Multiple Oscillatory Push–Pull Antagonisms Constrain Seizure Propagation

Jiang, Haiteng; Cai, Zhengxiang; Worrell, Greg; He, Bin

doi:10.1002/ana.25583

Cited by 26 publications

(30 citation statements)

References 52 publications

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“…Therefore, we speculate that the transient impairment of epileptic tissue presents varying pathophysiological status, leading to different levels of network disruption, thus possibly explaining the distinct presence of coupling between HFOs and spikes within the same epileptic foci. There is also evidence that the alternation of excitation–inhibition balance in the epileptic network has relevance for the development of interictal activities and evolvement into seizures ( 87 , 88 ). Therefore, the concurrent HFOs and spikes might share a mutual underlying pathological relationship and could reciprocally serve as a crucially important signature of epileptic status and therapeutic progress.…”

Section: Discussionmentioning

confidence: 99%

Noninvasive high-frequency oscillations riding spikes delineates epileptogenic sources

Cai

Sohrabpour

Jiang

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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High-frequency oscillations (HFOs) are a promising biomarker for localizing epileptogenic brain and guiding successful neurosurgery. However, the utility and translation of noninvasive HFOs, although highly desirable, is impeded by the difficulty in differentiating pathological HFOs from nonepileptiform high-frequency activities and localizing the epileptic tissue using noninvasive scalp recordings, which are typically contaminated with high noise levels. Here, we show that the consistent concurrence of HFOs with epileptiform spikes (pHFOs) provides a tractable means to identify pathological HFOs automatically, and this in turn demarks an epileptiform spike subgroup with higher epileptic relevance than the other spikes in a cohort of 25 temporal epilepsy patients (including a total of 2,967 interictal spikes and 1,477 HFO events). We found significant morphological distinctions of HFOs and spikes in the presence/absence of this concurrent status. We also demonstrated that the proposed pHFO source imaging enhanced localization of epileptogenic tissue by 162% (∼5.36 mm) for concordance with surgical resection and by 186% (∼12.48 mm) with seizure-onset zone determined by invasive studies, compared to conventional spike imaging, and demonstrated superior congruence with the surgical outcomes. Strikingly, the performance of spike imaging was selectively boosted by the presence of spikes with pHFOs, especially in patients with multitype spikes. Our findings suggest that concurrent HFOs and spikes reciprocally discriminate pathological activities, providing a translational tool for noninvasive presurgical diagnosis and postsurgical evaluation in vulnerable patients.

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Section: Discussionmentioning

confidence: 99%

Noninvasive high-frequency oscillations riding spikes delineates epileptogenic sources

Cai

Sohrabpour

Jiang

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…The posterior DMN is likely associated with states of awareness (9,17,55,59,61). Jing et al reported that a large number of within-and cross-frequency form dynamics was found in secondary generalization of focal seizures (62). It is therefore possible that a cross-frequency coupling (when slow and fast oscillations interact with one another) produces absence seizures.…”

Section: Fc Networkmentioning

confidence: 99%

Differences Between Interictal and Ictal Generalized Spike-Wave Discharges in Childhood Absence Epilepsy: A MEG Study

et al. 2020

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Purpose: To investigate the differences between interictal and ictal generalized spike-wave discharges (GSWDs) for insights on how epileptic activity propagates and the physiopathological mechanisms underlying childhood absence epilepsy (CAE). Methods: Twenty-five patients with CAE were studied using magnetoencephalography (MEG). MEG data were digitized at 6,000 Hz during the interictal and ictal GSWDs. GSWDs were analyzed at both neural magnetic source levels and functional connectivity (FC) in multifrequency bands: delta (1-4 Hz), theta (4-8 Hz), alpha (8-12 Hz), beta (12-30 Hz), gamma (30-80 Hz), ripple (80-250 Hz), and fast ripple (250-500 Hz). Brain FC was studied with the posterior cingulate cortex/precuneus (PCC/pC) as the seed region. Results: The magnetic source of interictal GSWDs mainly locates in the PCC/pC region at 4-8 and 8-12 Hz, while that of ictal GSWDs mainly locates in the medial frontal cortex (MFC) at 80-250 Hz. There were statistically significant differences between interictal and ictal GSWDs (p < 0.05). The FC network involving the PCC/pC showed strong connections in the anterior-posterior pathways (mainly with the frontal cortex) at 80-250 Hz during ictal GSWDs, while the interictal GSWDs FC were mostly limited to the posterior cortex region. There was no significant difference in the magnetic source strength among interictal and ictal GSWDs at all bandwidths. Conclusions: There are significant disparities in the source localization and FC between interictal and ictal GSWDs. Low-frequency activation in the PCC/pC during inhibition of seizures possibly relates to the maintenance of consciousness during interictal GSWDs. High-frequency oscillations (HFOs) of the MFC during CAE may associate with the inducing or occurrence of GSWDs. Weakened network connections may be in favor of preventing overexcitability and relates to the termination of GSWDs.

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“…Other network measures mostly focus on exploring the causality of electrophysiological oscillations within specific frequency, so the higher and lower frequency activities are analyzed independently. Those measures ignore the interactions between high-frequency and low-frequency networks, which is an essential feature when modeling some pathological or physiological process [23], [37], [38]. The proposed N CFC provides a chance for analyzing the interactions of higher and lower frequency epileptic networks in a unified framework to determine the role that HF or LF sub-networks play in ictal generation and propagation.…”

Section: A N Cfc Propertiesmentioning

confidence: 99%

High-Frequency Hubs of the Ictal Cross-Frequency Coupling Network Predict Surgical Outcome in Epilepsy Patients

Sohrabpour

Jiang

et al. 2021

IEEE Trans. Neural Syst. Rehabil. Eng.

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Seizure generation is thought to be a process driven by epileptogenic networks; thus, network analysis tools can help determine the efficacy of epilepsy treatment. Studies have suggested that low-frequency (LF) to high-frequency (HF) cross-frequency coupling (CFC) is a useful biomarker for localizing epileptogenic tissues. However, it remains unclear whether the LF or HF coordinated CFC network hubs are more critical in determining the treatment outcome. We hypothesize that HF hubs are primarily responsible for seizure dynamics. Stereoelectroencephalography (SEEG) recordings of 36 seizures from 16 intractable epilepsy patients were analyzed. We propose a new approach to model the temporal-spatialspectral dynamics of CFC networks. Graph measures are then used to characterize the HF and LF hubs. In the patient group with Engel Class (EC) I outcome, the strength of HF hubs was significantly higher inside the resected regions during the early and middle stages of seizure, while such a significant difference was not observed in the EC III group and only for the early stage in the EC II group. For the LF hubs, a significant difference was identified at the late stage and only in the EC I group. Our findings suggest that HF hubs increase at early and middle stages of the ictal interval while LF hubs increase activity at the late stages. In addition, HF hubs can predict treatment outcomes more precisely, compared to the LF hubs of the CFC network. The proposed method promises to identify more accurate targets for surgical interventions or neuromodulation therapies.

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Multiple Oscillatory Push–Pull Antagonisms Constrain Seizure Propagation

Abstract: View this article online at wileyonlinelibrary.com.

Cited by 26 publications

References 52 publications

Noninvasive high-frequency oscillations riding spikes delineates epileptogenic sources

Noninvasive high-frequency oscillations riding spikes delineates epileptogenic sources

Differences Between Interictal and Ictal Generalized Spike-Wave Discharges in Childhood Absence Epilepsy: A MEG Study

High-Frequency Hubs of the Ictal Cross-Frequency Coupling Network Predict Surgical Outcome in Epilepsy Patients

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