The relationship between heart and brain has intrigued not only poets and artists across centuries, but also researchers for the past two decades, with even a specific branch of medicine taking the name of neurocardiology (van der Wall, 2011). In the field of psychophysiology, Thayer and Lane have long proposed the existence of a neurovisceral integration model (Thayer and Lane, 2000), derived from the seminal work of Claude Bernard in the late 1800s (Bernard, 1867). From an anatomical and functional point of view, this model is based on the activity of structures such as the Central Autonomic Network (CAN), a key part of an internal regulatory system that allows the brain to manage visceromotor, neuroendocrine, and behavioral responses that are essential for goal-oriented behavior and adaptability (Benarroch, 1993). The structural bases of the CAN include the anterior cingulate, insular, and ventromedial prefrontal cortices, the central nucleus of the amygdala, the paraventricular and related nuclei of the hypothalamus, the periaqueductal gray matter, the parabrachial nucleus, the nucleus of the solitary tract (NTS), the nucleus ambiguus, the ventrolateral medulla, the ventromedial medulla, and the medullary tegmental field. Its primary output is mediated through the preganglionic sympathetic and parasympathetic neurons, which in turn innervate the heart via the stellate ganglia and the vagus nerve. Consequently, the output of the CAN is directly linked to Heart Rate Variability (HRV). Another important characteristic of this integrated system is the fact that sensory information from organs such as the heart are connected back to the CAN in a feedback loop, for example via the baroreceptor reflex, making communication between heart and brain not only top-down, but also bottom-up. In addition, the authors assert that this model may be crucial in explaining the relationship between cognitive processes and emotional ones, such as self-regulation, especially in the context of disorders in which emotional control is hindered (Thayer and Lane, 2000). More in detail, Cattaneo et al. (2021) recently published a review in which they listed findings pertaining to the relationship between heart rate variability, emotion dysregulation and executive control. Additional support for this comes from studies that found that people suffering from disorders such as Borderline Personality Disorder (BPD) exhibit lower resting vagal tone as compared with healthy controls (Ramesh et al., 2023; Koenig et al., 2016). Notably, these findings on the clinical correlates of low HRV were also confirmed in individuals with high levels of impulsivity and suffering from psychiatric disorders in general (Appelhans and Luecken, 2006; Thayer et al., 2012; Pinna and Edwards, 2020). More generally, the literature on large samples of psychiatric patients showed that most severe disorders exhibit at rest higher Heart Rates (HR, indexing greater distress vulnerability) compared with healthy controls (Latvala et al., 2016; Critchley et al., 2019).

Emotion dysregulation is a complex, multidimensional construct that has often been considered a transdiagnostic marker of disordered psychological functioning (Beauchaine et al., 2007). Concerning the psychophysiology of emotion dysregulation, the vast majority of studies in literature takes into account what can be considered the most representative personality disorder centered around emotion dysregulation as the main key symptom, which is BPD (American Psychiatric Association, 2013). Specifically, studies have reported a decreased activation in prefrontal regions in patients with BPD, both during emotional processing (Schulze et al., 2019) and when they were explicitly instructed to reduce their responses to emotion-triggering stimuli (Schulze et al., 2011). Additionally, individuals with BPD have demonstrated impaired activation of the ventrolateral and dorsolateral prefrontal cortices (vlPFC and dlPFC) when trying to use psychological distancing as a strategy for regulating negative emotions (Koenigsberg et al., 2009). Other research indicated that the dorsal anterior cingulate cortex (dACC) is deactivated during reappraisal tasks in BPD patients (Koenigsberg et al., 2009; Schulze et al., 2011; Lang et al., 2012; van Zutphen et al., 2018). These findings support the notion that, in BPD, difficulties returning to a baseline state following emotional stimuli can be at least partly due to an inadequate regulation from inhibitory brain regions (Neacsiu et al., 2015). When considering the psychophysiological characterization of emotion dysregulation as a subclinical feature, to the best of our knowledge the literature is almost absent. We had previously addressed this literature-gap in a 2022 paper (Fusina et al., 2022) in which we adopted an innovative approach based on source-localized resting state EEG data, to perform a seed-based functional connectivity analysis, in two groups of young women, one with high (HD) and one with low (LD) emotion dysregulation traits. In particular, we focused on Ventral Attention Network (VAN) connectivity due to its relevance in the orienting of attention towards salient stimuli, especially those concerning strong emotional content. The VAN includes the right inferior frontal gyrus (rIFG) and the right temporo-parietal junction (rTPJ) (Samogin et al., 2020), it is the cortical portion of a larger network including deeper structures that comprise the right insula and the right medial temporal regions which include hippocampus and the amygdala. For this reason the VAN is related to an increased elaboration/attention of biologically-emotionally salient stimuli (ElShafei et al., 2020) and their integration with information from the internal state of viscera (interoception) (Fusina et al., 2022). We analyzed activity in the Alpha (8–13 Hz) and Gamma (30–50 Hz) bands and found higher levels of inter- and intra-network VAN connectivity in the high as compared with the low dysregulation group. In particular, we found that Gamma band power in the VAN yielded a positive correlation with measures of emotion dysregulation in the HD group only (Fusina et al., 2022). This represented the first step aimed at analyzing the psychophysiology of emotional dysregulation at a trait level, to better characterize its profile while avoiding the confounding factors commonly found in clinical samples, particularly those related to pharmacological treatment.

Notably, the possibility of performing brain functional connectivity analyses at the source level, has opened the way for investigating brain function in a novel fashion (Marino and Mantini, 2024), by combining an excellent temporal resolution and rich spectral content with a relatively good spatial resolution. Indeed, EEG offers a direct measurement of neural activity with high temporal resolution (in milliseconds) by capturing scalp potentials in real time (Ahmad et al., 2015). EEG is easy to use, silent, cost-effective, and portable, providing high flexibility for various experimental designs and conditions (Glover, 2011). Thus, EEG enhances ecological validity of research, as participants typically are recorded in a comfortable posture, that is, sitting upright in front of a computer screen during EEG recordings (e.g., Spironelli and Angrilli, 2017).

To probe the brain-heart interaction from a psychophysiological perspective, many studies have focused on the relationship between heart rate variability and various neural measures. For example, EEG-derived measures, such as band power time series (Pardo-Rodriguez et al., 2021), power spectral density (Attar et al., 2021), and coherence (Alba et al., 2019) were employed to investigate the brain-heart axis and its relationship with behavior. This has also extended to brain functional connectivity analysis, by means of fMRI (Chang et al., 2013; Colenbier et al., 2022), to identify how heart rate variability was linked to the fluctuations of resting activity in specific brain regions. Other studies also focused on heart rate instead of heart rate variability (Umeno et al., 2003). Indeed, Carr and colleagues pointed out in their review that the use of many HR-related measures could be a potential confound when interpreting findings regarding HRV alterations in clinical populations such as BPD patients (Carr et al., 2018), thus heart rate measured at rest might represent a more direct measure of emotional instability and reactivity in psychiatric populations (Latvala et al., 2016; Critchley et al., 2019).

In this framework, the present research focuses on the investigation of the relationship between brain functional connectivity and heart rate in a population of healthy young women with variable traits of emotion dysregulation. Starting from our past study (Fusina et al., 2022) which analysed brain connectivity during resting state in two groups of selected students, here we focused on Alpha and Gamma EEG bands and VAN as a main hub deserving investigation during emotional stimulation. We interpreted the observed greater between and within-VAN connectivity in high dysregulated participants during resting state as due to their greater attention to visceral emotional responses (Fusina et al., 2022). The Gamma band is particularly effective in the measure of functional connectivity during tasks (Jensen et al., 2007; Womelsdorf and Fries, 2007), thus given the importance of HR in the visceral response, we expected the large observed VAN connectivity to be significantly correlated with HR during a variety of emotional ecological stimulation with standardized film clips.

We enrolled a sample of only women for several reasons: first, due to the well known gender differences in emotional responses (Bradley et al., 2001; Bianchin and Angrilli, 2012) we aimed to reduce sample variance in emotional response in order to focus individual differences especially on emotion dysregulation dimension. Second, the disorders characterized primarily by emotion dysregulation symptoms (such as BPD) affect far more frequently women than men (American Psychiatric Association, 2013). Knowing that Heart Rate (HR) itself may represent an index of emotional reactivity when high (Palomba et al., 2000) or emotional pathological coldness when low (Latvala et al., 2015), we expected that high dysregulation individuals would have exhibited high HR correlated with greater VAN intra- and inter-connectivity. To test the hypothesis we administered participants an ecological emotion stimulation task consisting in the viewing of video clips belonging to different emotional categories. Past research investigated brain connectivity by means of film clips classified in 8 specific emotional categories and using an EEG brain connectivity approach based on graph analysis (Aydın, 2023; Kılıç and Aydın, 2022). This started new innovative research lines investigating the effects of emotions on functional brain connectivity. In the present study we further added to current limited research by investigating the interaction between brain and heart during emotional stimulation. We hypothesized that Gamma band connectivity would positively correlate with heart rate in the high dysregulation group, especially to emotional and high arousal clips. Most importantly, we performed this investigation using state-of-the-art EEG tools to estimate functional connectivity within the brain using a neurophysiological, rather than a neuroimaging, technique. In this study, therefore, we aimed to expand our knowledge on the psychophysiology of emotion dysregulation by focusing not only on the neural features, but also on their relationship with heart-related metrics. In particular, we extracted seed-based functional connectivity values from source-reconstructed EEG data (Samogin et al., 2019) and we assessed the brain-heart interaction in the same population of healthy women with different levels of trait emotion dysregulation that was considered in our previous research (Fusina et al., 2022). Seed-based functional connectivity was used starting from source-reconstructed brain signals. In particular, for each seed, frequency-specific connectivity values were computed by performing a time-frequency decomposition on the neural signals, yielding power envelopes for each frequency. The correlation of band-limited power envelopes, with correction for zero-lag effects (i.e., signal orthogonalization) represented the extracted connectivity metric (Taberna et al., 2024). In this context, we used this approach to assess the correlation between heart rate and brain functional connectivity, with special interest in the Ventral Attention Network activity in the Gamma band with the Alpha band used as a control measure.

The objective of the present study was to evaluate the relationship between heart rate and brain functional connectivity, with a particular focus on the Ventral Attention Network (VAN) in the Gamma band, during an ecological emotion stimulation task in two groups of women with high and low levels of emotion dysregulation. The VAN plays a key role in the automatic redirection of attention towards emotional stimuli, which can ultimately disrupt top-down control that would require the individual to focus on different tasks (Iaria et al., 2008; Frank and Sabatinelli, 2012). Our previous findings (Fusina et al., 2022) point to the fact that an intensified focus on internal emotional experiences, particularly when they are negative, may be associated with heightened connectivity between the VAN and other resting-state networks (RSNs). This is particularly important for individuals who struggle with effectively regulating their emotional responses. Indeed, Gamma activity in the VAN has been found to increase during bottom-up attentional control in response to distracting stimuli (ElShafei et al., 2020), and similar patterns have been observed in the primate brain when attention is captured by external stimuli (Buschman and Miller, 2007). Additionally, the Gamma band has been shown to facilitate communication among task-relevant neural nodes (Jensen et al., 2007; Womelsdorf and Fries, 2007). We hypothesized that this increased connectivity in HD, given the greater attention oriented towards their own visceral responses, would have been linked/correlated with cardiovascular reactivity to emotional clips. HR showed an overall emotion-dependent pattern in both groups, with lower HR to Erotic, Sadness and Compassion compared with Scenery, Neutral and Fear. The lower HR during Erotic compared to Neutral clips is well known in the literature on emotions as it marks an increased attention (stimulus intake bradycardia) to biologically salient stimuli (Bianchin and Angrilli, 2012), similarly holds for Sadness and Compassion. The relatively greater HR to Fear compared to the other moderately unpleasant stimuli can be interpreted as due to defense parasympathetic response typically characterized by HR relative acceleration. While the two groups did not differ in this pattern, the HD group nevertheless exhibited overall greater HR with respect to the LD group (+1.67 Bpm). This effect was weak as measured by Cohen’s d (d = 0.18) because of the small sample size, but it is in line with the literature on larger samples, showing that most psychiatric disorders exhibit higher heart rates (indexing greater distress/cardiovascular reactivity) compared with healthy controls (Latvala et al., 2016; Critchley et al., 2019). Taking into account that our HD sample had high traits of emotion dysregulation, with significant greater symptoms of anxiety and depression, the HR found in Emotion Unstable/BPD and Mixed Anxiety/Depression patients by Critchley et al., (2019) was of about the same extent (+1.69 bpm). Thus, this increased HR is a cardiovascular measure that is weakly but significantly associated with psychopathology.

We hypothesized that Gamma band connectivity would have shown a positive correlation with heart rate in the high dysregulation group: namely, greater VAN intra- and inter-connectivity was expected to be correlated with higher HR. This hypothesis was supported both by findings from our prior study (Fusina et al., 2022), in which we found positive correlations between Gamma band activity in the VAN and measures of emotion dysregulation, and by the literature suggesting a co-occurring increase in both Gamma EEG activity and HR during stressful situations, such as, for example, mental arithmetic tasks, with Gamma EEG increase predicting autonomic activation (Umeno et al., 2003). Since we found greater Gamma band VAN connectivity at rest in the HD group as compared to the LD group, and we attributed this to the HD group being generally more focused on their internal emotional experience (Fusina et al., 2022), we expected to replicate these findings also during an ecological emotion stimulation task. In line with our hypothesis, we found a significant positive correlation of Gamma connectivity within the VAN with HR that was higher in the HD group compared with the LD group, especially during the exposure to low-arousal emotions such as those induced in Scenery, Neutral and Sadness clips. In these participants, HR increase also correlated with VAN connectivity of the other resting-state networks, suggesting a global recruitment of attention resources towards their own visceral emotional responses, and this process involved also different brain areas typically not involved in attentive processes. It is noteworthy that the highest correlations between Gamma connectivity in the VAN and HR was found for clips depicting Sadness. This correlation, in addition to being the strongest, was also found when analyzing the interaction between the VAN and all the other networks considered (except for the DAN). Indeed, while it is true that Sadness clips were characterized by low arousal levels, they may also have been especially touched the HD group characterized by greater significant depressive and anxious symptoms compared with the LD group (Fusina et al., 2022). These clips show individuals being alone in scenes of desolation; loneliness has been shown to predict social anxiety, with emotion dysregulation mediating the effect (Eres et al., 2023), and emotion dysregulation levels have been found to partially mediate the longitudinal relationship between loneliness and both depression and stress (Velotti et al., 2021). While for Neutral and Scenery clips, which may have been perceived as more boring – thus possibly triggering a heightened focus on a subjective emotional experience – the positive correlation between Gamma band connectivity in the VAN and HR may retrace the same mechanism that we found during resting state. This suggests that for Sadness clips a different pathway may be involved, but additional studies will be needed to further probe this possibility. The fact that a high HR-Gamma connectivity correlation was not found to other highly arousing unpleasant clips, such as the Fear ones, might be related to low variance in the data for this condition, to physiological response saturation to the most activating emotional stimuli or to the possibility that Sadness (implying social isolation, helplessness, abandonment) represents the most sensitive and salient emotional context triggering emotional worrying in HD women. We think the main agent of this effect is the specificity of sadness clips for HD women. It is also possible that, since in women compared to men, for extreme unpleasant stimuli such as fear, arousal ratings show a ceiling compression effect and a reduction of inter-individual differences (Bradley et al., 2001), this might have reduced both the variance and the size of the correlations.

Concerning the EEG Alpha band, which we considered to represent the control condition, the only significant correlation between HR and VAN connectivity in the LD group was found for Erotic movies, and was in the opposite direction with respect to HD group: while the correlation HR-connectivity in LD was significantly negative (VAN, VAN-LN, VAN-DMN, VAN-DAN) in the HD was positive (VAN-DAN, VAN-SMN). This means that in the Low Dysregulation group HR decreases were associated to Alpha connectivity increases when considering neural communication between VAN nodes and those belonging to the Dorsal Attention, Default Mode and Language Networks. The interpretation of this result is more straightforward, and suggests an attentive effect represented by HR deceleration, stimulus intake, greater orienting of attention to the highly arousing and appetitive content of Erotic clips in the LD group. Our past work evidenced a clear HR deceleration indexing automatic orienting of attention to Erotic stimuli in healthy women (Bianchin and Angrilli, 2012). Instead, in the HD group, increased connectivity in VAN-DAN and VAN-SMN was correlated with higher HR, indexing cardiovascular/sympathetic activation, which is a results opposite to that observed in the LD group. The literature suggests that emotion dysregulation is related to sexual difficulties and dissatisfaction, which points to the fact that Erotic stimuli in particular may elicit a disrupted response in people with problems in regulating their emotions (Fischer et al., 2022). Indeed, our sample showed an interesting effect in line with the above cited literature, in the evaluation of Erotic movies the level of Embarrassment was significantly higher in the HD compared to the LD group (see Figure 1). These findings are especially relevant when considering possible treatment interventions in emotion dysregulation, such as HR biofeedback or neurofeedback, possibly combined with psycho-educational interventions that may teach affected individualsto effectively manage their emotions both at rest and during everyday life situations, for example by means of imagery trainings. The fact that we used movies as a method to induce emotion, which are widely considered to be among the most efficacious stimuli (Westermann et al., 1996; Romeo et al., 2022), is a strong point in our research because it brings subjects closer to real-life experiences when participating in the study, allowing for a more ecological and true-to-life psychophysiological response to take place.

Notwithstanding the innovative approach of this research both in the stimuli that were presented and in the EEG processing methods we adopted, our research is not without limitations. Firstly, as was also stated in (Fusina et al., 2022), the generated head model relied on standard anatomical and electrode positioning templates, which somewhat limited the accuracy of the source localization. Furthermore, the focus on a female-only sample, while having the advantage of allowing us to study a homogeneous sample which has the additional benefit of being especially relevant for the construct of interest (Fusina et al., 2022), is limiting because it does not allow for our findings to be generalizable to the construct of emotion dysregulation as a whole, but only for emotion dysregulation in this specific population and context. Indeed, it would be interesting to probe the same aspects also in a male-only, or better, mixed population to allow a direct comparison between genders.

Furthermore, since to the extent of our knowledge there is very limited literature on these topics, future research will be crucial both in replicating these findings, and also in expanding our understanding of the complex interplay between heart rate measures and functional brain connectivity, especially when considering emotion dysregulation at a subclinical level. Indeed, the study of transdiagnostic markers of psychopathological vulnerability is of the utmost importance when the aim is to develop a more precise and comprehensive understanding of the interplay between physiological systems and how these, in turn, interact with emotions and their regulation. Such an approach could truly enrich both the scientific validity of the theoretical framework underlying these concepts, and the clinical treatment options that may be offered both to patients and to vulnerable, but still healthy, at-risk populations.