Skipping a Beat: Heartbeat-Evoked Potentials Reflect Predictions during Interoceptive-Exteroceptive Integration

Abstract

Several theories propose that emotions and self-awareness arise from the integration of internal and external signals and their respective precision-weighted expectations. Supporting these mechanisms, research indicates that the brain uses temporal cues from cardiac signals to predict auditory stimuli, and that these predictions and their prediction errors can be observed in the scalp heartbeat-evoked potential (HEP). We investigated the effect of precision modulations on these cross-modal predictive mechanisms, via attention and interoceptive ability. We presented auditory sequences at short (perceived synchronous) or long (perceived asynchronous) cardio-audio delays, with half of the trials including an omission. Participants attended to the cardio-audio synchronicity of the tones (internal attention) or the auditory stimuli alone (external attention). Comparing HEPs during omissions allowed for the observation of pure predictive signals, without contaminating auditory input. We observed an early effect of cardio-audio delay, reflecting a difference in heartbeat-driven expectations. We also observed a larger positivity to omissions of sounds perceived as synchronous than to omissions of sounds perceived as asynchronous when attending internally only, consistent with the role of attentional precision for enhancing predictions. These results provide support for attentionally-modulated cross-modal predictive coding, and suggest a potential tool for investigating its role in emotion and self-awareness.

Brain-heart interactions in the neurobiology of consciousness

“…Similarly, HERs correlate with somatosensory perception in a tactile detection task [74,75], confirming that HERs reflect the integration of internal signals during conscious perception. HERs also relate to the conscious detection of auditory irregularities [76,77], showing that cortical potentials locked to heartbeats reflect human expectations of the external world. HERs covary with different aspects of self-related cognition, including self-relatedness of spontaneous thoughts [78,79], self vs other distinction in imagination [80], bodily-self-identification of the full body [81], and face [82].…”

“…In addition to the evidence on brain-heart interactions reflecting states-of-consciousness [77,[110][111][112]116], abundant experimental evidence shows that the integration of exteroceptive and interoceptive information, beyond the heart, relate to perceptual and self-awareness [73,[75][76][77][117][118][119][120][121][122][123][124]. The biomarkers of brain-heart interactions have a great potential to measure and understand the different dimensions leading to a subjective, conscious experience.…”

Past and Future Explanations for Depersonalization and Derealization Disorder: A Role for Predictive Coding

“…In addition to the apparent unique HEP amplitude found in those with DP and DR (i.e., no increase in HEP during heartbeat detection), HEP offers a potential insight into the predictive coding mechanisms that may be responsible for this condition. If HEP represents a precision weighted interoceptive prediction error signal as has been proposed by others ( Ainley et al, 2016 ; Petzschner et al, 2019 ) then attending to one’s heartbeat should increase the precision of these prediction errors, increasingly their likelihood of propagating up the predictive coding hierarchy to update predictions ( Banellis and Cruse, 2020 ). However, if imprecise predictions are responsible for DP and DR, then consistent HEP responses, regardless of one’s focus of attention, could reflect an inability to adjust (or perhaps maintain) the precision weighting of interoceptive predictions versus prediction errors, leading to prediction errors that fail to update predictions.…”

Brain–Heart Interaction and the Experience of Flow While Playing a Video Game

“…HEP amplitudes around 400–500ms after the ECG R-peak have been mostly investigated and interpreted as correlates of the successive cognitive elaboration of interoceptive information ( Baranauskas et al, 2017 ). In the context of interoceptive predictive coding concepts ( Seth et al, 2012 ; Critchley and Garfinkel, 2018 ), the brain has been shown to use the interoceptive signals (cardiac information) to successfully predict upcoming exteroceptive events ( Park et al, 2014 ; Pfeiffer and De Lucia, 2017 ; Banellis and Cruse, 2020 ). Thumper is a dynamic rhythm game that demands high levels of concentration while performing challenging sensorimotor tasks.…”