Abstract
High gamma (HG, 80-150Hz) activity in macroscopic clinical records is considered a marker for critical brain regions involved in seizure initiation; it is correlated with pathological multiunit firing during neocortical seizures in the seizure core, where multiunit spiking correlates with seizure activity. However, the effects of the seizure’s spatiotemporal dynamics on HG power generation are not well understood. Here, we studied HG generation and propagation, using a three-step, multi-scale signal analysis and modeling approach. First, we analyzed concurrent neuronal and microscopic network HG activity in neocortical slices from seven intractable epilepsy patients. We found HG activity in these networks, especially when neurons displayed paroxysmal depolarization shifts (PDSs) and network activity was highly synchronized. Second, we examined HG activity acquired with microelectrode arrays (MEAs) recorded during human seizures (n=8). We confirmed the presence of synchronized HG power across microelectrode records and the macroscale, both specifically associated with the seizure’s core region. Third, we used volume conduction based modeling to relate HG activity and network synchrony at different network scales. We showed that local HG oscillations require high levels of synchrony to cross scales and that this requirement is met at the microscopic scale, but not within macroscopic networks. Instead, we present evidence that HG power at the macroscale may result from harmonics of ongoing seizure activity. Ictal HG power marks the seizure core, but the generating mechanism can differ across spatial scales.
Significance Statement: We demonstrate that ictal HG power (80-150Hz) in cortical measurements is increased in the seizure core and appears on clinical recordings as a result of volume conduction and synchrony between harmonics generated during ongoing seizure activity. The accuracy of ictal HG activity to localize the core is superior to that of the lower frequency seizure activity since these are generated across much larger cortical areas. Therefore, detection of HG power provides a promising tool for surgical evaluation of patients with epilepsy.
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