Sleep increases broadband fast oscillations in the epileptic focus of patients with focal cortical dysplasia

Rationale

Focal cortical dysplasia (FCD) is associated with increased seizure-risk during sleep, yet the underlying mechanisms remain unclear. Previous studies report increased oscillatory patterns during sleep in focal epilepsy patients with FCD. We investigated whether fast oscillations (FOs, 14-250 Hz) within the epileptic focus significantly change during sleep compared to wake, hypothesizing that analyzing broad frequency bands provides more comprehensive information than narrow bands alone.

Methods

We retrospectively analyzed intracranial EEG recordings from 22 FCD patients (2010-2023), focusing on contacts within the irritative zone (IZ) and seizure onset zone (SOZ). Using semiautomated detections, we compared FO rates between one-hour wake and sleep epochs across beta (14-40 Hz), gamma (40-80 Hz), and ripple (80-250 Hz) bands. Distance-based Multivariate Analysis of Variance (MANOVA) was applied to integrate the spatial organization of FO changes, enabling simultaneous analysis of individual and combined broadband ranges (BGR) while accounting for neocortical detection rates outside the epileptic focus and eloquent cortex.

Results

Analysis of 67 ± 28 (median ± standard deviation) bipolar iEEG contact pairs per patient (SOZ: 14 ± 12, IZ: 29 ± 16) revealed distinct sleep-related patterns. In the SOZ, gamma showed significant increases in 10 patients, followed by BGR in seven patients. The IZ exhibited strong changes in both BGR and gamma (13 patients each) with high concordance (12 matches). Beta and ripple bands showed moderate concordance. Notably, gamma oscillation rates in the SOZ specifically increased in patients with sleep-related epilepsy (p < 0.05).

Conclusion

Gamma oscillations showed the most robust sleep-related increases in the SOZ, while both gamma and BGR showed strong changes in the IZ. These findings suggest gamma oscillations, complemented by broadband analysis, may serve as reliable markers for sleep-related changes in FCD patients.

Funding

YLH (LI1904/2-1) and MH (HE6844/3-1; project ID for both: 468174690) were funded by the German Research Foundation (DFG)

Key points

• Within the seizure onset zone, gamma band oscillations (40-80 Hz) followed by combined broadband BGR (14-250 Hz) show more frequent significant increases from wake to sleep across patients

• Within the irritative zone, gamma band and broadband oscillations BRG show even more frequent increases from wake to sleep across patients

• Changes occur simultaneously across multiple frequency bands, supporting the value of multi-band analysis

• Gamma oscillation rates within the seizure onset zone significantly increased from wake to sleep in patients with sleep-related epilepsy (p < 0.05)