Assessing criticality in pre-seizure single-neuron activity of human epileptic cortex

Annika Hagemann, Jens Wilting, Bita Samimizad, Florian Mormann, Viola Priesemann

Abstract: Author summary In epilepsy patients, the brain regularly fails to control its activity, resulting in epileptic seizures. So far, it is not fully understood why the brains of epilepsy patients are susceptible to seizures and what the mechanism behind seizure generation is. We investigated epilepsy from the perspective of collective neural dynamics in the brain. It has been hypothesized that epileptic seizures might be a tipping over from stable, so-called subcritical, dynamics (which are commonly found in healthy brains) to unstable, so-called supercritical dynamics. We therefore examined two potential scenarios of seizure generation: (i) epileptic brain areas might generally operate closer to instability, which would make epilepsy patients generally susceptible to seizures, or (ii) epileptic brain areas might slowly drift towards instability before seizure onset. To test these two hypotheses, we analyzed activity of single neurons recorded with micro-electrodes in epilepsy patients. Contrary to widespread expectation, we found no evidence for either scenario, thus no evidence that epilepsy involves a transition to supercritical collective neural dynamics. In fact, our results from both seizure-free and pre-seizure intervals suggest that the human epileptic brain operates in the stable regime, just like the brains of other healthy mammalians.