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 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. Inter-individually, 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. Metacognitive efficiency for yes- responses was also modulated across the cardiac cycle reaching an optimum at the end of diastole. Expectation of stimulation induced a transient heart deceleration which was more pronounced for unconfident decision ratings. Inter-individually, stronger post-stimulus 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.
Significance statement Mechanistic studies on perception and cognition tend to focus on the brain neglecting contributions of the body. Here, we investigated how respiration and heartbeat influence tactile perception: Respiration phase-locking to expected stimulus onsets corresponds to highest heart rate (and presumably alertness/cortical excitability) and correlates with detection performance. Tactile detection varies across the heart cycle with a minimum 250 - 300 ms after heart contraction, when the pulse reaches the finger. Lower detection was associated with disturbed metacognition, indicating – together with our previous finding of unchanged early ERPs - that this effect is not a peripheral physiological artifact but a result of cognitive processes that model our body’s internal state, make predictions to guide behavior, and might also tune respiration to serve the task.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
New analyses: (i) We determined interbeat intervals/heart frequency (HF) across the respiratory cycle and found that highest HF (presumably corresponding to highest arousal) almost perfectly aligned with the preferred time point of stimulus presentation. (ii) We assessed detection rates along the respiratory cycle to find that they were maximum in the first quarter of the cardiac cycle, i.e., indicating a functional implication of aligning the respiratory cycle to the task. (iii) We performed a new analysis of metacognition along the cardiac cycle according to signal detection theory and determined metacognitive efficiency which shows a clear variation across the cardiac cycle for "hits". Only in the last phase of diastole, metacognition of "hits" is "optimal". (iv) To assess which cardiac phase (systole or diastole) caused the pronounced heart slowing with conscious tactile perception, the T-wave end (indicating the boundary of both phases) was determined for each cardiac cycle. Only diastoles for hits were significantly longer compared to misses. Systoles showed no significant differences. (v) To address the question which respiration phase might have caused the shorter respiratory cycle duration for hits compared to misses, we determined the expiration and inspiration duration for each respiratory cycle and compared these between conditions. This did not show any evidence for a modulation of only one phase which is why we assume both phases are adapted. Further improvements: - We improved Figure 6 to display the resultant length of each participant's mean angle as a measure of intra-individual variance. - We corrected throughout the manuscript that the respiration analysis was locked to expiration onset. - We substantially edited the abstract, introduction, and discussion to integrate the new results and the reviewers' suggestions.
