Dynamics of seizure-induced behavioral and autonomic arousal
Arousal is the most primitive, powerful instinct with survival benefit present in all vertebrates. Even though the arousal systems are classically viewed as “ascending” brainstem phenomena, there is a “descending” cortical feedback system that maintains consciousness. In this study, we provide electrophysiological confirmation that seizures localized to the anterior cingulum can behaviorally manifest as paroxysms of arousal from sleep.
Temporal dynamics of arousal induced by anterior cingulate seizures were analyzed by using multiple modalities including stereoelectroencephalography (phase lag index and phase amplitude coupling), lead-1 ECG (point-process heart rate variability analysis) and diffusion tractography (DTI).
The ictal arousal was associated with an increase in synchronization in the alpha band and an increase in local theta or alpha-gamma phase-amplitude coupling. In comparison to seizures that lacked clinical manifestations, ictal arousal was associated with an increase in heart rate but not heart rate variability. Finally, DTI demonstrated degeneration in white fiber tracts passing between the anterior cingulum and anterior thalamus ipsilateral to the epileptogenic cortex. The patient underwent resection of the anterior cingulum, and histopathology confirmed focal cortical dysplasia type II.
Anterior cingulate seizures inducing behavioral arousal have identifiable autonomic and EEG signatures.
KeywordsArousal Hypnopompic seizure Anterior cingulate Phase lag index Phase-amplitude coupling Heart rate variability
SP was instrumental in the conception and design of the study, evaluation of the patient and EMU acquisition of data, contributed to data analysis and writing the manuscript. ET and GC performed analysis and interpretation of data and drafting the article or revising it critically for important intellectual content. MPo and SPo were instrumental in the analysis of HR and HRV. DP and AI helped in data collection, timely critical review of the results and concepts and in the revision of the manuscript. SP in the capacity of the corresponding author agrees to be accountable for all aspects of the work in ensuring the accuracy or integrity of any part of the work investigated and resolved.
Emilia Toth, Diana Pizarro, and SP gratefully acknowledge support from the USA National Science Foundation (NSF RII-2 FEC OIA1632891).
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Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.