Glioma-induced neural functional remodeling in the hand motor cortex: precise mapping with ECoG grids during awake craniotomy.

Abstract

Background: The dilemma of achieving 'onco-functional balance' in gliomas affecting the motor cortex highlights the importance of functionally-guided resection strategies. While accurate mapping of eloquent areas often requires frequent electrical stimulation, this practice can lead to side effects like seizures and postoperative deficits. To enhance safety in functional mapping, we studied how gliomas impact hand movement areas and assessed the effectiveness of cortical electrical activity for functional mapping in this setting.

Materials and methods: We recruited patients with gliomas affecting the motor cortex and individuals with an unaffected motor cortex for awake craniotomy. During the procedures, electrocorticography (ECoG) grids were employed to record signals under three conditions: resting state, finger movements, and wrist movements. We then quantified the distances from the positively stimulated sites to the specific anatomical landmarks. Additionally, we analyzed the relationship between the ECoG power features and the stimulation responses.

Results: The cortical layout for finger activity in the motor cortex glioma (MCG) group was more dispersed and overlapped, typically clustering near the central sulcus and Sylvian fissure. The predictive performance of ECoG mapping exhibited significant variability across different frequency bands and clinical scenarios. Specifically, the area under the curve (AUC) for the non-MCG group during the resting state reached its peak, with a value of 0.802 for Gamma3 (95% CI = 0.729-0.875) and 0.865 for broadband (95% CI = 0.804-0.926). In contrast, the MCG group achieved the highest AUC during wrist movements, with Gamma3 at 0.785 (95% CI = 0.719-0.849) and broadband at 0.824 (95% CI = 0.753-0.890).

Conclusion: Gliomas in the motor cortex disrupt the distribution of hand activity, complicating intraoperative functional mapping. As a novel and reliable approach, ECoG technique can complement and guide direct cortical stimulation for precise mapping, potentially reducing its frequency, minimizing the risk of functional deficits, and achieving a balance between maximal tumor resection and neurological preservation.