Epileptic networks in action: Synchrony between distant hemodynamic responses

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Fundamental brain processes such as cognition and motor execution are believed to be established by synchronization of local and distributed neural networks.1 Abnormalities in some neurological diseases, especially epilepsy, are related to altered neuronal synchrony.3 In epilepsy, abnormal local neuronal synchronization causes seizures (ictal events) and interictal epileptic discharges (IEDs),4 but the significance of long‐range synchronization is still a matter of debate.5 IEDs are an important marker of the seizure‐generating region, the epileptogenic zone (EZ), although their extent, the irritative zone, is usually larger than the EZ. Growing evidence, mainly based on structural or functional imaging studies, has demonstrated abnormalities of multiple brain regions that extend beyond the EZ.6 These distributed abnormalities are often interpreted as representing a network, but actual interaction between these regions has not been demonstrated, and it is not obvious that they represent a functioning network.
Simultaneous electroencephalography (EEG)–functional magnetic resonance imaging (fMRI) is a technique that measures noninvasively and with high spatial resolution the changes in hemodynamic activity (the blood oxygen level–dependent [BOLD] responses) across the whole brain during epileptic discharges. This technique aids identification of the EZ9 and has the potential to become a clinical test for presurgical workup.11 EEG‐fMRI analyses in patients with epilepsy often show distributed patterns of BOLD response related to IEDs detected on scalp. They show responses not only in the EZ but also in remote regions, and it is often assumed that this response map represents an epileptic network.13 However, most studies of EEG‐fMRI in epilepsy have concentrated on the maximum BOLD responses, probably because of the complexity of analyzing all responses and because the maximum appears the most important, and have not studied the meaning of distributed responses. Furthermore, the BOLD response is a hemodynamic activity that does not directly represent neuronal activity and its neuronal underpinnings are uncertain. Consequently, little is known about the relationship between neuronal activity in these distributed brain regions and the BOLD response.
We want to understand the neuronal basis of the distributed BOLD responses often seen in EEG‐fMRI studies, and in particular whether the neuronal activities of these regions are synchronized and correspond to an epileptic network in which the nodes interact with each other. We sought to examine the electrophysiological underpinnings of distributed IED‐related BOLD responses during interictal periods using synchrony of IED activity recorded by intracerebral EEG (iEEG) in the regions of the brain showing BOLD responses. Our findings provide insights into the neuronal correlates of hemodynamic‐based imaging of epileptic events, especially the basis of the presumed interictal epileptic networks identified by EEG‐fMRI.

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