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NeuroImageNeurosciencePeer-reviewed journal article

Cardio-respiratory interactions in interoceptive perception: The role of heartbeat-modulated cortical oscillations

Andrea ZaccaroiD, Francesca della PennaiD, Francesco BubbicoiD, Başak BAYRAMiD, Eleonora ParrottaiD, Mauro Gianni PerrucciiD, Marcello CostantiniiD, Francesca FerriiD

PDFDOIPreprint

Abstract

The cardiovascular and respiratory systems are anatomically and functionally integrated within the cardio-respiratory system. This close connection suggests that breathing continuously shapes cardiac interoceptive perception. Previously, we demonstrated cardio-respiratory interoceptive interactions in the heartbeat-evoked potential, a neural marker of cortical processing of cardiac signals. Specifically, we observed enhanced late heartbeat-evoked potential positivity and greater interoceptive accuracy during exhalation compared to inhalation in participants engaged in cardiac interoceptive tasks. Here, we extended these findings to the time-frequency domain by reanalysing our previous dataset. We investigated heartbeat-modulated cortical oscillations, examining power, inter-trial coherence, and functional connectivity across the respiratory cycle at rest, during a cardiac interoceptive task (heartbeat counting), and an exteroceptive control task (cardiac-tone counting). Results revealed that during the heartbeat counting task, late heartbeat-related power, inter-trial coherence, and functional connectivity increased during exhalation compared to inhalation, particularly in the alpha and theta frequency bands. These effects were primarily localized to right fronto-centro-parietal electrodes. Furthermore, we identified interactive relationships between heartbeat-evoked potential and heartbeat-modulated cortical oscillations in the alpha band that predicted interoceptive accuracy. These relationships were independent of cardiac physiology and were absent in the exteroceptive task. We proposed a model of cardio-respiratory interactions within the framework of interoceptive predictive coding, suggesting that these interactions occur at multiple levels of the interoceptive hierarchy: peripheral, brainstem, and cortical. Our interpretation highlights the role of heartbeat-related alpha-band modulations in enhancing the precision-weighting of cardiac prediction errors, thereby facilitating attentional allocation to interoceptive signals and the suppression of task-irrelevant distractors, particularly during exhalation.

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Andrea Zaccaro, Mauro Gianni Perrucci, Eleonora Parrotta+2 more·NeuroImage·Aug 11, 2022· 69 citations