Numerical Simulation of Concussive-generated Cortical Spreading Depolarization to Optimize DC-EEG Electrode Spacing for Non-invasive Visual Detection

Abstract

Background: Cortical Spreading Depolarization (SD) is a propagating depolarization wave of neurons and glial cells in the cerebral gray matter. SD occurs in all forms of severe acute brain injury as documented using invasive detection methods. Based on many experimental studies of mechanical brain deformation and concussion, the occurrence of SDs in human concussion has often been hypothesized. However, this hypothesis cannot be confirmed in humans as SDs can only be detected with invasive detection methods that would require either a craniotomy or a burr hole to be performed on athletes. Typical electroencephalography (EEG) electrodes, placed on the scalp, can detect the possible presence of SD but have not been able to accurately and reliably identify SDs. Methods: To explore the possibility of a non-invasive method to resolve this hurdle, we developed a finite element numerical model that simulates scalp voltage changes that are induced by a brain-surface SD. We then compared our simulation results with retrospectively evaluated data in aneurysmal subarachnoid hemorrhage (aSAH) patients from Drenckhahn et al. (Brain 135:853, 2012). Results: The ratio of peak scalp to simulated peak cortical voltage, Vscalp/Vcortex, was 0.0735, whereas the ratio from the retrospectively evaluated data was 0.0316 (0.0221, 0.0527) [median (1st quartile, 3rd quartile), n = 161, p < 0.001, one sample Wilcoxon signed rank test]. This difference can be attributed to differences in shape between concussive- and aSAH-SDs, as well as the inherent limitations in human study voltage measurements. This simulated scalp surface potential was used to design a virtual scalp detection array. Error analysis and visual reconstruction showed that 1 cm is the optimal electrode spacing to visually identify and track the propagating scalp voltage from a cortical SD. Electrode spacing greater than 1.5 cm produces distorted images and unacceptable errors in velocity and dimensions. Conclusion: Our analysis suggests that concussive (and other) SDs can be detected from the scalp, which could confirm SD occurrence in human concussion, provide concussion diagnosis based on an underlying physiological mechanism, and lead to non-invasive SD detection in the setting of severe acute brain injury.