When the Heart Meets the Mind: Exploring the Brain-Heart Interaction during Time Perception.

Recent studies suggest that time estimation relies on bodily rhythms and interoceptive signals. We provide the first direct electrophysiological evidence suggesting an association between the brain's processing of heartbeat and duration judgment. We examined heartbeat-evoked potential (HEP) and contingent negative variation (CNV) during an auditory duration-reproduction task and a control reaction-time task spanning 4, 8, and 12 s intervals, in both male and female participants. Interoceptive awareness was assessed with the Self-Awareness Questionnaire (SAQ) and interoceptive accuracy through the heartbeat-counting task (HCT). Results revealed that SAQ scores, but not the HCT, correlated with mean reproduced durations with higher SAQ scores associating with longer and more accurate duration reproductions. Notably, the HEP amplitude changes during the encoding phase of the timing task, particularly within 130-270 ms (HEP1) and 470-520 ms (HEP2) after the R-peak, demonstrated interval-specific modulations that did not emerge in the control task. A significant ramp-like increase in HEP2 amplitudes occurred during the duration-encoding phase of the timing but not during the control task. This increase within the reproduction phase of the timing task correlated significantly with the reproduced durations for the 8 s and the 4 s intervals. The larger the increase in HEP2, the greater the under-reproduction of the estimated duration. CNV components during the encoding phase of the timing task were more negative than those in the reaction-time task, suggesting greater executive resources orientation toward time. We conclude that interoceptive awareness (SAQ) and cortical responses to heartbeats (HEP) predict duration reproductions, emphasizing the embodied nature of time.

Role of anatomical insular subdivisions in interoception: Interoceptive attention and accuracy have dissociable substrates.

Prior neuroimaging studies have supported the idea that the human insular cortex plays an important role in processing and representing internal bodily states, also termed "interoception." According to recent theoretical studies, interoception includes several aspects such as attention and accuracy. However, there is no consensus on the laterality and location of the insula to support each aspect of interoception. Thus, we aimed to identify the anatomical insular subdivisions involved in interoceptive attention and accuracy; we examined 28 healthy volunteers who completed the behavioral heartbeat counting task and interoceptive attention paradigm using functional magnetic resonance imaging. First, interoceptive attention induced significant activation in the bilateral frontal operculum, precentral gyrus, middle insula, middle cingulate cortex, and supplementary motor area. Then, we compared the activation in anatomically predefined insular subdivisions during interoceptive attention. The highest activation of the middle short gyrus was noted within the insular cortex, followed by the anterior short gyrus and posterior short gyrus, while no significant hemispheric differences were observed. Finally, the interoceptive accuracy index, measured using the heartbeat counting task, strongly correlated with the activity of the right dorsal anterior insula/frontal operculum. These findings suggest that interoceptive attention is associated with the bilateral dorsal mid-anterior insula, which supports the processing and representation of bodily signals. In contrast, the more dorsal anterior portion of the right insula plays a key role in obtaining accurate interoception.

Does it help to feel your body? Evidence is inconclusive that interoceptive accuracy and sensibility help cope with negative experiences.

In four studies (total N = 534), we examined the moderating impact of Interoceptive Accuracy (i.e. IAcc, as measured with the heartbeat counting task) and Interoceptive Sensibility (IS, assessed via questionnaire) on negative affect, following social exclusion or after receiving negative feedback. Results from an integrative data analysis combining the four studies confirmed that the manipulations were successful at inducing negative affect. However, no significant interaction between mood induction (control versus negative affect induction) and interoception on mood measures was observed, and this was true both for objective (i.e. IAcc) and subjective (i.e. IS) measures of interoception. Hence, previous conclusions on the moderating impact of interoception in the relationship between mood induction and self-reported mood were neither replicated nor generalised to this larger sample. We discuss these findings in light of theories of emotion regulation as well as recent concerns raised about the validity of the heartbeat counting task.

Interoception and gender: What aspects should we pay attention to?

Interoception is involved in both somatic and mental disorders with different prevalence between genders; however, gender differences are often neglected. To examine the potential gender differences in interoceptive awareness, we recruited 376 healthy subjects (51% males, aged 17-30years), to fill in the Multidimensional Assessment of Interoceptive Awareness (MAIA). Of that sample, in a subgroup of 40 subjects (50% males), interoceptive accuracy was assessed by heartbeat counting task (HCT). The results on interroceptive awareness suggest that females tendto notice bodily sensations more often, better understand relations between bodily sensations and emotional states, worry or experience more emotional distress with sensations of pain or discomfort and see body as less safe. The results of interoceptive accuracy further suggest that females are less efficient in consciously detecting heartbeats. Therefore, gender should be considered when interoceptive evaluation is performed in disorders associated to bodily sensations and to the emotional/mood states.

Should Adolescents Listen to Their Hearts? A Closer Look at the Associations Between Interoception, Emotional Awareness and Emotion Regulation in Adolescents.

The aim of the current study was to replicate findings from prior work among adults showing that individuals with better interoceptive skills have more emotional awareness, and show better emotion regulation abilities, in a sample of adolescents and by relying on instructions that reduce the contamination of known confound variables. A total of 102 Belgian adolescents (Mage = 14.10 years, SDage = .63; 50 males) completed self-report questionnaires of emotional processes (FEEL-KJ and DERS) and the modified heartbeat counting task. From this task, interoceptive accuracy, interoceptive sensibility (confidence ratings), and interoceptive awareness scores (within-person correlations) were derived per participant. Results revealed no associations between the three dimensions of interoception and adolescents' levels of emotional awareness, adaptive, and maladaptive emotion regulation. The lack of associations which contrast some prior work with adults may be due to developmental differences. However, these might also support the low validity of the heartbeat counting task, or could be attributed to the measurement of the emotion measures (i.e., self-report). Future studies should, nevertheless, also test whether these non-significant results can be explained by the developmental differences in adolescents. Longitudinal research is needed to capture interoceptive changes during adolescence, as well as to replicate the current findings using rigorous multimethod approaches that increase the validity of interoception measurement.

Thermosensation and emotion: Thermosensory accuracy in a dynamic thermal matching task is linked to depression and anxiety symptomatology.

Interoception is related to the generation of bodily feelings and the awareness of ourselves as 'sentient beings', informing the organism about its bodily needs to guarantee survival. Previous studies have reported links among interoception, emotion processing, and mental health. For example, the alignment of interoceptive dimensions (i.e., accuracy, sensibility, awareness) can predict emotional symptoms, such as anxiety. Here, we aimed to investigate the relationship between the perception of a certain type of skin-mediated interoceptive signal, i.e., thermosensation, and self-reported depression, anxiety, and stress. One hundred seventy participants completed the Depression Anxiety Stress Scale (DASS-21) and a dynamic thermal matching task, a static temperature detection task, and a heartbeat counting task. Our results revealed that self-reported anxiety and depression were related to the perception of temperature on hairy and non-hairy skin, respectively: higher anxiety was related to better performance on the thermal matching task on the forearm, while higher depression was related to poorer performance on dynamic and static temperature tasks on the palm. Discrepancies between thermosensory accuracy and sensibility measures ('trait prediction error') were related to heightened anxiety, in line with previous studies. No significant correlations were found between DASS-21 scores and heartbeat counting accuracy. In conclusion, this study suggests that individual differences in thermosensory perception in different areas of the body are associated with self-reported anxiety and depression.

Intranasal Oxytocin Improves Interoceptive Accuracy and Heartbeat-Evoked Potentials During a Cardiac Interoceptive Task.

BACKGROUND: Interoception represents perception of the internal bodily state, which is closely associated with social/emotional processing and physical health in humans. Understanding the mechanism that underlies interoceptive processing, particularly its modulation, is therefore of great importance. Given the overlap between oxytocinergic pathways and interoceptive signaling substrates in both peripheral visceral organs and the brain, intranasal oxytocin administration is a promising approach for modulating interoceptive processing. METHODS: Using a double-blind, placebo-controlled, between-participant design, we recruited 72 healthy male participants who performed a cardiac interoceptive task during electroencephalograph and electrocardiograph recording to examine whether intranasal administration of the neuropeptide oxytocin could modulate interoceptive processing. We also collected data in a resting state to examine whether we could replicate previous findings. RESULTS: The results showed that in the interoceptive task, oxytocin increased interoceptive accuracy at the behavioral level, which was paralleled by larger heartbeat-evoked potential amplitudes in frontocentral and central regions on the neural level. However, there were no significant effects of oxytocin on electroencephalograph or electrocardiograph during resting state. CONCLUSIONS: These findings suggest that oxytocin may only have a facilitatory effect on interoceptive processing under task-based conditions. Our findings not only provide new insights into the modulation of interoceptive processing via targeting the oxytocinergic system but also provide proof-of-concept evidence for the therapeutic potential of intranasal oxytocin in mental disorders with dysfunctional interoception.

The relationship between subjective difficulty in interoceptive processing and accuracy of heartbeat perception in autistic individuals.

Most autistic people experience difficulties in sensory processing, including interoceptive processing. For example, they often report subjective difficulties in the interoceptive processing of interoceptive input, such as difficulty in interpreting bodily signals, including hunger, thirst, and fatigue. However, whether these subjective interoceptive difficulties are from underlying problems in interoceptive accuracy remains unclear. This study investigated the relationship between subjective interoceptive difficulty and behavioral interoceptive accuracy in autistic adults and a control group. Subjective interoceptive accuracy was measured using an interoceptive sensitivity questionnaire, and behavioral interoceptive accuracy was measured using a heartbeat counting task. The results showed no significant relationship between subjective interoceptive difficulty and behavioral interoceptive accuracy in the autistic or control groups. This suggests that subjective interoceptive difficulty and behavioral interoceptive accuracy reflect different aspects of interoceptive processing. One possible interpretation is that autistic adults can identify individual local sensory inputs, such as heartbeats, however, they have difficulty integrating multiple inputs and recognizing internal body states such as hunger and fatigue.

Association Between Gestational Weeks, Initial Maternal Perception of Fetal Movement, and Individual Interoceptive Differences in Pregnant Women: Cross-Sectional Study.

BACKGROUND: Interoception encompasses the conscious awareness of homeostasis in the body. Given that fetal movement awareness is a component of interoception in pregnant women, the timing of initial detection of fetal movement may indicate individual differences in interoceptive sensitivity. OBJECTIVE: The aim of this study is to determine whether the association between the gestational week of initial movement awareness and interoception can be a convenient evaluation index for interoception in pregnant women. METHODS: A cross-sectional study was conducted among 32 pregnant women aged 20 years or older at 22-29 weeks of gestation with stable hemodynamics in the Obstetric Outpatient Department. Interoception was assessed using the heartbeat-counting task, with gestational weeks at the first awareness of fetal movement recorded via a questionnaire. Spearman rank correlation was used to compare the gestational weeks at the first awareness of fetal movement and heartbeat-counting task scores. RESULTS: A significant negative correlation was found between the gestational weeks at the first fetal movement awareness and heartbeat-counting task performance among all participants (r=-0.43, P=.01) and among primiparous women (r=-0.53, P=.03) but not among multiparous women. CONCLUSIONS: Individual differences in interoception appear to correlate with the differences observed in the timing of the first awareness of fetal movement.

Increasing familiarity with the heartbeat counting task does not affect performance.

BACKGROUND: Interoception is typically defined as the processing and perception of internal signals. A common evaluation of interoceptive abilities is the heartbeat counting task, during which participants count their heartbeats over a period of time. It has been argued recently, however, that performance in this task may reflect processes other than cardiac sensation. OBJECTIVE: This study aimed to: 1) observe heartbeat counting task performance changes across multiple repetitions of the task; and 2) compare performance in the heartbeat counting task with that for a visual counting task to investigate generalised propensities for how uncertain stimuli are reported. METHODS: Seventy-nine healthy participants performed seven blocks each of the heartbeat and visual counting tasks. Scores for each of the tasks were compared across blocks to identify any change in performance. Performance in the two tasks was then correlated. The study was preregistered at https://doi.org/10.17605/OSF.IO/GWAB7. RESULTS: Heartbeat counting task performance did not change over blocks. In contrast, scores for the visual counting task reduced over time. A positive correlation was seen between performance in the two tasks (ρ(79) = .27). CONCLUSION: Heartbeat counting task performance is stable across repetitions of the task, not changing with increasing familiarity. This suggests that non-interoceptive factors, such as beliefs, may be involved. The correlation between the heartbeat and visual counting tasks may point to a general propensity in counting uncertain stimuli across sensory domains. Together, these results raise questions about the interpretation of the heartbeat counting task as a measure of interoception.

Disrupted interoceptive awareness by auditory distractor: Difficulty inferring the internal bodily states?

Recent studies have associated interoceptive awareness, the perception of internal bodily sensations, with a predictive mechanism of perception across all sensory modalities. According to the framework, volitional attention plays a pivotal role in interoceptive awareness by prioritizing interoceptive sensations over exteroceptive ones. Consequently, it is hypothesized that the presence of irrelevant stimuli would disrupt the attentional modulation and interoceptive awareness, which remains untested. In this study, we investigated if interoceptive awareness is diminished by unrelated auditory distractors to validate the proposed perceptual framework. A total of 30 healthy human volunteers performed the heartbeat counting task both with and without auditory distractors. Additionally, we measured participant's psychophysiological traits related to interoception, including the high-frequency component of heart rate variability (HF-HRV) and trait interoceptive sensibility. The results showed that interoceptive accuracy, confidence, and heartbeat intensity decreased in the presence of distractor sound. Moreover, individuals with higher HF-HRV and a greater tendency to worry about bodily states experienced a more pronounced distractor effect on interoceptive awareness. These results provide support for the perceptual mechanism of interoceptive awareness in terms of the predictive process, highlighting the impact of relative precision across interoceptive and exteroceptive signals on perceptual experiences.

What counts when heartbeats are counted.

Schandry's mental heartbeat tracking task is a widely used measure of interoception, assessing heartbeat perception. We classify the factors that contribute to performance on the task as (i) trait-like characteristics, (ii) expectation-related factors, and (iii) factors showing participants' task set. We recommend conducting further research to better understand what exactly the task measures.

Does Long-Term Training in a Water Immersion Environment Change Interoception?

The aim of this study was to investigate individual interoception by comparing the responses of swimmers and baseball players when exposed to specific water environments, depending on training content and environment. Forty-eight healthy male university students were evaluated for their interoceptive response (accuracy, sensibility, and awareness) and heart rate following 25 min of water immersion (WI) at 35 °C. We assessed three conditions: pre-WI, during WI, and post-WI. The results indicated that interoceptive accuracy (IAcc) did not differ between groups because both swimming and baseball do not require emotional expression, as opposed to an activity such as dance. The heart rate was significantly decreased at post-WI compared to that at pre-WI. The IAcc of post-WI presented as higher than that of pre-WI. In addition, there was a significant negative correlation between the ratio of IAcc and that of HR among subjects. Moreover, the attention regulation subscale of the MAIA changed in the WI environment and the ratio of IAcc was negatively correlated with that of the not-distracting subscale of the MAIA. These results suggested that interoception did not differ among the athletes who had long-term training, which enabled them to acquire multi-modal sensorimotor integration, compared to that of non-athlete control participants. We conclude that interoception did not differ among athletes who had long-term training compared to that of non-athlete control participants.

Measuring interoception: The phase adjustment task.

Interoception, perception of one's bodily state, has been associated with mental health and socio-emotional processes. However, several interoception tasks are of questionable validity, meaning associations between interoception and other variables require confirmation with new measures. Here we describe the novel, smartphone-based Phase Adjustment Task (PAT). Tones are presented at the participant's heart rate, but out of phase with heartbeats. Participants adjust the phase relationship between tones and heartbeats until they are synchronous. Data from 124 participants indicates variance in performance across participants which is not affected by physiological or strategic confounds. Associations between interoception and anxiety, depression and stress were not significant. Weak associations between interoception and mental health variables may be a consequence of testing a non-clinical sample. A second study revealed PAT performance to be moderately stable over one week, consistent with state effects on interoception.

The effect of haptic stimulation simulating heartbeats on the regulation of physiological responses and prosocial behavior under stress: The influence of interoceptive accuracy.

Research has discovered the modulatory effect of peripheral stimulation simulating altered bodily signals on emotion. Whether such an effect varies depending on one's interoceptive accuracy (IAc) remains unclear. Therefore, we provided haptic stimulation simulating participants' slowed-down heartbeats or no stimulation while they engaged in socially stressful tasks to examine whether participants reacted differently depending on their IAc. Results showed that haptic stimulation exhibited the opposite effect on participants with different levels of IAc for both heart rate and heart rate variability (HRV). When receiving the stimulation, participants with higher IAc showed less increased heart rate and more elevated HF than participants with lower IAc. In contrast, in the absence of stimulation, an opposite pattern of response depending on participants' IAc was observed. The modulatory effect of stimuli and IAc on prosocial behavior was not significant. Individual differences in IAc were shown to affect how one perceives/responds to altered bodily signals.

Contribution of Time Estimation and Knowledge to Heartbeat Counting Task Performance under Original and Adapted Instructions.

Interoceptive accuracy is frequently assessed using the Heartbeat Counting Task (HCT), requiring participants to count the number of times their heart beats. The HCT validity has been questioned, as participants may perform the task by estimating, rather than counting, their felt heartbeats. Participants could estimate the time or use their knowledge of their heart rate. Some research ruled out the contribution of time estimation in HCT performance. However, we believe these studies relied on a problematic analytic rationale. We revisited this question by relying on new analytic strategies, and by examining the role of estimation in HCT performance, while varying task instructions. The findings support the role of time and knowledge-based estimations under original instructions. They also highlight the critical impact of instructions on HCT validity. Given the many limitations of the HCT, we urge researchers to test the robustness of published effects and to reconsider the interpretation of replicable results.

Comment on "Zamariola et al. (2018), Interoceptive Accuracy Scores are Problematic: Evidence from Simple Bivariate Correlations"-The empirical data base, the conceptual reasoning and the analysis behind this statement are misconceived and do not support the authors' conclusions.

A recent paper by Zamariola and colleagues is widely cited as an authority on the invalidity of the Heartbeat Counting Task as a measure of interoceptive accuracy. Given the widespread interest in this field, it is essential that papers about methods are conceptually sound. However, only one of the authors' four criticisms appears substantiated - that people count too few heartbeats. Their arguments about "simple bivariate correlations" and their finding that interoceptive accuracy and heart rate correlate, depend on 'spurious correlations' arising from the overlooked point that interoceptive accuracy is a ratio. Moreover, scrutiny of the authors' data shows that their fourth criticism (that interoceptive accuracy is lower on longer trials) is confounded by differences in mean heart rate between trials. We present data from our own labs to refute it. We draw the authors' and editors' attention to these issues and trust that they will reconsider these erroneous conclusions.

Individual Differences in Interoceptive Accuracy Are Correlated With Salience Network Connectivity in Older Adults.

Interoceptive accuracy refers to the ability to consciously perceive the physical condition of the inner body, including one's heartbeat. In younger adults, interoceptive accuracy is correlated with insular and orbitofrontal cortical connectivity within the salience network (SN). As interoceptive accuracy and insular cortex volume are known to decrease with aging, we aimed to evaluate the correlation between SN connectivity and interoceptive accuracy in older adults. 27 older adults (mean age, 77.29 years, SD = 6.24; 19 female) underwent resting-state functional magnetic resonance imaging, followed by a heartbeat counting task and neuropsychological test. We evaluated the correlation between interoceptive accuracy and SN connectivity with age, sex, cognitive function, and total gray matter volume as covariates. Region of interest-to-region of interest analyses showed that interoceptive accuracy was positively correlated with the functional connectivity (FC) of the left rostral prefrontal cortex with the right insular, right orbitofrontal, and anterior cingulate cortices [F(6,16) = 4.52, false discovery rate (FDR)-corrected p < 0.05]. Moreover, interoceptive accuracy was negatively correlated to the FC of the left anterior insular cortex with right intra-calcarine and visual medial cortices (F(6,16) = 2.04, FDR-corrected p < 0.10). These findings suggest that coordination between systems, with a positive correlation between left rostral prefrontal cortex and the SN and a negative correlation between left insular cortex and vision-related exteroceptive brain regions, is important for maintaining interoceptive accuracy in older adults.

Modulating interoception by insula stimulation: A double-blinded tDCS study.

Interoception consists in the perception and processing of internal body signals, such as heartbeat. Previous neuroimaging studies revealed that attention to heartbeat activated bilateral insula and premotor regions. In the present double-blind study, we aimed at testing the role of insula in interoception by means of transcranial direct current stimulation (tDCS) interfering with its activity. Sixteen healthy participants responded to a questionnaire to evaluate the tendency to be internally focused and performed a heartbeat counting task before and after tDCS in three sessions (left insula stimulation, right insula stimulation, sham stimulation). Real and reported heartbeat were recorded and used to calculate the accuracy scores. A significant interaction between stimulation condition and time (pre- and post-stimulation) was found due to a significant improvement of the interoceptive accuracy in the sham condition only. Our results demonstrated that stimulation over the insula reduced the possibility to improve the precision with which individuals detect internal signals.

Interoceptive accuracy scores from the heartbeat counting task are problematic: Evidence from simple bivariate correlations.

Interoception, the capacity to perceive internal bodily states, is thought to influence cognitive, affective and interpersonal functioning. It is frequently assessed using the heartbeat counting task, introduced recently in interoceptive research. In this task participants are requested to count their heartbeats without relying on external cues. Interoceptive Accuracy (i.e., IAcc) scores are then computed based on absolute comparisons between actual and reported heartbeats. In a large sample of participants (N = 572), we observed that, whereas IAcc scores are meant to be theoretically agnostic to error type (i.e., over- or underestimation of heartbeats), these scores massively (i.e., > 95%) reflect under-reports. Of concern too, the correlation between actual and reported heartbeats is low overall (r = .16), varies non-linearly across IAcc score quantiles, and suggests undistinguishable interoceptive capacities within the top 60% IAcc scorers. We also found that IAcc scores, which are conceptually independent from actual heart rates, are structurally bound to them. Finally, we show that IAcc scores vary across the time intervals used in the task. We encourage researchers using this score for studying cognitive and emotional processes to reconsider its meaning.