Cardiac signals inform auditory regularity processing in the absence of consciousness

Article Article scientifique Article Cardiac signals inform auditory regularity processing in the absence of consciousness eng 2025-05-12 2025-05-20 author Pelentritou Andria Brain-Body and Consciousness Laboratory, Department of Clinical Neuroscience, Lausanne University Hospital, University of Lausanne, Lausanne 1011, Switzerland. 405456 author Pfeiffer Christian Vice-Presidency for Personnel Development and Leadership, Federal Institute of Technology Zurich, Zurich 8050, Switzerland. author Iten Manuela 0000-0002-0140-2066 Department of Intensive Care Medicine, Inselspital, Bern University Hospital, University of Bern, Bern 3010, Switzerland. author Haenggi Matthias Institute of Intensive Care Medicine, Zurich University Hospital, Zurich 8091, Switzerland. author Zubler Frédéric Alexis Rudolf 0000-0003-0090-7297 Department of Neurology, Spitalzentrum Biel, University of Bern, Biel 2502, Switzerland. 89355 author Schwartz Sophie 0000-0001-7718-4053 Department of Neuroscience, Faculty of Medicine, University of Geneva, Geneva 1211, Switzerland.,Swiss Center for Affective Sciences, University of Geneva, Geneva 1202, Switzerland. 35633 Département de neurosciences fondamentales (NEUFO) author De Lucia Marzia 0000-0001-8792-7885 Brain-Body and Consciousness Laboratory, Department of Clinical Neuroscience, Lausanne University Hospital, University of Lausanne, Lausanne 1011, Switzerland.,Center for Biomedical Imaging, Lausanne 1011, Switzerland. e2505454122 10.1073/pnas.2505454122 40354541 0027-8424 PMC12107109 https://pnas.org/doi/10.1073/pnas.2505454122 In healthy awake individuals, the neural processing of bodily signals is not only essential for survival but can also influence perception and compete with external stimulus processing. Yet, the mechanism underlying this bidirectional processing of bodily and external stimuli, as well as its persistence or modulation in unconscious states, remains largely unknown. Here, we investigated the role of cardiac activity on auditory regularity processing in coma. We recorded continuous electroencephalography and electrocardiography in 48 comatose patients on the first day after cardiac arrest during a closed-loop auditory paradigm. We tested whether sounds presented in synchrony with the ongoing heartbeat and sounds presented with fixed, isochronous intervals, would facilitate auditory processing, compared to an asynchronous sequence with variable heartbeat-to-sound and sound-to-sound intervals and a baseline without auditory stimulation. To assess sound prediction based on sequence regularity, we introduced sound omissions within the sequences, violating expected auditory patterns. In coma survivors only, the neural omission response differed in the synchronous against both control conditions. These results were corroborated by a multivariate decoding analysis of the single-trial neural responses to the synchronous omissions and baseline wherein survivors exhibited a higher degree of cardio-audio regularity encoding compared to nonsurvivors. Furthermore, omissions within the synchronous sequence elicited a heart rate deceleration exclusively in coma survivors, which was predictive of patient outcome. We show that the unconscious human brain infers on the temporal relationship across cardiac and auditory inputs and that the neural and cardiac correlates of cardio-audio regularity encoding are predictive of patient outcome. EEG HEP Auditory processing Coma Interoception Dewey 128.37 Dewey 616.8 Swiss National Science Foundation The impact of heartbeat signals on auditory regularity processing in humans 212981 CH 53 Département de neurosciences fondamentales 21A 16 Centre interfacultaire de neurosciences 0D9 15 Centre interfacultaire en sciences affectives 0D8 false 495 Neuroimagerie du Sommeil et de la Cognition 832 https://github.com/DNC-EEG-platform/CardioAudio_Coma Proceedings of the National Academy of Sciences of the United States of America 122 20 56a0054d-ff08-41f3-8d72-a17ba986250d Article (Published version) Public pelentritou-et-al-2025-PNAS.pdf 2404020 application/pdf CC BY-NC-ND-4.0 a8cc5bd19d79076bccce57cae9e6ea45774d6a04961734b2b81a38df271d2004 e7a62a9d-226a-47c4-ae9a-067469955648 Supplemental data Public pnas.2505454122.sapp.pdf 1505378 application/pdf 413904a5f0813e1e0f4102f0cf291a8e6efcbd83118e033cbbc9123ce174e511 openAccess Faculté de médecine / Section de médecine fondamentale / Département de neurosciences fondamentales Centres et instituts / Centre interfacultaire de neurosciences Centres et instituts / Centre interfacultaire en sciences affectives

Title	Published in	Access level	OA Policy	Year	Views	Downloads

Cardiac signals inform auditory regularity processing in the absence of consciousness	Proceedings of the National Academy of Sciences of the United States of America			2025	12	1,333

Archive ouverte UNIGE

Zubler, Frédéric Alexis Rudolf