Impaired brain-heart axis in focal epilepsy: Alterations in information flow and implications for seizure dynamics

Abstract

This study delves into functional brain-heart interplay (BHI) dynamics during interictal periods before and after seizure events in focal epilepsy. Our analysis focuses on elucidating the causal interaction between cortical and autonomic nervous system (ANS) oscillations, employing electroencephalography and heart rate variability series. The dataset for this investigation comprises 47 seizure events from 14 independent subjects, obtained from the publicly available Siena Dataset. Our findings reveal an impaired brain-heart axis especially in the heart-to-brain functional direction. This is particularly evident in bottom-up oscillations originating from sympathovagal activity during the transition between preictal and postictal periods. These results indicate a pivotal role of the ANS in epilepsy dynamics. Notably, the brain-to-heart information flow targeting cardiac oscillations in the low-frequency band does not display significant changes. However, there are noteworthy changes in cortical oscillations, primarily originating in central regions, influencing heartbeat oscillations in the high-frequency band. Our study conceptualizes seizures as a state of hyperexcitability and a network disease affecting both cortical and peripheral neural dynamics. Our results pave the way for a deeper understanding of BHI in epilepsy, which holds promise for the development of advanced diagnostic and therapeutic approaches also based on bodily neural activity for individuals living with epilepsy.

Author Summary

This study focuses on brain-heart interplay (BHI) during pre- and postictal periods surrounding seizures. Employing multichannel EEG and heart rate variability data from subjects with focal epilepsy, our analysis reveals a disrupted brain-heart axis dynamic, particularly in the heart-to-brain direction. Notably, sympathovagal activity alterations during preictal to postictal transitions underscore the autonomic nervous system’s pivotal role in epilepsy dynamics. While brain-to-heart information flow targeting low-frequency band cardiac oscillations remains stable, significant changes occur in cortical oscillations, predominantly in central regions, influencing high-frequeny-band heartbeat oscillations, that is, vagal activity. Viewing seizures as states of hyperexcitability and confirming focal epilepsy as a network disease affecting both central and peripheral neural dynamics, our study enhances understanding of BHI in epilepsy. These findings offer potential for advanced diagnostic and therapeutic approaches grounded in bodily neural activity for individuals with epilepsy.