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

Abstract

Abstract Variations in interoceptive signals from the baroreceptors (BRs) across the cardiac and respiratory cycle can modulate cortical excitability and so affect awareness. It remains debated at what stages of processing they affect awareness-related event-related potentials (ERPs) in different sensory modalities. 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 electroencephalogram (EEG), electrocardiogram (ECG) and respiration were simultaneously recorded. We compared ERPs and their intracranial generators for stimuli classified 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: an early sensory component (P1) was the earliest marker of awareness for low (diastole/inhalation) and a perceptual component (visual awareness negativity, VAN) for high (systole/exhalation) BR activity, indicating that BR signals interfere with the sensory processing of the visual input. Likewise, activity spread from the primary visceral cortex (posterior insula) to posterior parietal cortices during high and from associative interoceptive centers (anterior insula) to prefrontal cortex during low BR activity. Consciousness is thereby resolved in cognitive/associative regions when BR is low and in perceptual centers when it is high. Our results suggest that cyclic fluctuations of BR signaling affect both the earliest markers of awareness and the brain processes underlying conscious awareness. Significance Statement The 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. Cyclic variations of bodily signal can modulate cortical excitability and so shape the pathway to awareness and we propose to consider them as functionally relevant signals rather dismissing them as noise.