From baseline to epileptiform activity: A path to synchronized rhythmicity in large-scale neural networks

Abstract

In large-scale neural networks in the brain the emergence of global behavioral patterns, manifested by electroencephalographic activity, is driven by the self-organization of local neuronal groups into synchronously functioning ensembles. However, the laws governing such macrobehavior and its disturbances, in particular epileptic seizures, are poorly understood. Here we use a mean-field population network model to describe a state of baseline physiological activity and the transition from the baseline state to rhythmic epileptiform activity. We describe principles which explain how this rhythmic activity arises in the form of spatially uniform self-sustained synchronous oscillations. In addition, we show how the rate of migration of the leading edge of the synchronous oscillations can be theoretically predicted, and compare the accuracy of this prediction with that measured experimentally using multichannel electrocorticographic recordings obtained from a human subject experiencing epileptic seizures. The comparison shows that the experimentally measured rate of migration of the leading edge of synchronous oscillations is within the theoretically predicted range of values. Computer simulations have been performed to investigate the interactions between different regions of the brain and to show how organization in one spatial region can promote or inhibit organization in another. Our theoretical predictions are also consistent with the results of functional magnetic resonance imaging (fMRI), in particular with observations that lower-frequency electroencephalographic (EEG) rhythms entrain larger areas of the brain than higher-frequency rhythms. These findings advance the understanding of functional behavior of interconnected populations and might have implications for the analysis of diverse classes of networks.