Multiple-brain systems dynamically interact during tonic and phasic states to support language integrity in temporal lobe epilepsy.

Multiple-brain systems dynamically interact during tonic and phasic states to support language integrity in temporal lobe epilepsy.
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DOI:
10.1016/j.nicl.2021.102861
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发表时间:
2021
期刊:
NeuroImage. Clinical
影响因子:
--
通讯作者:
Tracy JI
Tracy JI
中科院分区:
其他
文献类型:
--
作者:
Modi S;He X;Chaudhary K;Hinds W;Crow A;Beloor-Suresh A;Sperling MR;Tracy JI

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左颞叶癫痫(TLE)患者在语言任务中表现出独特的脑动力学特征。多个大脑系统相互作用,以实现TLE中的补偿语言状态。紧张性/静止性动力会产生影响,并可能启动阶段/任务动力的水平。对于语言技能较低的患者,多网络整合是一种补偿。主要颞叶的致痫灶可能会导致语言系统的重组,以补偿受损的功能。我们研究了左颞叶癫痫(TLE)背景下语言的代偿性重组,考虑了语言(L)与关键的非语言网络如背侧注意、额顶叶和扣带盖的相互作用,这些系统为成功的语言操作提供了认知资源。我们将动态网络神经科学的工具应用于23名TLE患者和23名匹配的健康对照在静息状态(RS)和句子补全(SC)任务中收集的功能磁共振数据,以捕捉语言网络的功能结构如何在这两个背景下动态变化并与NL系统相互作用。我们提供的证据表明,核心语言功能所在的大脑区域与非语言功能网络动态互动,以执行语言功能。我们证明在TLE中存在语言和DAN之间的异常整合,并且既存在主音状态,也存在相位状态。这种整合被认为反映了视觉注意系统对致力于词汇语义加工的系统的夹带。我们的数据表明,语言子系统与某些语言系统(如DAN、FPN)之间的基线整合水平对L/NL系统之间的任务整合的总体水平有至关重要的影响,这并不是癫痫所特有的规范性发现。我们还发现,在对外汉语学习中,L/NL整合的一系列任务对语言能力具有预测作用,表明这些整合对整体语言技能较低的患者是补偿的。我们的结论是,RS建立了L/NL整合的广泛集合,并为在任务中使用做好了准备,但这些互动在TLE环境中的实际使用取决于语言技能水平。我们相信,我们的分析首次捕捉到了复杂语言任务执行过程中多个大脑系统之间的动态网络重新配置所起的潜在补偿作用,此外,我们还测试了在颞叶病理环境中实现语言能力所必需的阶段/任务和紧张/休息状态的特征。我们的分析强调了构成TLE独特语言处理基础的系统内和系统间沟通,指出动态的重新配置提供了维持语言技能和能力所需的广泛的多系统支持。
Unique brain dynamics occur during language task in left temporal lobe epilepsy (TLE). Multiple brain systems interact to implement compensated language status in TLE. Tonic/rest dynamics exert influence and may prime the level of phasic/task dynamics. Multi-network integrations are compensatory in patients with lower language skills. An epileptogenic focus in the dominant temporal lobe can result in the reorganization of language systems in order to compensate for compromised functions. We studied the compensatory reorganization of language in the setting of left temporal lobe epilepsy (TLE), taking into account the interaction of language (L) with key non-language (NL) networks such as dorsal attention (DAN), fronto-parietal (FPN) and cingulo-opercular (COpN), with these systems providing cognitive resources helpful for successful language performance. We applied tools from dynamic network neuroscience to functional MRI data collected from 23 TLE patients and 23 matched healthy controls during the resting state (RS) and a sentence completion (SC) task to capture how the functional architecture of a language network dynamically changes and interacts with NL systems in these two contexts. We provided evidence that the brain areas in which core language functions reside dynamically interact with non-language functional networks to carry out linguistic functions. We demonstrated that abnormal integrations between the language and DAN existed in TLE, and were present both in tonic as well as phasic states. This integration was considered to reflect the entrainment of visual attention systems to the systems dedicated to lexical semantic processing. Our data made clear that the level of baseline integrations between the language subsystems and certain NL systems (e.g., DAN, FPN) had a crucial influence on the general level of task integrations between L/NL systems, with this a normative finding not unique to epilepsy. We also revealed that a broad set of task L/NL integrations in TLE are predictive of language competency, indicating that these integrations are compensatory for patients with lower overall language skills. We concluded that RS establishes the broad set of L/NL integrations available and primed for use during task, but that the actual use of those interactions in the setting of TLE depended on the level of language skill. We believe our analyses are the first to capture the potential compensatory role played by dynamic network reconfigurations between multiple brain systems during performance of a complex language task, in addition to testing for characteristics in both the phasic/task and tonic/resting state that are necessary to achieve language competency in the setting of temporal lobe pathology. Our analyses highlighted the intra- versus inter-system communications that form the basis of unique language processing in TLE, pointing to the dynamic reconfigurations that provided the broad multi-system support needed to maintain language skill and competency.
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