Abstract
It is increasingly recognized that deep understanding of epileptic seizures requires both localizing and characterizing the functional network of the region where they are initiated, i. e., the epileptic focus. Previous investigations of the epileptogenic focus' functional connectivity have yielded contrasting results, reporting both pathological increases and decreases during resting periods and seizures. In this study, we shifted paradigm to investigate the time course of connectivity in relation to interictal epileptiform discharges. We recruited 35 epileptic patients undergoing intracranial EEG (iEEG) investigation as part of their presurgical evaluation. For each patient, 50 interictal epileptic discharges (IEDs) were marked and iEEG signals were epoched around those markers. Signals were narrow-band filtered and time resolved phase-locking values were computed to track the dynamics of functional connectivity during IEDs. Results show that IEDs are associated with a transient decrease in global functional connectivity, time-locked to the peak of the discharge and specific to the high range of the gamma frequency band. Disruption of the long-range connectivity between the epileptic focus and other brain areas might be an important process for the generation of epileptic activity. Transient desynchronization could be a potential biomarker of the epileptogenic focus since 1) the functional connectivity involving the focus decreases significantly more than the connectivity outside the focus and 2) patients with good surgical outcome appear to have a significantly more disconnected focus than patients with bad outcomes.
Highlights
Networks at WorkIt has long been recognized that most anatomical subdivisions of the brain exhibit some degree of functional specialization [1, 2], and localization of the neural substrate of brain function has constituted the workhorse of neuroscientists for decades
Low frequency bands (θ, α, β) display an increase in phase-locking value (PLV)-based synchrony time-locked to the appearance of the interictal epileptiform discharges (IEDs) while high frequency bands display a decrease in PLV-based synchrony
We found that IED-locked high-frequency PLV-based synchrony was significantly lower in patients with good than in patients with bad outcome (p = 0.023, corrected) while no difference was found for low-frequency PLV-based synchrony (p = 0.59, uncorrected)
Summary
Networks at WorkIt has long been recognized that most anatomical subdivisions of the brain exhibit some degree of functional specialization [1, 2], and localization of the neural substrate of brain function has constituted the workhorse of neuroscientists for decades. As was originally postulated by Spencer, seizures arise when an epileptic focus disrupts the balance of functional connectivity within a network, thereby driving its constituting regions into aberrant discharges [6] This theoretical framework is supported empirically by a number of studies showing permanent alterations in brain connectivity in epilepsy. Abnormal increases in functional connectivity seem to be closely associated with evolution of the disease [10] and local hypersynchrony/ hyposynchrony were found to be potential electrophysiological/hemodynamic biomarkers for localizing the epileptic focus [11,12,13,14,15] This clinical perspective was further investigated during epileptiform discharges [16] and seizures [17,18,19], during which regions with elevated connectivity spatially overlapped with the clinically defined epileptic focus. At least three possible explanations could explain these discrepancies: [1] the definition of the electrical onset of seizures can vary among epileptologists; [2] the changes in connectivity that culminate in seizures might begin before visually identified electrical onset, and [3] different frequency bands could act as distinct information transfer channels during seizures, which has been seldom investigated
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