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The Journal of Neuroscience, August 31, 2005, 25(35):8077-8084; doi:10.1523/JNEUROSCI.1046-05.2005

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Neurobiology of Disease
Enhanced Synchrony in Epileptiform Activity? Local versus Distant Phase Synchronization in Generalized Seizures

Luis Garcia Dominguez,,¹ Richard A. Wennberg,³ William Gaetz,² Douglas Cheyne,² O. Carter Snead, III,¹ and Jose Luis Perez Velazquez¹

¹Brain and Behaviour Program and Division of Neurology, and ²Neuromagnetic Imaging Laboratory, The Hospital for Sick Children, Toronto, Ontario, Canada M5G 1X8, and ³Krembil Neuroscience Centre, Toronto Western Hospital, Department of Paediatrics and Institute of Medical Science, University of Toronto, Toronto, Ontario, Canada M5T 2S8

Synchronization is a fundamental characteristic of complex systems and a basic mechanism of self-organization. A traditional, accepted perspective on epileptiform activity holds that hypersynchrony covering large brain regions is a hallmark of generalized seizures. However, a few recent reports have described substantial fluctuations in synchrony before and during ictal events, thus raising questions as to the widespread synchronization notion. In this study, we used magnetoencephalographic recordings from epileptic patients with generalized seizures and normal control subjects to address the extent of the phase synchronization (phase locking) in local (neighboring) and distant cortical areas and to explore the ongoing temporal dynamics for particular ranges of frequencies at which synchrony occurs, during interictal and ictal activity. Synchronization patterns were found to differ somewhat depending on the epileptic syndrome, with primary generalized absence seizures displaying more long-range synchrony in all frequency bands studied (3–55 Hz) than generalized tonic motor seizures of secondary (symptomatic) generalized epilepsy or frontal lobe epilepsy. However, all seizures were characterized by enhanced local synchrony compared with distant synchrony. There were fluctuations in the synchrony between specific cortical areas that varied from seizure to seizure in the same patient, but in most of the seizures studied, regardless of semiology, there was a constant pattern in the dynamics of synchronization, indicating that seizures proceed by a recruitment of neighboring neuronal networks. Together, these data indicate that the concept of widespread "hypersynchronous" activity during generalized seizures may be misleading and valid only for very specific neuronal ensembles and circumstances.

Key words: synchrony; phase locking; epilepsy; neocortex; magnetoencephalography; seizures

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Received March 17, 2005; revised July 20, 2005; accepted July 22, 2005.

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