Respiration, Heartbeat, and Conscious Tactile Perception

Abstract

Previous studies have shown that timing of sensory stimulation during the cardiac cycle interacts with perception. Given the natural coupling of respiration and cardiac activity, we investigated here their joint effects on tactile perception. Forty-one healthy female and male human participants reported conscious perception of finger near-threshold electrical pulses (33% null trials) and decision confidence while electrocardiography, respiratory activity, and finger photoplethysmography were recorded. Participants adapted their respiratory cycle to expected stimulus onsets to preferentially occur during late inspiration/early expiration. This closely matched heart rate variation (sinus arrhythmia) across the respiratory cycle such that most frequent stimulation onsets occurred during the period of highest heart rate probably indicating highest alertness and cortical excitability. Tactile detection rate was highest during the first quadrant after expiration onset. Interindividually, stronger respiratory phase-locking to the task was associated with higher detection rates. Regarding the cardiac cycle, we confirmed previous findings that tactile detection rate was higher during diastole than systole and newly specified its minimum at 250-300 ms after the R-peak corresponding to the pulse wave arrival in the finger. Expectation of stimulation induced a transient heart deceleration which was more pronounced for unconfident decision ratings. Interindividually, stronger poststimulus modulations of heart rate were linked to higher detection rates. In summary, we demonstrate how tuning to the respiratory cycle and integration of respiratory-cardiac signals are used to optimize performance of a tactile detection task.

Allostasis as a core feature of hierarchical gradients in the human brain

“…Further, to the extent that interoceptive signals (as modeled by the brain) act as control signals for allostasis (Sennesh et al, 2021), those signals may also play a role in the sampling of unanticipated exteroceptive signals (i.e., exteroceptive prediction errors). This hypothesis is supported by evidence that sampling of visual, auditory, and other data from the sensory surfaces of the body is statistically related to bodily signals such as heart beats and respiration (e.g., Al et al, 2020;Aspell et al, 2013;Galvez-Pol et al, 2020;Grund et al, 2021;Kluger et al, 2021;Kunzendorf et al, 2019;Zelano et al, 2016).…”

Active tactile discrimination is coupled with and modulated by the cardiac cycle

“…Importantly, they freely initiated, held, and ended the sensing of the stimuli. From an interoceptive inference framework, studies in passive sensing have shown that tactile sensitivity is reduced during the systole phase of the cardiac cycle (Al, Iliopoulos, et al, 2021;Grund et al, 2022;Motyka et al, 2019). Hence, to avoid this drop in sensitivity, participants could circumvent the sampling of information in systole.…”

“…Psychophysiological studies and analyses of cardio-sensory processing usually involve sample sizes on the order of 30-45 participants (Al et al, 2020; Galvez-Pol et al, 2020; Grund et al, 2022; Herman & Tsakiris, 2021; Kunzendorf et al, 2019; Motyka et al, 2019). Accordingly, we recruited 50 healthy adults (32 females; age range = 18-35) who participated in the current study.…”

“…For each touch, we computed the phase of the cardiac cycle in which each tactile event occurred, as well as the concomitant consequences of such an alignment in participants' responses. From an interoceptive inference perspective, studies in passive sensing have shown that tactile sensitivity is reduced during the systole phase (Al, Iliopoulos, et al, 2021;Grund et al, 2022;Motyka et al, 2019), therefore, we predicted that participants behaviour would reflect this and would sample more in the diastole phase than systole.…”

“…Previous studies have shown that participants’ responses to stimuli vary according to the phase of the heartbeat in which exteroceptive stimuli are presented. Perceptual sensitivity to painful, visual, tactile, and auditory stimuli are typically reduced when they are presented in systole compared with diastole (Al et al, 2020; Edwards et al, 2001, 2007; Grund et al, 2022; McIntyre et al, 2006; Motyka et al, 2019; Pramme et al, 2016). It has been proposed that these cardiac-related sensory attenuation effects reflect the competing allocation of attentional resources (Berntson & Khalsa, 2021; Critchley & Garfinkel, 2018; Khalsa et al, 2018) during periods in which there are afferent signals from baroreceptors (Critchley & Harrison, 2013; Garfinkel et al, 2014).…”