Martin Grund

Perception is biased by expectations and previous actions. Pre-stimulus brain oscillations are a potential candidate for implementing biases in the brain. In two EEG studies (43 and 39 participants) on somatosensory near-threshold detection, we investigated the pre-stimulus neural correlates of an (implicit) previous choice bias and an explicit bias. The explicit bias was introduced by informing participants about stimulus probability on a single-trial level (volatile context) or block-wise (stable context). Behavioural analysis confirmed adjustments in the decision criterion and confidence ratings according to the cued probabilities and previous choice-induced biases. Pre-stimulus beta power with distinct sources in sensory and higher-order cortical areas predicted explicit and implicit biases, respectively, on a single subject level and partially mediated the impact of previous choice and stimulus probability on the detection response. We suggest pre-stimulus beta oscillations in distinct brain areas as a neural correlate of explicit and implicit biases in somatosensory 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 STATEMENTMechanistic 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.

Cardiac activity has been shown to interact with conscious tactile perception: Detecting near-threshold tactile stimuli is more likely during diastole than systole and heart slowing is more pronounced for detected compared to undetected stimuli. Here, we investigated how cardiac cycle effects on conscious tactile perception relate to respiration given the natural coupling of these two dominant body rhythms. Forty-one healthy participants had to report conscious perception of weak electrical pulses applied to the left index finger (yes/no) and confidence about their yes/no-decision (unconfident/confident) while electrocardiography (ECG), respiratory activity (chest circumference), and finger pulse oximetry were recorded. We confirmed the previous findings of higher tactile detection rate during diastole and unimodal distribution of hits in diastole, more specifically, we found this only when participants were confident about their detection decision. Lowest tactile detection rate occurred 250-300 ms after the R-peak corresponding to pulse-wave onsets in the finger. Inspiration was locked to tactile stimulation, and this was more consistent in hits than misses. Respiratory cycles accompanying misses were longer as compared to hits and correct rejections. Cardiac cycle effects on conscious tactile perception interact with decision confidence and coincide with pulse-wave arrival, which suggests the involvement of higher cognitive processing in this phenomenon possibly related to predictive coding. The more consistent phase-locking of inspiration with stimulus onsets for hits than misses is in line with previous reports of phase-locked inspiration to cognitive task onsets which were interpreted as tuning the sensory system for incoming information. 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: We show that inspiration locked to expected stimulus onsets optimizes detection task performance and that tactile detection varies across the heart cycle with a minimum 250-300 milliseconds after heart contraction, when the pulse reaches the finger. Lower detection was associated with reduced confidence ratings, indicating – together with our previous finding of unchanged early ERPs - that this effect is not a peripheral physiological artifact but a result of higher cognitive processes that model the internal state of our body, make predictions to guide behavior, and might also tune respiration to serve the task.

Significance: Our brain continuously receives signals from the body and the environment. Although we are mostly unaware of internal bodily processes, such as our heartbeats, they can affect our perception. Here, we show two distinct ways in which the heartbeat modulates conscious perception. First, increased heartbeat-evoked neural activity before stimulation is followed by decreased somatosensory detection. This effect can be explained by subjects adopting a more conservative decision criterion, which is accompanied by changes in early and late somatosensory-evoked responses. Second, stimulus timing during the cardiac cycle affects sensitivity but not criterion for somatosensory stimuli, which is reflected only in late somatosensory-evoked responses. We propose that these heartbeat-related modulations are connected to fluctuations of interoceptive attention and (unconscious) predictive coding mechanisms.

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.

Human perception either refers to the external world, exteroception, or internal body parts such as the heart, interoception. How these two types of perception interact is poorly understood. Using electroencephalography, we identify two heartbeat-related modulations of conscious somatosensory perception: (i) When stimulus timing coincided with systole of the cardiac cycle, participants were less likely to detect and localize somatosensory stimuli, and late components (P300) of the somatosensory-evoked potential (SEP) were attenuated. (ii) The amplitude of the heartbeat-evoked potential (HEP) negatively correlated with detection bias (criterion) and localization accuracy. Furthermore, higher HEP amplitudes were followed by decreases in both early and late SEP amplitudes. Both heartbeat-related effects were independent of the alpha oscillations’ influence on somatosensory processing. We conclude that internal signals are integrated into our conscious perception of the world, and connect our results to predictive processing (heartbeat-coupled stimulus timing) and attentional shifts between exteroception and interoception (HEP amplitude).

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.

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. We here investigated whether the phase of the cardiac cycle and the pre-stimulus 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. Impact Statement: It is highly debated to what extent cardiac activity modulates the access of external stimuli to consciousness. The evidence is inconsistent across sensory modalities and previous research focused at specific intervals within the cardiac cycle. Here, we examined the perception of near-threshold electrical pulses across the entire cardiac cycle. Our results show that conscious somatosensory perception is enhanced during the late phase of the cardiac cycle (at diastole) and associated with a more pronounced cardiac deceleration (as compared to non-detected stimuli). This strengthens the evidence that the physiological state of the body influences how we perceive the world.