Pairwise and higher-order measures of brain-heart interactions in children with temporal lobe epilepsy

Abstract

Abstract Objective. While it is well-known that epilepsy has a clear impact on the activity of both the central nervous system (CNS) and the autonomic nervous system (ANS), its role on the complex interplay between CNS and ANS has not been fully elucidated yet. In this work, pairwise and higher-order predictability measures based on the concepts of Granger Causality (GC) and partial information decomposition (PID) were applied on time series of electroencephalographic (EEG) brain wave amplitude and heart rate variability (HRV) in order to investigate directed brain-heart interactions associated with the occurrence of focal epilepsy. Approach. HRV and the envelopes of δ and α EEG activity recorded from ipsilateral (ipsi-EEG) and contralateral (contra-EEG) scalp regions were analyzed in 18 children suffering from temporal lobe epilepsy monitored during pre-ictal, ictal and post-ictal periods. After linear parametric model identification, we compared pairwise GC measures computed between HRV and a single EEG component with PID measures quantifying the unique, redundant and synergistic information transferred from ipsi-EEG and contra-EEG to HRV. Main results. The analysis of GC revealed a dominance of the information transfer from EEG to HRV and negligible transfer from HRV to EEG, suggesting that CNS activities drive the ANS modulation of the heart rhythm, but did not evidence clear differences between δ and α rhythms, ipsi-EEG and contra-EEG, or pre- and post-ictal periods. On the contrary, PID revealed that epileptic seizures induce a reorganization of the interactions from brain to heart, as the unique predictability of HRV originated from the ipsi-EEG for the δ waves and from the contra-EEG for the α waves in the pre-ictal phase, while these patterns were reversed after the seizure. Significance. These results highlight the importance of considering higher-order interactions elicited by PID for the study of the neuro-autonomic effects of focal epilepsy, and may have neurophysiological and clinical implications.