Heartbeat-evoked Potential Research Articles

Distinctive body perception mechanisms in high versus low symptom reporters: A neurophysiological model for medically-unexplained symptoms

ObjectiveThe neurophysiological processes involved in the generation of medically-unexplained symptoms (MUS) remain unclear. This study tested three assumptions of the perception-filter model contributing to MUS: (I.) increased bodily signal strength (II.) decreased filter function, (III.) increased perception. MethodsIn this cross-sectional, observational study, trait MUS were assessed by a web-based survey (N = 486). The upper and lower decile were identified as extreme groups of high (HSR; n = 29; 26 women; Mage = 26.0 years) and low symptom reporters (LSR; n = 29; 21 women; Mage = 28.4 years). Mean heart rate (HR) and heart rate variability (HRV), and cortisol awakening response (CAR) were assessed as indicators of bodily signal strength (I.). Heartbeat-evoked potentials (HEPs) were assessed during rest and a heartbeat perception task. HEPs reflect attentional resources allocated towards heartbeats and served as index of filter function (II.). Interoceptive accuracy (IAc) in heartbeat perception was assessed as an indicator of perception (III.). ResultsHSR showed higher HR and lower HRV (RMSSD) than LSR (I.), but no differences in CAR. HSR exhibited a stronger increase of HEPs when attention was focused on heartbeats than LSR (II.); there were no group differences in IAc (III.). ConclusionsThe perception-filter model was partially confirmed in that HSR showed altered bodily signals suggesting higher sympathetic activity (I.); higher HEP increases indicated increased filter function for bodily signals (II.). As more attentional resources are mobilized to process heartbeats, but perception accuracy remains unchanged (III.), this overflow could be responsible for detecting minor bodily changes associated with MUS.

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

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 the omissions of sounds perceived as synchronous than to the 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.

Methodological Considerations on EEG Electrical Reference: A Functional Brain-Heart Interplay Study.

The growing interest in the study of functional brain-heart interplay (BHI) has motivated the development of novel methodological frameworks for its quantification. While a combination of electroencephalography (EEG) and heartbeat-derived series has been widely used, the role of EEG preprocessing on a BHI quantification is yet unknown. To this extent, here we investigate on four different EEG electrical referencing techniques associated with BHI quantifications over 4-minute resting-state in 15 healthy subjects. BHI methods include the synthetic data generation model, heartbeat-evoked potentials, heartbeat-evoked oscillations, and maximal information coefficient (MIC). EEG signals were offline referenced under the Cz channel, common average, mastoids average, and Laplacian method, and statistical comparisons were performed to assess similarities between references and between BHI techniques. Results show a topographical agreement between BHI estimation methods depending on the specific EEG reference. Major differences between BHI methods occur with the Laplacian reference, while major differences between EEG references are with the MIC analysis. We conclude that the choice of EEG electrical reference may significantly affect a functional BHI quantification.

Heart–brain interactions shape somatosensory perception and evoked potentials

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) somatosensory-evoked 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 attenuation was 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.

A New Technique to Measure the Level of Interest Using Heartbeat-Evoked Brain Potential

Abstract. Interest is a positive emotion related to attention. The event-related brain potential (ERP) probe technique is a useful method to evaluate the level of interest in dynamic stimuli. However, even in the irrelevant probe technique, the probe is presented as a physical stimulus and steals the observer’s attentional resources, although no overt response is required. Therefore, the probe might become a problematic distractor, preventing deep immersion of participants. Heartbeat-evoked brain potential (HEP) is a brain activity, time-locked to a cardiac event. No probe is required to obtain HEP data. Thus, we aimed to investigate whether the HEP can be used to evaluate the level of interest. Twenty-four participants (12 males and 12 females) watched attractive and unattractive individuals of the opposite sex in interesting and uninteresting videos (7 min each), respectively. We performed two techniques each for both the interesting and the uninteresting videos: the ERP probe and the HEP techniques. In the former, somatosensory stimuli were presented as task-irrelevant probes while participants watched videos: frequent (80%) and infrequent (20%) stimuli were presented at each wrist in random order. In the latter, participants watched videos without the probe. The P2 amplitude in response to the somatosensory probe was smaller and the positive wave amplitudes of HEP were larger while watching the videos of attractive individuals than while watching the videos of unattractive ones. These results indicate that the HEP technique is a useful method to evaluate the level of interest without an external probe stimulus.

Heart and brain: Cortical representation of cardiac signals is disturbed in borderline personality disorder, but unaffected by oxytocin administration

BackgroundEmotional dysregulation, a core feature of borderline personality disorder (BPD) has recently been linked to deficits in the cortical representation of bodily signals. Oxytocin modulates the salience of external social cues. However, its role in interoception is still not fully understood. The aim of the current study was to replicate reduced heartbeat-evoked potentials (HEPs) as a marker for the cortical representation of cardiac signals in BPD and to explore potential effects of oxytocin on HEP amplitude. MethodsFifty-three medication-free women with a DSM-IV diagnosis of BPD and sixty healthy female controls (HCs) participated in the study. In a randomized, double-blind placebo-controlled trial, participants self-administered either 24 I.U. of oxytocin or placebo and took part in a 5-minute resting-state electrocardiogram (ECG) with parallel electroencephalogram (EEG) measurement. In addition, emotional dysregulation and BPD symptomatology were assessed with self-report questionnaires. ResultsPatients with BPD had significantly lower mean HEP amplitudes than HCs. Furthermore, HEP amplitudes were negatively correlated with emotional dysregulation in the whole sample. However, oxytocin had no significant effect on HEP amplitude. LimitationsOnly female participants were investigated and no clinicial controls were included. ConclusionsThis is the first replication from an independent sample showing a reduced cortical representation of cardiac signals in BPD patients. This, together with other body-related symptoms, suggests deficits in the processing of bodily signals, which seem to be associated with emotional dysregulation. Whether oxytocin influences HEP during emotion regulation tasks needs to be investigated in future studies.

Affective and temporal orientation of thoughts: Electrophysiological evidence

The factors that determine the content and valence of spontaneous thoughts have not yet been clarified. In this study, we focused on the effects of bodily states and depression and anxiety traits. Participants performed a past/future thinking task in which three-part sentences including temporal cues were presented in a sequential pattern, for example “in the near future/dreams/will come true”. We measured heartbeat-evoked potentials (HEPs) to assess affective processing, and event-related potentials (ERPs) to assess temporal processing of thoughts that emerged when the temporal cue words were presented. The HEPs predicted thought valence irrespective of personality traits. Larger N400 ERPs were observed in response to past-oriented than to future-oriented words in participants with higher levels of depression, whereas the opposite was the case in participants with higher social anxiety. Our data suggest that afferent signals modulate affective thought-orientations as triggers, and that individuals with depression and anxiety have sensitivity toward temporal information at the neural level.

Heartbeat-evoked cortical responses: Underlying mechanisms, functional roles, and methodological considerations

The heart continuously and cyclically communicates with the brain. Beyond homeostatic regulation and sensing, recent neuroscience research has started to shed light on brain-heart interactions in diverse cognitive and emotional processes. In particular, neural responses to heartbeats, as measured with the so-called heartbeat-evoked potential, have been shown to be useful for investigating cortical activity processing cardiac signals. In this review, we first overview and discuss the basic properties of the HEP such as underlying physiological pathways, brain regions, and neural mechanisms. We then provide a systematic review of the mental processes associated with cortical HEP activations, notably heartbeat perception, emotional feelings, perceptual awareness, and self-consciousness, in healthy subjects and clinical populations. Finally, we discuss methodological issues regarding the experimental design and data analysis for separating genuine HEP components from physiological artifacts (e.g., cardiac field artifact, pulse artifact) or other neural activities that are not specifically associated with the heartbeat. Findings from this review suggest that when intrinsic limitations (e.g., artifacts) are carefully controlled, the HEP could provide a reliable neural measure for investigating brain-viscera interactions in diverse mental processes.

IR-camera-based measurements of 2D/3D cognitive fatigue in 2D/3D display system using task-evoked pupillary response.

This study was carried out to evaluate a method used to measure three-dimensional (3D) cognitive fatigue based on the pupillary response. This technique was designed to overcome measurement burdens by using non-contact methods. The pupillary response is related to cognitive function by a neural pathway and may be an indicator of 3D cognitive fatigue. Twenty-six undergraduate students (including 14 women) watched both 2D and 3D versions of a video for 70min. The participants experienced visual fatigue after viewing the 3D content. Measures such as subjective rating, response time, event-related potential latency, heartbeat-evoked potential (HEP) alpha power, and task-evoked pupillary response (TEPR) latency were significantly different. Multitrait-multimethod matrix analysis indicated that HEP and TEPR latency measures had stronger reliability and higher correlations with 3D cognitive fatigue than other measures. TEPR latency may be useful for quantitatively determining 3D visual fatigue, as it can be easily used to evaluate 3D visual fatigue using a non-contact method without measuring burden.

I feel what I do: Relating interoceptive processes and reward-related behavior

Interoceptive signalling has been shown to contribute to action regulation and action experience. Here, we assess whether motor behaviour can be influenced by anticipated homeostatic feeling states induced through different predictable contexts. Participants performed a reward incentive paradigm in which accurate responses increased (gain) or avoided the depletion (averted loss) of a credit score. Across two types of blocks, we varied the predictability of the outcome state. In predictable blocks, a cue signaled a gain, loss or control trial (motor response did not affect the credit score). This allowed participants to anticipate the interoceptive feeling state associated with the outcome. In unpredictable blocks, the cue had no relation to the type of outcome. Thus, participants were unable to anticipate the feeling state it produced. Via EEG, we measured the Heartbeat Evoked Potential (HEP) and the Contingent Negative Variation (CNV) as indices of interoceptive and motor processing respectively. In addition, we measured feedback P3 amplitude following outcome presentation and accuracy and reaction times of the required motor response. We observed higher HEP and CNV amplitudes as well as faster and more accurate motor responses in predictable compared to unpredictable outcome blocks. Similarly, feedback-related P3 amplitudes were significantly lower for predictable relative to unpredictable outcomes. Crucially, HEP amplitudes measured prior to feedback predicted feedback-related P3 amplitudes for anticipated outcome events. Results suggest that accurate anticipation of homeostatic feeling states associated with gain, loss or control outcomes facilitates motor execution and outcome evaluation. Findings are hereby the first to empirically assess the link between interoceptive and motor domains and provide primary evidence for a joint processing structure.

Increased heartbeat-evoked potential during REM sleep in nightmare disorder.

Nightmares are characterized by the experience of strong negative emotions occurring mainly during REM sleep. Some people suffer from nightmare disorder, which is defined by the repeated occurrence of nightmares and by significant distress in wakefulness. Yet, whether frequent nightmares relate to a general increase in emotional reactivity or arousal during sleep remains unclear. To address this question, we recorded heartbeat-evoked potentials (HEPs) during wakefulness, NREM and REM sleep in patients with nightmare disorder and healthy participants. The HEP represents a cortical (EEG) response to the heartbeat and indexes brain-body interactions, such as interoceptive processing and intrinsic levels of arousal. HEP amplitude is typically increased during states of high emotional arousal and motivation, and is decreased in depression. Here we compared the amplitude of HEPs between nightmare patients and healthy controls separately during AWAKE, NREM, REM periods, and found higher HEP amplitude in nightmare patients compared to healthy controls over a cluster of frontal regions only during REM sleep. This effect was not paralleled by any group difference in cardiac control measures (e.g. heart rate variability, interbeat interval). These findings corroborate the notion that nightmares are essentially a REM pathology and suggest that increased emotional arousal during REM sleep, as measured by HEP, is a physiological condition responsible for frequent nightmares. This result also supports that HEP may be used as a biomarker of increased emotional and sensory processing during REM sleep in these patients.

Focus of attention modulates the heartbeat evoked potential

Theoretical frameworks such as predictive coding suggest that the perception of the body and world – interoception and exteroception – involve intertwined processes of inference, learning, and prediction. In this framework, attention is thought to gate the influence of sensory information on perception. In contrast to exteroception, there is limited evidence for purely attentional effects on interoception. Here, we empirically tested if attentional focus modulates cortical processing of single heartbeats, using a newly-developed experimental paradigm to probe purely attentional differences between exteroceptive and interoceptive conditions in the heartbeat evoked potential (HEP) using EEG recordings. We found that the HEP is significantly higher during interoceptive compared to exteroceptive attention, in a time window of 524–620 ms after the R-peak. Furthermore, this effect predicted self-report measures of autonomic system reactivity. Our study thus provides direct evidence that the HEP is modulated by pure attention and suggests that this effect may provide a clinically relevant readout for assessing interoception.

The relationship between social anxiety and heartbeat evoked potential amplitude

Past research suggests that social anxiety is associated with increased processing of cardiac activity. Cognitive theories propose that this is one aspect of self-focus, which is driven by concerns that features of the self, such as anxiety symptoms, will elicit evaluation from others. We investigated the relationship of social anxiety to the cortical processing of heartbeats as reflected in the heartbeat evoked potential (HEP) during false feedback of accelerated heart rate. Thirty-eight participants with high social anxiety (HSA; n = 19) and non-elevated social anxiety (NSA; n = 19) completed a cognitive task during which false feedback of accelerated heart rate was randomly provided on 50% of trials. HEP amplitude was larger in HSAs, but not NSAs, during false heartbeat acceleration cues compared to standard cues. HEP amplitude also was larger in HSAs compared to NSAs during acceleration cues. HEP amplitude during acceleration cues, but not standard cues correlated with social anxiety. Within the first second after the R-peak, social anxiety correlated with voltage at Fz from 223 to 305 ms. Social concerns about the consequences of anxiety symptoms accounted for an indirect relationship between social anxiety and the HEP. These data extend prior evidence of increased processing of cardiac activity in socially anxious individuals, providing support for cognitive theories.

An Effect of Rhythmic Stimuli, Internal Attention and Exercise on Heartbeat-evoked Potential

An Effect of Rhythmic Stimuli, Internal Attention and Exercise on Heartbeat-evoked Potential

Affective interoceptive inference: Evidence from heart-beat evoked brain potentials.

The perception of internal bodily signals (interoception) is central to many theories of emotion and embodied cognition. According to recent theoretical views, the sensory processing of visceral signals such as one's own heartbeat is determined by top-down predictions about the expected interoceptive state of the body (interoceptive inference). In this EEG study we examined neural responses to heartbeats following expected and unexpected emotional stimuli. We used a modified stimulus repetition task in which pairs of facial expressions were presented with repeating or alternating emotional content, and we manipulated the emotional valence and the likelihood of stimulus repetition. We found that affective predictions of external socially relevant information modulated the heartbeat-evoked potential, a marker of cardiac interoception. Crucially, the HEP changes highly relied on the expected emotional content of the facial expression. Thus, expected negative faces led to a decreased HEP amplitude, whereas such an effect was not observed after an expected neutral face. These results suggest that valence-specific affective predictions, and their uniquely associated predicted bodily sensory state, can reduce or amplify cardiac interoceptive responses. In addition, the affective repetition effects were dependent on repetition probability, highlighting the influence of top-down exteroceptive predictions on interoception. Our results are in line with recent models of interoception supporting the idea that predicted bodily states influence sensory processing of salient external information.

Altered neural signatures of interoception in multiple sclerosis.

Multiple sclerosis (MS) patients present several alterations related to sensing of bodily signals. However, no specific neurocognitive impairment has yet been proposed as a core deficit underlying such symptoms. We aimed to determine whether MS patients present changes in interoception-that is, the monitoring of autonomic bodily information-a process that might be related to various bodily dysfunctions. We performed two studies in 34 relapsing-remitting, early-stage MS patients and 46 controls matched for gender, age, and education. In Study 1, we evaluated the heartbeat-evoked potential (HEP), a cortical signature of interoception, via a 128-channel EEG system during a heartbeat detection task including an exteroceptive and an interoceptive condition. Then, we obtained whole-brain MRI recordings. In Study 2, participants underwent fMRI recordings during two resting-state conditions: mind wandering and interoception. In Study 1, controls exhibited greater HEP modulation during the interoceptive condition than the exteroceptive one, but no systematic differences between conditions emerged in MS patients. Patients presented atrophy in the left insula, the posterior part of the right insula, and the right anterior cingulate cortex, with abnormal associations between neurophysiological and neuroanatomical patterns. In Study 2, controls showed higher functional connectivity and degree for the interoceptive state compared with mind wandering; however, this pattern was absent in patients, who nonetheless presented greater connectivity and degree than controls during mind wandering. MS patients were characterized by atypical multimodal brain signatures of interoception. This finding opens a new agenda to examine the role of inner-signal monitoring in the body symptomatology of MS.

Cardiac interoceptive learning is modulated by emotional valence perceived from facial expressions.

Interoception refers to the processing of homeostatic bodily signals. Research demonstrates that interoceptive markers can be modulated via exteroceptive stimuli and suggests that the emotional content of this information may produce distinct interoceptive outcomes. Here, we explored the impact of differently valenced exteroceptive information on the processing of interoceptive signals. Participants completed a repetition-suppression paradigm viewing repeating or alternating faces. In experiment 1, faces wore either angry or pained expressions to explore the interoceptive response to different types of negative stimuli in the observer. In experiment 2, expressions were happy or sad to compare interoceptive processing of positive and negative information. We measured the heartbeat evoked potential (HEP) and visual evoked potentials (VEPs) as a respective marker of intero- and exteroceptive processing. We observed increased HEP amplitude to repeated sad and pained faces coupled with reduced HEP and VEP amplitude to repeated angry faces. No effects were observed for positive faces. However, we found a significant correlation between suppression of the HEP and VEP to repeating angry faces. Results highlight an effect of emotional expression on interoception and suggest an attentional trade-off between internal and external processing domains as a potential account of this phenomenon.

Late heartbeat-evoked potentials are associated with survival after cardiac arrest

RationaleCardiac arrest (CA) is a serious condition characterized by high mortality rates, even after initial successful resuscitation, mainly due to neurological damage. Whether brain-heart communication is associated with outcome after CA is unknown. Heartbeat-evoked brain potentials (HEPs) represent neurophysiological indicators of brain-heart communication. The aim of this study was to address the association between HEPs and survival after CA. MethodsHEPs were calculated from resting EEG/ECG in 55 CA patients 24 h after resuscitation. All patients were treated with targeted temperature management and a standardized sedation protocol during assessment. We investigated the association between HEP amplitude (180–320 ms, 455–595 ms, 860–1000 ms) and 6-month survival. ResultsTwenty-five of 55 patients (45%) were still alive at 6-month follow-up. Survivors showed a higher HEP amplitude at frontopolar and frontal electrodes in the late HEP interval than non-survivors. This effect remained significant after controlling for between-group differences in terms of age, Fentanyl dose, and time lag between resuscitation and EEG assessment. There were no group differences in heart rate or heart rate variability. ConclusionBrain-heart communication, as reflected by HEPs, is associated with survival after CA. Future studies should address the brain-heart axis in CA.

Exteroceptive expectations modulate interoceptive processing: repetition-suppression effects for visual and heartbeat evoked potentials

Interoception refers to the signaling of internal bodily commands. Here, we explore repetition suppression of intero- and exteroceptive neural markers to test whether the perception and predictability of exteroceptive stimulus material affects their expression. Participants completed a repetition suppression paradigm in which angry or neutral facial expressions repeated or alternated. Participants received either an implicit (experiment 1) or explicit (experiment 2) cue enabling the formation of expectations regarding the upcoming facial expression. We measured the heartbeat-evoked potential (HEP) indexing cardiac processing and visual evoked potentials (VEP) in response to viewing the second (repeated or alternated) face. Repeating angry facial expressions produced repetition suppression of both HEP and VEP amplitude while repeating neutral expressions led to repetition enhancement of HEP amplitude. This effect was magnified when participants were explicitly aware of predictive cues. Furthermore, repetition suppression of HEP amplitude correlated with neural attenuation of VEP activity. Results highlight repetition effects for interoceptive as well as exteroceptive neural markers and support top-down, expectation-based accounts of the phenomenon. Furthermore, results demonstrate that the perception of exteroceptive stimulus information has an effect on the processing of interoceptive signals and suggest a direct neural connection between the processing of external and internal sensory information.

Brain responses and self-reported indices of interoception: Heartbeat evoked potentials are inversely associated with worrying about body sensations

Interoception may be defined as a group of senses reflecting physiological state of the body; however the link between physiological and self-reported indices of interoception is not well established. We aimed to elucidate the relationship between the CNS representation of interoceptive processing – the late part of the heartbeat evoked potential (HEP) – and the self-reported interoceptive abilities and tendencies as assessed with the scales of Multidimensional Assessment of Interoceptive Awareness (MAIA) questionnaire. The HEP amplitudes at 400–600ms and MAIA scores from 30 healthy participants were subjected to the cluster-based permutation tests on the t-values of Pearson correlations. HEP amplitudes were positively associated with individual scores on the Not-Worrying scale of MAIA at Cz in the time window from 400ms to 545ms after the R peak. No other MAIA scales were related to the late HEP amplitudes, suggesting that scales and HEPs measure different aspects that are not directly interrelated. This supports the need to treat interoception as a multidimensional construct.