Respiration, Heartbeat, and Conscious Tactile Perception.

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.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 when the pulse reaches the finger and a maximum in diastole. Taken together with our previous finding of unchanged early event-related potentials across the cardiac cycle, we conclude that these effects are 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.

Heart-brain interactions shape somatosensory perception and evoked potentials.

Even though humans are mostly not aware of their heartbeats, several heartbeat-related effects have been reported to influence conscious perception. It is not clear whether these effects are distinct or related phenomena, or whether they are early sensory effects or late decisional processes. Combining electroencephalography and electrocardiography, along with signal detection theory analyses, we identify two distinct heartbeat-related influences on conscious perception differentially related to early vs. late somatosensory processing. First, an effect on early sensory processing was found for the heartbeat-evoked potential (HEP), a marker of cardiac interoception. The amplitude of the prestimulus HEP negatively correlated with localization and detection of somatosensory stimuli, reflecting a more conservative detection bias (criterion). Importantly, higher HEP amplitudes were followed by decreases in early (P50) as well as late (N140, P300) somatosensory-evoked potential (SEP) amplitudes. Second, stimulus timing along the cardiac cycle also affected perception. During systole, stimuli were detected and correctly localized less frequently, relating to a shift in perceptual sensitivity. This perceptual attenuation was accompanied by the suppression of only late SEP components (P300) and was stronger for individuals with a more stable heart rate. Both heart-related effects were independent of alpha oscillations' influence on somatosensory processing. We explain cardiac cycle timing effects in a predictive coding account and suggest that HEP-related effects might reflect spontaneous shifts between interoception and exteroception or modulations of general attentional resources. Thus, our results provide a general conceptual framework to explain how internal signals can be integrated into our conscious perception of the world.

Neural correlates of conscious tactile perception: An analysis of BOLD activation patterns and graph metrics.

Theories of human consciousness substantially vary in the proposed spatial extent of brain activity associated with conscious perception as well as in the assumed functional alterations within the involved brain regions. Here, we investigate which local and global changes in brain activity accompany conscious somatosensory perception following electrical finger nerve stimulation, and whether there are whole-brain functional network alterations by means of graph metrics. Thirty-eight healthy participants performed a somatosensory detection task and reported their decision confidence during fMRI. For conscious tactile perception in contrast to undetected near-threshold trials (misses), we observed increased BOLD activity in the precuneus, the intraparietal sulcus, the insula, the nucleus accumbens, the inferior frontal gyrus and the contralateral secondary somatosensory cortex. For misses compared to correct rejections, bilateral secondary somatosensory cortices, supplementary motor cortex and insula showed greater activations. The analysis of whole-brain functional network topology for hits, misses and correct rejections, did not result in any significant differences in modularity, participation, clustering or path length, which was supported by Bayes factor statistics. In conclusion, for conscious somatosensory perception, our results are consistent with an involvement of (probably) domain-general brain areas (precuneus, insula, inferior frontal gyrus) in addition to somatosensory regions; our data do not support the notion of specific changes in graph metrics associated with conscious experience. For the employed somatosensory submodality of fine electrical current stimulation, this speaks for a global broadcasting of sensory content across the brain without substantial reconfiguration of the whole-brain functional network resulting in an integrative conscious experience.

Interactions between cardiac activity and conscious somatosensory perception.

Fluctuations in the heart's activity can modulate the access of external stimuli to consciousness. The link between perceptual awareness and cardiac signals has been investigated mainly in the visual and auditory domain. Here, we investigated whether the phase of the cardiac cycle and the prestimulus heart rate influence conscious somatosensory perception. We also tested how conscious detection of somatosensory stimuli affects the heart rate. Electrocardiograms (ECG) of 33 healthy volunteers were recorded while applying near-threshold electrical pulses at a fixed intensity to the left index finger. Conscious detection was not uniformly distributed across the cardiac cycle but significantly higher in diastole than in systole. We found no evidence that the heart rate before a stimulus influenced its detection, but hits (correctly detected somatosensory stimuli) led to a more pronounced cardiac deceleration than misses. Our findings demonstrate interactions between cardiac activity and conscious somatosensory perception, which highlights the importance of internal bodily states for sensory processing beyond the auditory and visual domain.

Rhythmic activity in a motor axon induced by axotomy.

Rhythmic bursting in the axon of a flexor motoneuron in the stick insect Cuniculina impigra was evoked by cutting the main leg nerve at the autotomy plane of a leg. Bursts of up to 12 spikes were recorded extracellularly from the distal stump of the cut nerve for up to 30 min. With time the number of spikes per burst and mean burst duration decreased and interspike intervals increased. Maximum burst duration gained was very constant, approximately 0.19 s, and independent of spike number per burst. Mean cycle period was also relatively constant, approximately 0.7 s, apparently due to a waning excitation that was countered by a waning spike dependent inhibition.