Interictal high-frequency oscillations generated by seizure onset and eloquent areas may be differentially coupled
Yutaka Nonoda1, Makoto Miyakoshi2, Alejandro Ojeda2
1Pediatrics, Wayne State University, Children's Hospital of Michigan, Detroit, MI, USA.
Insights
High-frequency oscillations (HFOs) coupled with specific slow-wave frequencies can help differentiate seizure-onset zones from physiological areas in epilepsy patients. This finding aids in improving presurgical evaluations for focal epilepsy.
Area of Science:
- Neuroscience
- Epileptology
- Signal Processing
Background:
- High-frequency oscillations (HFOs) are neural signals that can originate from both seizure-onset zones and functionally important brain regions.
- Distinguishing between epileptogenic and physiological HFOs is crucial for effective presurgical evaluation in focal epilepsy.
Purpose of the Study:
- To investigate whether coupling patterns between HFOs and slow-wave frequencies can differentiate seizure-onset sites from non-epileptogenic brain areas.
- To assess the diagnostic performance of HFO rates and modulation indices (MI) in localizing epileptic foci.
Main Methods:
- A study involving 13 children with focal epilepsy using extraoperative electrocorticography during slow-wave sleep.
- Measurement of HFO rates and modulation indices (MI) reflecting the coupling between HFO amplitude and slow-wave phase.
- Receiver-operating characteristics (ROC) analysis to quantify the predictive accuracy (Area Under the Curve - AUC) of different metrics.
Main Results:
- Increased HFO rates effectively localized seizure-onset sites (AUC ≥ 0.72) but also identified non-epileptogenic sensorimotor-visual sites (AUC ≥ 0.58).
- Modulation index MI(HFOs)&(3-4Hz) showed similar performance in detecting both seizure-onset (AUC ≥ 0.74) and non-epileptogenic sites (AUC ≥ 0.59).
- Subtraction-MIHFOs [MI(HFOs)&(3-4Hz) - MI(HFOs)&(0.5-1Hz)] accurately localized seizure-onset sites (AUC ≥ 0.71) while avoiding non-epileptogenic sites (AUC ≤ 0.42).
Conclusions:
- Epileptogenic HFOs exhibit preferential coupling with 3-4 Hz slow-waves, whereas physiological HFOs show stronger coupling with 0.5-1 Hz slow-waves during sleep.
- The subtraction-MIHFOs metric demonstrates potential for improved presurgical localization by distinguishing epileptic from physiological HFOs.
- Further validation in larger cohorts is needed to confirm the utility of slow-wave coupled HFO analysis in presurgical planning for focal epilepsy.
Objective:
High-frequency oscillations (HFOs) can be spontaneously generated by seizure-onset and functionally-important areas. We determined if consideration of the spectral frequency bands of coupled slow-waves could distinguish between epileptogenic and physiological HFOs.
Methods:
We studied a consecutive series of 13 children with focal epilepsy who underwent extraoperative electrocorticography. We measured the occurrence rate of HFOs during slow-wave sleep at each electrode site. We subsequently determined the performance of HFO rate for localization of seizure-onset sites and undesirable detection of nonepileptic sensorimotor-visual sites defined by neurostimulation. We likewise determined the predictive performance of modulation index: MI(XHz)&(YHz), reflecting the strength of coupling between amplitude of HFOsXHz and phase of slow-waveYHz. The predictive accuracy was quantified using the area under the curve (AUC) on receiver-operating characteristics analysis.
Results:
Increase in HFO rate localized seizure-onset sites (AUC⩾0.72; p<0.001), but also undesirably detected nonepileptic sensorimotor-visual sites (AUC⩾0.58; p<0.001). Increase in MI(HFOs)&(3-4Hz) also detected both seizure-onset (AUC⩾0.74; p<0.001) and nonepileptic sensorimotor-visual sites (AUC⩾0.59; p<0.001). Increase in subtraction-MIHFOs [defined as subtraction of MI(HFOs)&(0.5-1Hz) from MI(HFOs)&(3-4Hz)] localized seizure-onset sites (AUC⩾0.71; p<0.001), but rather avoided detection of nonepileptic sensorimotor-visual sites (AUC⩽0.42; p<0.001).
Conclusion:
Our data suggest that epileptogenic HFOs may be coupled with slow-wave3-4Hz more preferentially than slow-wave0.5-1Hz, whereas physiologic HFOs with slow-wave0.5-1Hz more preferentially than slow-wave3-4Hz during slow-wave sleep.
Significance:
Further studies in larger samples are warranted to determine if consideration of the spectral frequency bands of slow-waves coupled with HFOs can positively contribute to presurgical evaluation of patients with focal epilepsy.
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