Heart cycle-related effects on event-related potentials, spectral power changes, and connectivity patterns in the human ECoG

Abstract

The perception of one's own heartbeat is a fundamental interoceptive process that involves cortical and subcortical structures. Yet, the precise spatiotemporal neuronal activity patterns underlying the cortical information processing have remained largely elusive. Although the high temporal and spatial resolution of electrocorticographic (ECoG) recordings is increasingly being exploited in functional neuroimaging, it has not been used to study heart cycle-related effects. Here, we addressed the capacity of ECoG to characterize neuronal signals within the cardiac cycle, as well as to disentangle them from heart cycle-related artifacts. Based on topographical distribution and latency, we identified a biphasic potential within the primary somatosensory cortex, which likely constitutes a heartbeat-evoked potential (HEP) of neuronal origin. We also found two different types of artifacts: i) oscillatory potential changes with a frequency identical to the heart pulse rate, which probably represent pulsatility artifacts and ii) sharp potentials synchronized to the R-peak, corresponding to the onset of ventricular contraction and the cardiac field artifact (CFA) in EEG. Finally, we show that heart cycle-related effects induce pronounced phase-synchrony patterns in the ECoG and that this kind of correlation patterns, which may confound ECoG connectivity studies, can be reduced by a suitable correction algorithm. The present study is, to our knowledge, the first one to show a focally localized cortical HEP that could be clearly and consistently observed over subjects, suggesting a basic role of primary sensory cortex in processing of heart-related sensory inputs. We also conclude that taking into account and reducing heart cycle-related effects may be advantageous for many ECoG studies, and are of crucial importance, particularly for ECoG-based connectivity studies. Thus, in summary, although ECoG poses new challenges, it opens up new possibilities for the investigation of heartbeat-related viscerosensory processing in the human brain.

Keywords: CFA; CSF; Connectivity; ECoG; EEG; EMG; ESM; Electrocorticogram; FDR; HEP; Heartbeat-evoked potential; PSI; Phase synchrony; SNR; Signal quality; Somatosensory cortex; cardiac field artifact; cerebrospinal fluid; electrical stimulation mapping; electrocorticogram; electroencephalogram; electromyogram; false discovery rate; heartbeat-evoked potential; phase synchrony index; signal-to-noise-ratio.