Fluctuations in phase synchronization in brain activity: physiological interpretations of phase locking patterns

Current conceptualisations of brain function implicate synchronization of neuronal activity as an important factor determining brain activity and its relation to behaviour. Many obstacles arise in the assessment of synchrony in neuronal recordings, especially those derived from electroencephalography (EEG) or magnetoencephalography (MEG), as the experimental time series thus obtained are nonstationary, and are characterised by important noise and fluctuations. We studied phase synchronization during generalized epileptiform activity, in attempts to address the apparent "hypersynchrony" seen in visual inspection of EEG/MEG recordings, and to determine possible differences depending upon the specific epileptic syndrome. To this end, we used MEG recordings from epileptic patients with generalized seizures, as well as control subjects, in order to address the extent of phase synchronization (phase locking) in local (neighbouring) and distant cortical areas, and to explore the time scales (frequencies) at which synchrony occurs. All seizures were characterised by enhanced local-although not necessarily stable-synchrony as compared with distant phase locking. 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 there was a constant pattern in the dynamics of synchronization indicating that seizures proceed by a recruitment of neighbouring neuronal networks in the neocortex. Taken together, these data indicate that the concept of widespread "hypersynchronous" activity during generalized seizures may be misleading and valid only for specific neuronal ensembles and circumstances.