Transient impact of spike on theta rhythm in temporal lobe epilepsy

Abstract

Epileptic spike is an indicator of hyper-excitability and hyper-synchrony of neural networks. While cognitive deficit in epilepsy is a common observation, how spikes transiently influence brain oscillations, especially those essential for cognitive functions, remains obscure. Here we aimed to quantify the transient impacts of sporadic spikes on theta oscillations and investigate how such impacts may evolve during epileptogenesis. Longitudinal depth EEG data were recorded in the CA1 area of pilocarpine temporal lobe epilepsy (TLE) rat models. Phase stability, a measure of synchrony, and theta power were estimated around spikes as well as in the protracted spike-free periods (FP) at least 1h after spike bursts. We found that the change in theta power did not correlate with the change in phase stability. More importantly, the impact of spikes on theta rhythm was highly time-dependent. While theta power decreased abruptly after spikes both in the latent and chronic stages, changes of theta phase stability demonstrated opposite trends in the latent and chronic stages, potentially due to the substantial reorganization of neural circuits along epileptogenesis. During FP, theta phase stability was significantly higher than the baseline level before injections, indicating that hyper-synchrony remained even hours after the spike bursts. We concluded that spikes have transient negative effects on theta rhythm, however, impacts are different during latent and chronic stages, implying that its influence on cognitive processes may also change over time during epileptogenesis.