More widespread functionality of posterior language area in patients with brain tumors

IF 3.5 2区 医学 Q1 NEUROIMAGING Human Brain Mapping Pub Date : 2024-08-01 DOI:10.1002/hbm.26801
Riho Nakajima, Takahiro Osada, Masashi Kinoshita, Akitoshi Ogawa, Hirokazu Okita, Seiki Konishi, Mitsutoshi Nakada
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Abstract

Damage to the posterior language area (PLA), or Wernicke's area causes cortical reorganization in the corresponding regions of the contralateral hemisphere. However, the details of reorganization within the ipsilateral hemisphere are not fully understood. In this context, direct electrical stimulation during awake surgery can provide valuable opportunities to investigate neuromodulation of the human brain in vivo, which is difficult through the non-invasive approaches. Thus, in this study, we aimed to investigate the characteristics of the cortical reorganization of the PLA within the ipsilateral hemisphere. Sixty-two patients with left hemispheric gliomas were divided into groups depending on whether the lesion extended to the PLA. All patients underwent direct cortical stimulation with a picture-naming task. We further performed functional connectivity analyses using resting-state functional magnetic resonance imaging (MRI) in a subset of patients and calculated betweenness centrality, an index of the network importance of brain areas. During direct cortical stimulation, the regions showing positive (impaired) responses in the non-PLA group were localized mainly in the posterior superior temporal gyrus (pSTG), whereas those in the PLA group were widely distributed from the pSTG to the posterior supramarginal gyrus (pSMG). Notably, the percentage of positive responses in the pSMG was significantly higher in the PLA group (47%) than in the non-PLA group (8%). In network analyses of functional connectivity, the pSMG was identified as a hub region with high betweenness centrality in both the groups. These findings suggest that the language area can spread beyond the PLA to the pSMG, a hub region, in patients with lesion progression to the pSTG. The change in the pattern of the language area may be a compensatory mechanism to maintain efficient brain networks.

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脑肿瘤患者的后语言区功能更加广泛。
后语言区(PLA)或韦尼克区受损会导致对侧半球相应区域的皮质重组。然而,同侧大脑半球内重组的细节还不完全清楚。在这种情况下,清醒手术过程中的直接电刺激可以为研究人脑的体内神经调控提供宝贵的机会,而这是非侵入性方法难以实现的。因此,在本研究中,我们旨在研究同侧大脑半球内 PLA 皮层重组的特征。根据病变是否扩展到解放区,我们将62名左侧大脑半球胶质瘤患者分为几组。所有患者都接受了图片命名任务的直接皮层刺激。我们还利用静息态功能磁共振成像(MRI)对部分患者进行了功能连通性分析,并计算了脑区网络重要性指数--"间度中心性"(betweenness centrality)。在直接刺激皮层时,非 PLA 组出现阳性(受损)反应的区域主要集中在后颞上回(pSTG),而 PLA 组则广泛分布在从后颞上回到后边际上回(pSMG)的各个区域。值得注意的是,PLA 组在 pSMG 中的阳性反应百分比(47%)明显高于非 PLA 组(8%)。在功能连通性网络分析中,pSMG 在两组中均被确定为具有高间度中心性的枢纽区域。这些研究结果表明,在病变进展到 pSTG 的患者中,语言区可以超越 PLA 扩散到 pSMG 这一枢纽区域。语言区模式的改变可能是一种维持高效大脑网络的补偿机制。
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来源期刊
Human Brain Mapping
Human Brain Mapping 医学-核医学
CiteScore
8.30
自引率
6.20%
发文量
401
审稿时长
3-6 weeks
期刊介绍: Human Brain Mapping publishes peer-reviewed basic, clinical, technical, and theoretical research in the interdisciplinary and rapidly expanding field of human brain mapping. The journal features research derived from non-invasive brain imaging modalities used to explore the spatial and temporal organization of the neural systems supporting human behavior. Imaging modalities of interest include positron emission tomography, event-related potentials, electro-and magnetoencephalography, magnetic resonance imaging, and single-photon emission tomography. Brain mapping research in both normal and clinical populations is encouraged. Article formats include Research Articles, Review Articles, Clinical Case Studies, and Technique, as well as Technological Developments, Theoretical Articles, and Synthetic Reviews. Technical advances, such as novel brain imaging methods, analyses for detecting or localizing neural activity, synergistic uses of multiple imaging modalities, and strategies for the design of behavioral paradigms and neural-systems modeling are of particular interest. The journal endorses the propagation of methodological standards and encourages database development in the field of human brain mapping.
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