Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processing

• Published in: PNAS nexus Vol. 3; no. 12; p. pgae531
• Main Authors: Fló, Emilia, Belloli, Laouen, Cabana, Álvaro, Ruyant-Belabbas, Alessia, Jodaitis, Lise, Valente, Melanie, Rohaut, Benjamin, Naccache, Lionel, Rosanova, Mario, Comanducci, Angela, Andrillon, Thomas, Sitt, Jacobo
• Format: Journal Article
• Language: English
• Published: US Oxford University Press 01.12.2024
• Subjects: Attention; Auditory stimuli; Biological, Health, and Medical Sciences; Brain; Complexity; Consciousness; External stimuli; Heart; Information processing; Medical research; Medicine, Experimental; Modulation; Neural networks; Patients; Permutations; Power spectral density; Sensory integration; Sleep and wakefulness; Theta rhythms; Wakefulness; France; Italy; disorders of consciousness; exteroception; attention; HEP; interoception
• ISSN: 2752-6542; 2752-6542
• DOI: 10.1093/pnasnexus/pgae531

Abstract Attention shapes our consciousness content and perception by increasing the probability of becoming aware and/or better encoding a selection of the incoming inner or outer sensory world. Engaging interoceptive and exteroceptive attention should elicit distinctive neural responses to visceral and external stimuli and could be useful in detecting covert command-following in unresponsive patients. We designed a task to engage healthy participants’ attention toward their heartbeats or auditory stimuli and investigated whether brain dynamics and the heartbeat-evoked potential (HEP) distinguished covert interoceptive–exteroceptive attention. Exteroceptive attention yielded an overall flattening of the power spectral density (PSD), whereas during interoception, there was a decrease in complexity, an increase in frontal connectivity and theta oscillations, and a modulation of the HEP. Subject-level classifiers based on HEP features classified the attentional state of 17/20 participants. Kolmogorov complexity, permutation entropy, and weighted symbolic mutual information showed comparable accuracy in classifying covert attention and exhibited a synergic behavior with the HEP features. PSD features demonstrated exceptional performance (20/20). Command-following was assessed in five 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 together with the explored brain markers suggest that patients were complying with task instructions. Our findings underscore the importance of attentional mechanisms in shaping interoceptive and exteroceptive sensory processing and expand the framework of heart–brain interactions employed for diagnostic purposes in patients with disorders of consciousness.