Heart–brain interactions shape somatosensory perception and evoked potentials

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 117; no. 19; pp. 10575 - 10584
• Main Authors: Al, Esra, Iliopoulos, Fivos, Forschack, Norman, Nierhaus, Till, Grund, Martin, Motyka, Paweł, Gaebler, Michael, Nikulin, Vadim V., Villringer, Arno
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 12.05.2020
• Subjects: Adult; Amplitudes; Attention - physiology; Attenuation; Awareness - physiology; Biological Sciences; Brain - physiology; Brain Mapping - methods; Consciousness - physiology; Decision theory; EEG; EKG; Electrocardiography; Electrocardiography - methods; Electroencephalography; Electroencephalography - methods; Event-related potentials; Evoked Potentials - physiology; Evoked Potentials, Somatosensory - physiology; Female; Heart - physiology; Heart rate; Heart Rate - physiology; Humans; Information processing; Interoception - physiology; Localization; Male; Neural coding; Oscillations; Perception; Perception - physiology; Sensory integration; Signal detection; Signal processing; Somatosensory Cortex - physiology; Somatosensory evoked potentials; Somatosensory stimuli; Stimuli; Systole; rhythms; body–brain interaction; consciousness; somatosensory awareness; EEG
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.1915629117

Even though humans are mostly not aware of their heartbeats, several heartbeat-related effects have been reported to influence conscious perception. It is not clear whether these effects are distinct or related phenomena, or whether they are early sensory effects or late decisional processes. Combining electroencephalography and electrocardiography, along with signal detection theory analyses, we identify two distinct heartbeat-related influences on conscious perception differentially related to early vs. late somatosensory processing. First, an effect on early sensory processing was found for the heartbeat-evoked potential (HEP), a marker of cardiac interoception. The amplitude of the prestimulus HEP negatively correlated with localization and detection of somatosensory stimuli, reflecting a more conservative detection bias (criterion). Importantly, higher HEP amplitudes were followed by decreases in early (P50) as well as late (N140, P300) somatosensoryevoked potential (SEP) amplitudes. Second, stimulus timing along the cardiac cycle also affected perception. During systole, stimuli were detected and correctly localized less frequently, relating to a shift in perceptual sensitivity. This perceptual attenuationwas accompanied by the suppression of only late SEP components (P300) and was stronger for individuals with a more stable heart rate. Both heart-related effects were independent of alpha oscillations’ influence on somatosensory processing. We explain cardiac cycle timing effects in a predictive coding account and suggest that HEP-related effects might reflect spontaneous shifts between interoception and exteroception or modulations of general attentional resources. Thus, our results provide a general conceptual framework to explain how internal signals can be integrated into our conscious perception of the world.