Interoceptive signals shape the earliest markers and neural pathway to awareness at the visual threshold

Abstract

AbstractConscious awareness for threshold-stimuli fluctuates stochastically with the pre-stimulus brain state and variations of interoceptive signals across the cardiac and respiratory cycle. It remains debated whether interoceptive signals are suppressed or not and at what stages of processing they affect awareness in different sensory modalities. Because cardiac and respiratory activity are coupled through respiratory sinus arrythmia (RSA), we investigated the influence of the cardiac (systole/diastole) and the respiratory (inhalation/exhalation) phase on awareness-related ERPs. Subjects discriminated visual threshold stimuli while their EEG, ECG and respiration were simultaneously recorded. We compared ERPs and their intracranial generators for stimuli identified correctly with and without awareness as a function of the cardiac and respiratory phase. Cyclic variations of interoceptive signals from the baroreceptors (BRs) modulated both the earliest electrophysiological markers and the trajectory of brain activity when subjects became aware of the stimuli: the P1 was the earliest marker of awareness for low (diastole/inhalation) and the VAN for high (systole/exhalation) BR activity, indicating that interoceptive signals interfere with sensory processing of the visual input. Likewise, activity spread from the anterior insula to prefrontal cortex during low and from the posterior insula to posterior parietal cortex during high BR activity, providing a new solution to the debate whether activity in prefrontal or posterior parietal cortex is crucial for awareness: these regions were differentially recruited as a function of cyclic variations of BR activity rather than task demands. Our results suggest that the cardiac and respiratory rhythms are important rhythms that shape awareness-related brain activity.Significance StatementThe brain continuously processes stimuli from inside and outside the body, and interoceptive stimuli can modulate the perception of external stimuli. Cardiac and respiratory rhythms are important pacemakers of the organism and we show how they shape awareness-related brain activity for visual threshold stimuli in two ways. Variations of baroreceptor (BR) activity across the cardiac and respiratory cycle affect 1) the earliest electrophysiological marker (P1 for low (diastole/inhalation), VAN for high (systole/exhalation) BR activity) and 2) the brain areas activated (frontal cortex for low and parietal cortex for high BR activity) when subjects become aware of a stimulus. We propose to consider cardiac and respiratory activity as important modulators of brain activity rather than dismissing them as noise.