Significance: We investigate the temporal dynamics of brain and cardiac activities in healthy subjects who underwent an emotional elicitation through videos. We demonstrate that, within the first few seconds, emotional stimuli modulate heartbeat activity, which in turn stimulates an emotion intensity (arousal)–specific cortical response. The emotional processing is then sustained by a bidirectional brain–heart interplay, where the perceived arousal level modulates the amplitude of ascending heart-to-brain neural information flow. These findings may constitute fundamental knowledge linking neurophysiology and psychiatric disorders, including the link between depressive symptoms and cardiovascular disorders.
Recent experimental evidence on patients with disorders of consciousness revealed that observing brain-heart interactions helps to detect residual consciousness, even in patients with absence of behavioral signs of consciousness. Those findings support hypotheses suggesting that visceral activity is involved in the neurobiology of consciousness, and sum to the existing evidence in healthy participants in which the neural responses to heartbeats reveal perceptual and self-consciousness. More evidence obtained through mathematical modeling of physiological dynamics revealed that emotion processing is prompted by an initial modulation from ascending vagal inputs to the brain, followed by sustained bidirectional brain-heart interactions. Those findings support long-lasting hypotheses on the causal role of bodily activity in emotions, feelings, and potentially consciousness. In this paper, the theoretical landscape on the potential role of heartbeats in cognition and consciousness is reviewed, as well as the experimental evidence supporting these hypotheses. I advocate for methodological developments on the estimation of brain-heart interactions to uncover the role of cardiac inputs in the origin, levels, and contents of consciousness. The ongoing evidence depicts interactions further than the cortical responses evoked by each heartbeat, suggesting the potential presence of non-linear, complex, and bidirectional communication between brain and heartbeat dynamics. Further developments on methodologies to analyze brain-heart interactions may contribute to a better understanding of the physiological dynamics involved in homeostatic-allostatic control, cognitive functions, and consciousness.
The neural monitoring of visceral inputs might play a role in first-person perspective (i.e., the unified viewpoint of subjective experience). In healthy participants, how the brain responds to heartbeats, measured as the heartbeat-evoked response (HER), correlates with perceptual, bodily, and self-consciousness. Here we show that HERs in resting-state EEG data distinguishes between postcomatose male and female human patients (n = 68, split into training and validation samples) with the unresponsive wakefulness syndrome and in patients in a minimally conscious state with high accuracy (random forest classifier, 87% accuracy, 96% sensitivity, and 50% specificity in the validation sample). Random EEG segments not locked to heartbeats were useful to predict unconsciousness/consciousness, but HERs were more accurate, indicating that HERs provide specific information on consciousness. HERs also led to more accurate classification than heart rate variability. HER-based consciousness scores correlate with glucose metabolism in the default-mode network node located in the right superior temporal sulcus, as well as with the right ventral occipitotemporal cortex. These results were obtained when consciousness was inferred from brain glucose met`abolism measured with positron emission topography. HERs reflected the consciousness diagnosis based on brain metabolism better than the consciousness diagnosis based on behavior (Coma Recovery Scale-Revised, 77% validation accuracy). HERs thus seem to capture a capacity for consciousness that does not necessarily translate into intentional overt behavior. These results confirm the role of HERs in consciousness, offer new leads for future bedside testing, and highlight the importance of defining consciousness and its neural mechanisms independently from behavior.
The choice of EEG reference has been widely studied. However, the choice of the most appropriate re-referencing for EEG data is still debated. Moreover, the role of EEG reference in the estimation of functional Brain-Heart Interplay (BHI), together with different multivariate modelling strategies, has not been investigated yet. This study identifies the best methodology combining a proper EEG electrical reference and signal processing methods for an effective functional BHI assessment. The effects of the EEG reference among common average, mastoids average, Laplacian reference, Cz reference, and the reference electrode standardization technique (REST) were explored throughout different BHI methods including synthetic data generation (SDG) model, heartbeat-evoked potentials, heartbeat-evoked oscillations, and maximal information coefficient. The SDG model exhibited high robustness between EEG references, whereas the maximal information coefficient method exhibited a high sensitivity. The common average and REST references for EEG showed a good consistency in the between-method comparisons. Laplacian, and Cz references significantly bias a BHI measurement. The use of EEG reference based on a common average outperforms on the use of other references for consistency in estimating directed functional BHI. We do not recommend the use of EEG references based on analytical derivations as the experimental conditions may not meet the requirements of their optimal estimation, particularly in clinical settings. The use of a common average for EEG electrical reference is concluded to be the most appropriate choice for a quantitative, functional BHI assessment.
The interplay between the brain and interoceptive signals is key in maintaining internal balance and orchestrating neural dynamics, encompassing influences on perceptual and self-awareness. Central to this interplay is the differentiation between the external world, others and the self, a cornerstone in the construction of bodily self-awareness. This review synthesizes physiological and behavioral evidence illustrating how interoceptive signals can mediate or influence bodily self-awareness, by encompassing interactions with various sensory modalities. To deepen our understanding of the basis of bodily self-awareness, we propose a network physiology perspective. This approach explores complex neural computations across multiple nodes, shifting the focus from localized areas to large-scale neural networks. It examines how these networks operate in parallel with and adapt to changes in visceral activities. Within this framework, we propose to investigate physiological factors that disrupt bodily self-awareness, emphasizing the impact of interoceptive pathway disruptions, offering insights across several clinical contexts. This integrative perspective not only can enhance the accuracy of mental health assessments but also paves the way for targeted interventions.