明显。FLE和TLE的功能异常总体上受到疾病负荷的调节。总的来说,我们的研究阐明了FLE中语言和工作记忆障碍的神经过程,确定了两种最常见的局灶性癫痫中的共享和综合征特异性改变,并揭示了可能适用于未来补救策略的系统行为。Caciagli等人利用功能磁共振成像和网络科学研究额叶癫痫,将注意力和执行区域的激活受损以及默认模式失活受损确定为介导认知障碍的关键神经过程,并捕获额叶癫痫与颞叶癫痫的不同功能特征。
Cognitive impairment is a common comorbidity of epilepsy and adversely impacts people with both frontal lobe (FLE) and temporal lobe (TLE) epilepsy. While its neural substrates have been investigated extensively in TLE, functional imaging studies in FLE are scarce. In this study, we profiled the neural processes underlying cognitive impairment in FLE and directly compared FLE and TLE to establish commonalities and differences. We investigated 172 adult participants (56 with FLE, 64 with TLE and 52 controls) using neuropsychological tests and four functional MRI tasks probing expressive language (verbal fluency, verb generation) and working memory (verbal and visuo-spatial). Patient groups were comparable in disease duration and anti-seizure medication load. We devised a multiscale approach to map brain activation and deactivation during cognition and track reorganization in FLE and TLE. Voxel-based analyses were complemented with profiling of task effects across established motifs of functional brain organization: (i) canonical resting-state functional systems; and (ii) the principal functional connectivity gradient, which encodes a continuous transition of regional connectivity profiles, anchoring lower-level sensory and transmodal brain areas at the opposite ends of a spectrum. We show that cognitive impairment in FLE is associated with reduced activation across attentional and executive systems, as well as reduced deactivation of the default mode system, indicative of a large-scale disorganization of task-related recruitment. The imaging signatures of dysfunction in FLE are broadly similar to those in TLE, but some patterns are syndrome-specific: altered default-mode deactivation is more prominent in FLE, while impaired recruitment of posterior language areas during a task with semantic demands is more marked in TLE. Functional abnormalities in FLE and TLE appear overall modulated by disease load. On balance, our study elucidates neural processes underlying language and working memory impairment in FLE, identifies shared and syndrome-specific alterations in the two most common focal epilepsies and sheds light on system behaviour that may be amenable to future remediation strategies. Studying frontal lobe epilepsy with fMRI and network science, Caciagli et al. identify impaired activation of attentional and executive areas and impaired default-mode deactivation as key neural processes mediating cognitive impairment and capture distinct functional signatures in frontal versus temporal lobe epilepsy.