Ictal high-frequency oscillations at 80-200 Hz coupled with delta phase in epileptic spasms

Abstract

Previous studies of epileptic spasms reported that ictal events were associated with high-frequency oscillations (HFOs) or delta waves involving widespread regions. We determined whether ictal HFOs at 80-200 Hz were coupled with a phase of slow-wave, whether ictal slow-waves were diffusely or locally synchronous signals, and whether the mode of coupling between HFOs and slow-wave phases differed between ictal and interictal states. We studied 11 children who underwent extraoperative electrocorticography (ECoG) recording. The phases and amplitudes of slow-waves were measured at the peak of ictal and interictal HFOs in the seizure-onset sites. Ictal HFOs were locked tightly to the phase of slow-wave at ≤1 Hz. Ictal slow-waves propagated from the seizure-onset site to other regions. In contrast, interictal HFOs in the seizure-onset site were loosely locked to the phase of slow-wave at ≤1 Hz but tightly to that of ≥3-Hz. Ictal slow-waves coupled with HFOs can be explained as near-field and locally synchronized potentials generated by the neocortex rather than far-field potentials generated by subcortical structures. Ictal slow-waves in epileptic spasms may be generated by a mechanism different from what generates interictal HFOs-slow-wave complexes.

Figure 1

Cross-frequency coupling between ictal HFOs and slow-wave phase in a 2-year and 6-month-old boy with epileptic spasms. (A) Three-dimensional brain surface image shows the location of seizure-onset site (channel 1). (B) ECoG traces show ictal HFOs superimposed on a slow-wave. Both ictal HFOs and slow-waves propagated from the seizure-onset site to the surrounding sites. (C) Time-frequency matrixes demonstrate that augmentation of HFOs occurred at the seizure-onset site earlier than those in the surrounding sites (Nariai et al., 2011). (D) Amplitude augmentation of slow-waves at 1 Hz occurred at the seizure-onset site earlier than those in the surrounding sites. (E) When the amplitude of ictal HFOs reached the peak (i.e., at 0 ms), average slow-wave coherence (at 1 Hz) with the seizure-onset site was high in some surrounding sites (0.74 at channel 2; 0.33 at channel 3) but minimal in other sites (0.07 at channel 4). Epilepsia © ILAE

Figure 2

Difference in cross-frequency coupling between ictal and interictal events. (A) Upper row. Ictal HFOs in the seizure-onset site were tightly coupled with the phase of slow-wave at ≤1 Hz. X-axis: frequency of phase of slow-oscillation. Y-axis: mean z-value on Ray-leigh’s test of nonuniformity with error bars. A larger z-value on Rayleigh’s test indicates a tighter cross-frequency coupling between the peak of HFOs and a given phase of slow-wave. The size of each time-frequency bin was “0.05 Hz and 1,000 ms” for frequencies between 0.1 and 1.0 Hz (graphs on the left side), while being “0.5-Hz and 100-ms” for frequencies between 1 and 10 Hz (graphs on the right side). (B) Lower row. Interictal HFOs in the seizure-onset site were only loosely coupled with the phases of slow-oscillations at ≤1 Hz but tightly coupled with those at ≥3 Hz. Epilepsia © ILAE