Attenuation of High Gamma Activity by Repetitive Motor Tasks

Abstract

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.