Brain-heart interactions are optimized across the respiratory cycle via interoceptive attention

Abstract

Respiration and heartbeat continuously interact within the living organism at many different levels, representing two of the main oscillatory rhythms of the body and providing major sources of interoceptive information to the brain. Despite the modulatory effect of respiration on exteroception and cognition has been recently established in humans, its role in shaping interoceptive perception has been scarcely investigated so far.In two independent studies, we investigated the effect of spontaneous breathing on cardiac interoception by assessing the Heartbeat Evoked Potential (HEP) in healthy humans. In Study 1, we compared HEP activity for heartbeats occurred during inhalation and exhalation in 40 volunteers during resting-state. We found higher HEP amplitude during exhalations, compared to inhalations, over fronto-centro-parietal areas. This suggests increased brain-heart interactions and improved cortical processing of the heartbeats during exhalations. In Study 2, we tested the respiratory-phase dependent modulation of HEP activity in 20 volunteers during Exteroceptive and Interoceptive conditions of the Heartbeat Detection (HBD) task. In these conditions, participants were requested to tap at each heartbeat, either recorded or felt, respectively. Results showed higher HEP activity and higher detection accuracy at exhalation than inhalation in the Interoceptive condition only. These effects were positively correlated, suggesting that both cortical processing of cardiac signals and perception of heartbeats are optimized across the respiratory cycle. Direct comparisons of Interoceptive and Exteroceptive conditions confirmed stronger respiratory-phase dependent modulation of HEP and accuracy when attention was directed towards the interoceptive stimuli.We provide data showing that respiration shapes cardiac interoception at the neurophysiological and behavioural levels. Specifically, exhalation may allow attentional shift towards the internal bodily states.

Respiratory rhythms of the predictive mind.

“…With respect to tactile processing, Grund et al (2022) found that both cardiac and respiratory cycles modulated stimulus sensitivity, with hit rates being maximal at peak expiration and minimal at peak inspiration. With respect to interoception (i.e., the perception of internal, visceral sensations), Zaccaro et al (2022) investigated respiratory cycle effects on cardiac interoception and reported that heartbeat-evoked cortical potentials were maximal during exhalation versus inhalation. This was further coupled with higher heartbeat tapping accuracy, suggesting that interoceptive sensitivity may be greatest when diaphragmatic pressure increases in the chest during the respiratory baroreflex (Molle & Coste, 2022; Zaccaro et al, 2022).…”

“…With respect to interoception (i.e., the perception of internal, visceral sensations), Zaccaro et al (2022) investigated respiratory cycle effects on cardiac interoception and reported that heartbeat-evoked cortical potentials were maximal during exhalation versus inhalation. This was further coupled with higher heartbeat tapping accuracy, suggesting that interoceptive sensitivity may be greatest when diaphragmatic pressure increases in the chest during the respiratory baroreflex (Molle & Coste, 2022; Zaccaro et al, 2022). Finally, with respect to self-related processing, a study reported the existence of an “embreathment illusion” such that projecting respiratory rhythms onto a virtual avatar increased feelings of bodily awareness and immersion (Monti et al, 2020).…”