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.
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 post-comatose male and female human patients (n=68, split into training and validation samples) suffering from the unresponsive wakefulness syndrome and patients in 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 (un)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 occipito-temporal cortex. These results were obtained when consciousness was inferred from brain glucose metabolism 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. Significance statementDetecting consciousness without relying neither on overt behavior nor on asking to mentally perform a specific task is both a fundamental issue pertaining to the nature of consciousness, and a clinical challenge. Here we show that the transient brain response elicited at each heartbeat captures residual consciousness in the resting-state EEG of post-comatose patients.The results show that brain responses to an internal bodily signal might help specify the gray zone of consciousness, i.e., the fleeting conscious feelings that are not necessarily associated with the performance of a specific task nor translate into behavioral outputs.
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