Dataset Information

Seizure epicenter depth and translaminar field potential synchrony underlie complex variations in tissue oxygenation during ictal initiation.

ABSTRACT: Whether functional hyperemia during epileptic activity is adequate to meet the heightened metabolic demand of such events is controversial. Whereas some studies have demonstrated hyperoxia during ictal onsets, other work has reported transient hypoxic episodes that are spatially dependent on local surface microvasculature. Crucially, how laminar differences in ictal evolution can affect subsequent cerebrovascular responses has not been thus far investigated, and is likely significant in view of possible laminar-dependent neurovascular mechanisms and angioarchitecture. We addressed this open question using a novel multi-modal methodology enabling concurrent measurement of cortical tissue oxygenation, blood flow and hemoglobin concentration, alongside laminar recordings of neural activity, in a urethane anesthetized rat model of recurrent seizures induced by 4-aminopyridine. We reveal there to be a close relationship between seizure epicenter depth, translaminar local field potential (LFP) synchrony and tissue oxygenation during the early stages of recurrent seizures, whereby deep layer seizures are associated with decreased cross laminar synchrony and prolonged periods of hypoxia, and middle layer seizures are accompanied by increased cross-laminar synchrony and hyperoxia. Through comparison with functional activation by somatosensory stimulation and graded hypercapnia, we show that these seizure-related cerebrovascular responses occur in the presence of conserved neural-hemodynamic and blood flow-volume coupling. Our data provide new insights into the laminar dependency of seizure-related neurovascular responses, which may reconcile inconsistent observations of seizure-related hypoxia in the literature, and highlight a potential layer-dependent vulnerability that may contribute to the harmful effects of clinical recurrent seizures. The relevance of our findings to perfusion-related functional neuroimaging techniques in epilepsy are also discussed.

SUBMITTER: Harris SS

PROVIDER: S-EPMC5883323 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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Seizure epicenter depth and translaminar field potential synchrony underlie complex variations in tissue oxygenation during ictal initiation.

Harris Samuel S SS Boorman Luke W LW Kennerley Aneurin J AJ Sharp Paul S PS Martin Chris C Redgrave Peter P Schwartz Theodore H TH Berwick Jason J

NeuroImage 20171230

Whether functional hyperemia during epileptic activity is adequate to meet the heightened metabolic demand of such events is controversial. Whereas some studies have demonstrated hyperoxia during ictal onsets, other work has reported transient hypoxic episodes that are spatially dependent on local surface microvasculature. Crucially, how laminar differences in ictal evolution can affect subsequent cerebrovascular responses has not been thus far investigated, and is likely significant in view of ...[more]

PMID: 29294386

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Project description:High frequency oscillations have been proposed as a clinically useful biomarker of seizure generating sites. We used a unique set of human microelectrode array recordings (four patients, 10 seizures), in which propagating seizure wavefronts could be readily identified, to investigate the basis of ictal high frequency activity at the cortical (subdural) surface. Sustained, repetitive transient increases in high gamma (80-150 Hz) amplitude, phase-locked to the low-frequency (1-25 Hz) ictal rhythm, correlated with strong multi-unit firing bursts synchronized across the core territory of the seizure. These repetitive high frequency oscillations were seen in recordings from subdural electrodes adjacent to the microelectrode array several seconds after seizure onset, following ictal wavefront passage. Conversely, microelectrode recordings demonstrating only low-level, heterogeneous neural firing correlated with a lack of high frequency oscillations in adjacent subdural recording sites, despite the presence of a strong low-frequency signature. Previously, we reported that this pattern indicates a failure of the seizure to invade the area, because of a feedforward inhibitory veto mechanism. Because multi-unit firing rate and high gamma amplitude are closely related, high frequency oscillations can be used as a surrogate marker to distinguish the core seizure territory from the surrounding penumbra. We developed an efficient measure to detect delayed-onset, sustained ictal high frequency oscillations based on cross-frequency coupling between high gamma amplitude and the low-frequency (1-25 Hz) ictal rhythm. When applied to the broader subdural recording, this measure consistently predicted the timing or failure of ictal invasion, and revealed a surprisingly small and slowly spreading seizure core surrounded by a far larger penumbral territory. Our findings thus establish an underlying neural mechanism for delayed-onset, sustained ictal high frequency oscillations, and provide a practical, efficient method for using them to identify the small ictal core regions. Our observations suggest that it may be possible to reduce substantially the extent of cortical resections in epilepsy surgery procedures without compromising seizure control.

Project description:PurposeAdequate epileptic seizure detection may have the potential to minimize seizure-related complications and improve treatment evaluation. Autonomic changes often precede ictal electroencephalographic discharges and therefore provide a promising tool for timely seizure detection. We reviewed the literature for seizure detection algorithms using autonomic nervous system parameters.MethodsThe PubMed and Embase databases were systematically searched for original human studies that validate an algorithm for automatic seizure detection based on autonomic function alterations. Studies on neonates only and pilot studies without performance data were excluded. Algorithm performance was compared for studies with a similar design (retrospective vs. prospective) reporting both sensitivity and false alarm rate (FAR). Quality assessment was performed using QUADAS-2 and recently reported quality standards on reporting seizure detection algorithms.ResultsTwenty-one out of 638 studies were included in the analysis. Fifteen studies presented a single-modality algorithm based on heart rate variability (n = 10), heart rate (n = 4), or QRS morphology (n = 1), while six studies assessed multimodal algorithms using various combinations of HR, corrected QT interval, oxygen saturation, electrodermal activity, and accelerometry. Most studies had small sample sizes and a short follow-up period. Only two studies performed a prospective validation. A tendency for a lower FAR was found for retrospectively validated algorithms using multimodal autonomic parameters compared to those using single modalities (mean sensitivity per participant 71-100% vs. 64-96%, and mean FAR per participant 0.0-2.4/h vs. 0.7-5.4/h).ConclusionsThe overall quality of studies on seizure detection using autonomic parameters is low. Unimodal autonomic algorithms cannot reach acceptable performance as false alarm rates are still too high. Larger prospective studies are needed to validate multimodal automatic seizure detection.

Dataset Information

Seizure epicenter depth and translaminar field potential synchrony underlie complex variations in tissue oxygenation during ictal initiation.

Publications

Seizure epicenter depth and translaminar field potential synchrony underlie complex variations in tissue oxygenation during ictal initiation.

Similar Datasets

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