Confounding effects of heart rate, breathing rate, and frontal fNIRS on interoception

Abstract

Recent studies have established that cardiac and respiratory phases can modulate perception and related neural dynamics. While heart rate and respiratory sinus arrhythmia possibly affect interoception biomarkers, such as heartbeat-evoked potentials, the relative changes in heart rate and cardiorespiratory dynamics in interoceptive processes have not yet been investigated. In this study, we investigated the variation in heart and breathing rates, as well as higher functional dynamics including cardiorespiratory correlation and frontal hemodynamics measured with fNIRS, during a heartbeat counting task. To further investigate the functional physiology linked to changes in vagal activity caused by specific breathing rates, we performed the heartbeat counting task together with a controlled breathing rate task. The results demonstrate that focusing on heartbeats decreases breathing and heart rates in comparison, which may be part of the physiological mechanisms related to "listening" to the heart, the focus of attention, and self-awareness. Focusing on heartbeats was also observed to increase frontal connectivity, supporting the role of frontal structures in the neural monitoring of visceral inputs. However, cardiorespiratory correlation is affected by both heartbeats counting and controlled breathing tasks. Based on these results, we concluded that variations in heart and breathing rates are confounding factors in the assessment of interoceptive abilities and relative fluctuations in breathing and heart rates should be considered to be a mode of covariate measurement of interoceptive processes.

Figure 1

(A) Brite 23 (Artinis Medical Systems B.V., the Netherlands), the fNIRS system used in the experimental protocol. (B) Experimental protocol: heartbeat counting task and breathing control task. (C) Detailed transition during the breathing control task. (D) Estimation of heart and breathing rates.

Figure 2

Average heart rate, breathing rate, and heart/breathing rate ratio during the experimental conditions.

Figure 3

Respiratory modulations induced on heart rate. (A) Group median + MAD representing relative change in heart and breathing rates, triggered by the transition from the performance to the cessation of focusing on heartbeats. Heart rate data were smoothed using a 10-s moving mean window and a sample step of 1. Each subject data corresponded to an average over six trials. (B) Relative change in heart (group median + MAD) and breathing rates during slower-to-faster and faster-to-slower transitions. Each subject data corresponded to the average over the two trials for each transition. All signals represent the group median ± median absolute deviation. All signals used for computing the medians were the rates expressed in Hz, the z-score was normalized per subject over a window of − 50 to 50 s with respect to each transition in breathing rate.

Figure 4

(A) Cardiorespiratory correlation lag, and the relationships between (B) cardiorespiratory coupling and heartbeat counting accuracy, (C) cardiorespiratory correlation and self-confidence regarding heartbeat counting, and (D) heartbeat counting accuracy and self-confidence regarding heartbeat detection.

Figure 5

Frontal hemodynamics results. (A) Changes in connectivity induced by the cessation of focusing on heartbeats. (B) Changes in connectivity induced by switching the breathing rate in the breathing rate control task. (C) Changes in the respiratory response in fNIRS with respect to changes in breathing rhythm. Thick white channels indicate significance corrected for multiple comparisons. (D) Exemplary fNIRS signals for one trial of the heartbeats counting and breathing control tasks.