Heartbeat-evoked potential and ongoing brain dynamics during interoceptive and exteroceptive information processing predict attentional focus

Abstract

Attention shapes our consciousness content and perception by increasing the probability of becoming aware and, or, better encode a selection of the incoming inner or outer sensory world. We designed a task to engage interoceptive and exteroceptive attention by orienting healthy participants to their heartbeats or auditory stimuli and investigated whether brain dynamics (Kolmogorov complexity - KC, permutation entropy - PE, weighted symbolic mutual information - wSMI, power spectrum density - PSD) and the heartbeat-evoked potential (HEP) distinguished interoceptive from exteroceptive covert attention. Exteroceptive attention yielded an overall flattening of the PSD, whereas during interoceptive attention there was a decrease in complexity, an increase in frontal connectivity and oscillations in the theta range, and a modulation of the HEP. Subject-level classifiers based on HEP features classified the attentional state of 17/20 participants. KC, PE, and wSMI showed comparable accuracy in classifying exteroceptive-interoceptive attention and exhibited a synergic behavior with the HEP features. PSD features demonstrated exceptional performance (20/20). Command-following was assessed in 5 brain-injured patients with a modified version of the task. An Unresponsive Wakefulness Syndrome/Vegetative State patient and a locked-in syndrome patient demonstrated a willful modulation of the HEP and the patient-level classifiers suggest that patients were complying with task instructions. Our findings show that directing attention to bodily rhythms or external stimuli elicits distinct neural responses that can be employed to track covert attention at the individual level. Importantly, the brain markers studied in this work provide multiple layers to explore information processing in disorders of conscious patients. Significance statementWe show that directing attention to bodily rhythms or external stimuli induces specific neural responses, allowing for individual-level tracking of covert attention in healthy participants. The time-locked and dynamical brain markers identified as relevant to distinguish between interoceptive-exteroceptive attention were further assessed in a small cohort of brain-injured patients as an EEG proxy of command-following. We show for the first time the willful modulation of the HEP in an UWS/VS patient and a locked-in syndrome patient, along with significant classification accuracies when combining the explored features. Importantly, the brain markers studied in this work provide multiple layers to explore information processing in disorders of conscious patients, and expand the framework of heart-brain interactions employed for diagnostic purposes.