Nakajima Riho, Ogawa Akitoshi, Kinoshita Masashi, Osada Takahiro, Okita Hirokazu, Konishi Seiki, Nakada Mitsutoshi
Department of Occupational Therapy, Faculty of Health Science, Institute of Medical, Pharmaceutical and Health Sciences, Kanazawa University, Kanazawa, Japan.
Department of Neurophysiology, Juntendo University School of Medicine, Tokyo, Japan.
Neuroimage Clin. 2025 Aug 6;48:103860. doi: 10.1016/j.nicl.2025.103860.
The frontal language area (FLA; left posterior inferior frontal gyrus [pIFG] or Broca's area), critical for language processing can reorganize in response to lesion progression. While reorganization in the contralateral hemisphere is well known, how reorganization occurs within the ipsilateral hemisphere, especially in the perilesional region, remains unclear. Direct electrical stimulation (DES) during awake surgery enables identification of causal relationships between brain regions and language functions with high spatial resolution. In this study, we investigated cortical reorganization within the ipsilateral hemisphere of the FLA. Seventy-two patients with left hemisphere gliomas were studied. Patients were divided into FLA and non-FLA groups based on whether lesions included the pIFG (n = 10 and n = 62, respectively). All patients underwent DES during a picture-naming task, as recommended by awake surgery guidelines. A subset also underwent resting-state functional MRI (rsfMRI) before surgery to calculate betweenness centrality, an index of network importance of brain areas. DES revealed that the pIFG exhibited positive (impaired) responses to the picture-naming task in both groups. Notably, the frequency of positive responses in the middle frontal gyrus (MFG) was significantly higher in the FLA group than in the non-FLA group. RsfMRI-based network analyses revealed that two areas in the MFG, one in the anterior part and the other in the posterior part, showed higher centrality than surrounding frontal areas in both groups, especially the posterior one. These results suggest that language areas can be observed in the perilesional MFG regions following tumor progression, and raise the possibility that network hubs contribute to maintaining cognitive functions after brain lesions.
额叶语言区(FLA;左后下额叶回[pIFG]或布洛卡区)对语言处理至关重要,可随病变进展而重新组织。虽然对侧半球的重组已为人熟知,但同侧半球内,尤其是病变周围区域的重组如何发生仍不清楚。清醒手术期间的直接电刺激(DES)能够以高空间分辨率识别脑区与语言功能之间的因果关系。在本研究中,我们调查了FLA同侧半球内的皮质重组。对72例左侧半球胶质瘤患者进行了研究。根据病变是否累及pIFG将患者分为FLA组和非FLA组(分别为n = 10和n = 62)。按照清醒手术指南的建议,所有患者在图片命名任务期间接受了DES。一部分患者还在手术前接受了静息态功能磁共振成像(rsfMRI),以计算中介中心性,这是一个衡量脑区网络重要性的指标。DES显示,两组中pIFG对图片命名任务均表现出阳性(受损)反应。值得注意的是,FLA组中额中回(MFG)的阳性反应频率显著高于非FLA组。基于rsfMRI的网络分析显示,MFG中的两个区域,一个在前部,另一个在后部,在两组中均显示出比周围额叶区域更高的中心性,尤其是后部区域。这些结果表明,肿瘤进展后,在病变周围的MFG区域可观察到语言区,并增加了网络枢纽有助于维持脑损伤后认知功能的可能性。