Heartbeat induces a cortical theta-synchronized network in the resting state

Abstract

In the resting state, heartbeats evoke cortical responses called heartbeat-evoked responses (HERs), which reflect cortical cardiac interoceptive processing. While previous studies have reported that the heartbeat evokes cortical responses at a regional level, whether the heartbeat induces synchronization between regions to form a network structure remains unknown. Using resting-state magnetoencephalography data from 85 human subjects of both genders, we first showed that heartbeat increases the phase synchronization between cortical regions in the theta frequency but not in other frequency bands. This increase in synchronization between cortical regions formed a network structure called the heartbeat-induced network (HIN), which did not reflect artificial phase synchronization. In the HIN, the left inferior temporal gyrus and parahippocampal gyrus played a central role as hubs. Furthermore, the HIN was modularized, containing 5 subnetworks called modules. In particular, module 1 played a central role in between-module interactions in the HIN. Furthermore, synchronization within module 1 had a positive association with the mood of an individual. In this study, we show the existence of the HIN and its network properties, advancing the current understanding of cortical heartbeat processing and its relationship with mood, which was previously confined to region-level.

Significance statement Complex brain processing usually occurs at a network level, which requires an interaction between brain regions. However, despite its importance in homeostasis and affective processing, a network level processing of cardiac interoception has not been investigated. Here, we first provided an evidence that the heartbeat induces phase synchronizations between cortical regions those comprise a heartbeat-induced network (HIN) with control analyses excluding the possibility of an artificial synchronization. Furthermore, by applying graph-theoretical analysis, we find hubs of the HIN and found out that it is a modularized network with five modules. Finally, we also showed the relationship between the participants’ mood and the HIN. These results provide the first evidence of network-level heartbeat processing and its relevance with emotion.