A semiological marker of emotional insulo-cingulate network activation in epileptic human brain

There are limited reports on the "chapeau de gendarme" (CDG) sign, which is considered reliable evidence for the verification of frontal epilepsy. However, several recent reports of scattered cases of extra-frontal epilepsy suggest the complexity of the cortical networks underlying CDG generation. The present study aimed to investigate the anatomo-electro-clinical correlations and explore the cortical mechanisms of the generation of CDG via video-stereoelectroencephalography (SEEG). Patients with focal epilepsy who underwent SEEG and epilepsy surgery in our center from March 2017 to December 2019 were retrospectively reviewed. Ten patients with epilepsy with habitual seizures presenting with CDG were included. Most CDG signs were discerned visually into two chronological components referred to as the "prodromal component" and the "major component." The CDG signs occurred at 2.4-26.1 s after electrical onset and lasted for 2.2-16.6 s. The two sequential components were visually discerned in 64 included seizures of the six patients. The epileptogenic zones were diverse in distribution. Cluster analysis was performed based on the neurophysiological features of distinct cortical areas, and the agranulo-dysgranular insular and cingulate cortices were emphasized. Pearson correlation and linear regression showed a linear relationship between the latencies of CDG onset and the latencies of co-activation of agranulo-dysgranular cingulate and insular cortex in gamma bands. Our results suggest that (1) the CDG sign should be interpreted as a type of facial behavior with social-emotional features and considered a semiological marker of emotional insulo-cingulate cortex involvement in focal epilepsy, and (2) epileptic discharges arising directly from or propagating indirectly into this anterior limbic network have a high likelihood of evoking the CDG sign.