Sanada Takahiro, Kapeller Christoph, Jordan Michael, Miyauchi Masaharu, Fukuyama Shusei, Kimura Teruo, Hiroshima Satoru, Kinoshita Manabu, Nakano Naoki, Guger Christoph, Tsuyuguchi Naohiro
Department of Neurosurgery, Asahikawa Medical University, Asahikawa, Japan.
Department of Neurosurgery, Japanese Red Cross Kitami Hospital, Kitami, Japan.
Hum Brain Mapp. 2025 Feb 1;46(2):e70153. doi: 10.1002/hbm.70153.
High gamma activity (HGA) is a crucial biomarker for functional brain mapping, particularly in sensorimotor areas, to preserve functionality after brain surgeries. HGA mapping paradigms typically involve multiple task blocks alternating with resting (R) conditions, where each block comprises consecutive tasks under nonresting (NR) conditions. However, the repetitive nature of these tasks may lead to attenuation due to repetition suppression, potentially compromising the accuracy of HGA mapping. This study tests the hypothesis that repetitive grasping paradigms result in attenuated HGA over time in sensorimotor areas. It explores the temporal and spatial characteristics of this attenuation to optimize electrocorticography (ECoG) HGA protocols and enhance result interpretation. Eleven consecutive patients who underwent surgical treatment of intractable epilepsy or malignant glioma were included in this study. Intracranial electrode locations on the pre- and postcentral gyrus were considered regions of interest (ROI). Each patient performed ten blocks of ten consecutive grasping trials. The mean z-scored HGA (60-170 Hz) across these trials was calculated, and attenuation was analyzed using the Kruskal-Wallis test. Obtained signals were also divided into three grouped periods for R and NR groups to assess short-term attenuation within movement blocks and long-term attenuation over multiple blocks. Electrode locations were mapped to the MNI152 (Montreal Neurological Institute) brain template to investigate the spatial distribution of attenuation. Distances from each electrode to the hand-knob region were compared between attenuated and nonattenuated electrodes. A total of 568 electrodes from 11 patients were analyzed, including 139 electrodes within the ROI. Thus, 60 electrodes demonstrated significant HGAs during the grasping task (p < 0.05). Sensorimotor HGA z-scores significantly attenuated over time during both consecutive grasping trials and repeated blocks. Short-term attenuation (25%, 15/60 electrodes in ROI) was more pronounced than long-term attenuation (15%, 9/60 electrodes in ROI). Notably, three patients undergoing intraoperative mapping demonstrated less short-term attenuation compared to long-term attenuation. Spatially, attenuated electrodes clustered around the hand-knob region of the precentral gyrus and adjacent areas of the postcentral gyrus. However, no significant differences were observed in the distances from electrodes to the hand-knob region between attenuated and nonattenuated electrodes. The present study showed that repetitive grasping tasks attenuated the HGA of significant electrodes in the sensorimotor area over time. Considering the findings with the characteristics can further improve the usability of ECoG mapping in terms of more precise results in the most reasonable mapping time.
高伽马活动(HGA)是功能性脑图谱的关键生物标志物,尤其在感觉运动区域,对于脑手术后保留功能至关重要。HGA图谱范式通常涉及多个任务块与静息(R)状态交替,其中每个块包含非静息(NR)状态下的连续任务。然而,这些任务的重复性可能导致由于重复抑制而衰减,这可能会损害HGA图谱的准确性。本研究检验了这样一个假设,即重复抓握范式会导致感觉运动区域随时间推移HGA衰减。它探索了这种衰减的时间和空间特征,以优化皮质脑电图(ECoG)HGA方案并增强结果解释。本研究纳入了11例连续接受难治性癫痫或恶性胶质瘤手术治疗的患者。中央前回和中央后回上的颅内电极位置被视为感兴趣区域(ROI)。每位患者进行10个块,每个块包含10次连续抓握试验。计算这些试验中平均z评分的HGA(60 - 170 Hz),并使用Kruskal - Wallis检验分析衰减情况。获得的信号还被分为R组和NR组的三个分组时间段,以评估运动块内的短期衰减和多个块上的长期衰减。将电极位置映射到MNI152(蒙特利尔神经病学研究所)脑模板上,以研究衰减的空间分布。比较衰减电极和未衰减电极到手部旋钮区域的距离。共分析了11例患者的568个电极,其中包括ROI内的139个电极。因此,60个电极在抓握任务期间显示出显著的HGA(p < 0.05)。在连续抓握试验和重复块期间,感觉运动HGA z评分随时间显著衰减。短期衰减(25%,ROI内60个电极中的15个)比长期衰减(15%,ROI内60个电极中的9个)更明显。值得注意的是,3例接受术中图谱绘制的患者短期衰减比长期衰减少。在空间上,衰减电极聚集在中央前回的手部旋钮区域和中央后回的相邻区域周围。然而,衰减电极和未衰减电极到手部旋钮区域的距离没有观察到显著差异。本研究表明,重复抓握任务会使感觉运动区域中显著电极的HGA随时间衰减。考虑到这些具有特征性的发现,可以在最合理的图谱绘制时间获得更精确的结果,从而进一步提高ECoG图谱的可用性。