Spatiotemporal patterns of electrocorticographic very fast oscillations (>80 Hz) consistent with a network model based on electrical coupling between principal neurons

Abstract

Purpose: We sought to characterize spatial and temporal patterns of electrocorticography (ECoG) very fast oscillations (> ∼80 Hz, VFOs) prior to seizures in human frontotemporal neocortex, and to develop a testable network model of these patterns. Methods: ECoG data were recorded with subdural grids from two preoperative patients with seizures of frontal lobe onset in an epilepsy monitoring unit. VFOs were recorded from rat neocortical slices. A "cellular automaton" model of network oscillations was developed, extending ideas of Traub et al. (Neuroscience, 92, 1999, 407) and Lewis & Rinzel (Network: Comput Neural Syst, 11, 2000, 299); this model is based on postulated electrical coupling between pyramidal cell axons. Results: Layer 5 of rat neocortex, in vitro, can generate VFOs when chemical synapses are blocked. Human epileptic neocortex, in situ, produces preseizure VFOs characterized by the sudden appearance of "blobs" of activity that evolve into spreading wavefronts. When wavefronts meet, they coalesce and propagate perpendicularly but never pass through each other. This type of pattern has been described by Lewis & Rinzel in cellular automaton models with spatially localized connectivity, and is demonstrated here with 120,000- to 5,760,000-cell models. We provide a formula for estimating VFO period from structural parameters and estimate the spatial scale of the connectivity. Discussion: These data provide further evidence, albeit indirect, that preseizure VFOs are generated by networks of pyramidal neurons coupled by gap junctions, each predominantly confined to pairs of neurons having somata separated by < ∼1-2 mm. Plausible antiepileptic targets are tissue mechanisms, such as pH regulation, that influence gap-junction conductance. © 2009 International League Against Epilepsy.