The impact of high grade glial neoplasms on human cortical electrophysiology

Abstract

Objective: The brain's functional architecture of interconnected network-related oscillatory patterns in discrete cortical regions has been well established with functional magnetic resonance imaging (fMRI) studies or direct cortical electrophysiology from electrodes placed on the surface of the brain, or electrocorticography (ECoG). These resting state networks exhibit a robust functional architecture that persists through all stages of sleep and under anesthesia. While the stability of these networks provides a fundamental understanding of the organization of the brain, understanding how these regions can be perturbed is also critical in defining the brain's ability to adapt while learning and recovering from injury.

Methods: Patients undergoing an awake craniotomy for resection of a tumor were studied as a unique model of an evolving injury to help define how the cortical physiology and the associated networks were altered by the presence of an invasive brain tumor.

Results: This study demonstrates that there is a distinct pattern of alteration of cortical physiology in the setting of a malignant glioma. These changes lead to a physiologic sequestration and progressive synaptic homogeneity suggesting that a de-learning phenomenon occurs within the tumoral tissue compared to its surroundings.

Significance: These findings provide insight into how the brain accommodates a region of "defunctionalized" cortex. Additionally, these findings may have important implications for emerging techniques in brain mapping using endogenous cortical physiology.

Fig 1. Intraoperative Photograph.

(A) Exposed cortical surface demonstrating gross tumor. (B) Axial MRI slice from same patient identifying left temporo-occipital tumor. (C) Intraoperative ECoG grid on cortical surface for mapping.

Fig 2. Preoperative MR Imaging.

Representative axial slices demonstrating preoperative T2 weighted (upper panel) and contrast enhanced T1 weighted (lower panel) MR imaging demonstrating intracranial neoplasm in each patient.

Fig 3. Power spectra comparing tumor (red) and distant (blue) spectral densities from each individual subject.

Fig 4

A. Bar plot demonstrating comparison between average correlation values between all tumor electrode pairs (red) and all distant electrode pairs (blue). This suggests that connectivity is maintained within cortical regions invaded by glioma. B. Bar histogram demonstrating comparison between distributions of correlation values (detrended for distance) between tumor electrodes (red) and a multiply permuted and resampled subpopulation of distant electrodes (blue) normalized to their respective probability density functions. This accounts for differences in the number of tumor electrodes compared to distant electrodes as well as smaller inter-electrode differences in the tumor electrode subgroup. There was no significant difference between the two groups

Fig 5. Patient specific correlation matrices demonstrating representative correlation maps with seeds placed centrally within each patient’s tumor (left column) and remotely within distant cortex (right column) for each individual subject.