Interoception vs. Exteroception: Cardiac interoception competes with tactile perception, yet also facilitates self-relevance encoding

Abstract

Internal bodily signals, notably the heartbeat, influence our perception of the external world - but the nature of this influence remains unclear. Different frameworks, originating in opposing views of the function of interoception, have developed largely in parallel. One line of evidence (Internal/External Competition) indicates that interoceptive and exteroceptive inputs compete for neural resources. Another line (Self-related Facilitation) shows a link between interoceptive and self-related processing, which might include computing the self-relevance of exteroceptive inputs. We contrasted these accounts within a single experimental task for which they yielded distinct predictions. We measured heartbeat-evoked potentials (HEPs, a measure of cardiac interoception) with EEG, and manipulated the self-relevance of an audio-tactile stimulus by placing the audio source either inside or outside the peripersonal space immediately around the body. On one hand, pre-stimulus HEP amplitudes over somatosensory cortex were linked to slower reaction times, and affected audio-tactile stimulus-evoked responses in the same area, indicating competition for shared neural resources. On the other hand, pre-stimulus HEPs over integrative sensorimotor and default-mode network regions facilitated stimulus self-relevance encoding, both in reaction times and audio-tactile evoked responses. Importantly, Competition and Facilitation effects were spatially and statistically independent from each other. We therefore reconcile the two views by showing the co-existence of two independent mechanisms: one that allocates neural resources to either internal bodily signals or the external world, and another by which interoception and exteroception are combined to determine the self-relevance of external signals. Our results highlight the multi-dimensionality of HEPs, and of internal states more generally. Significance StatementDo internal bodily signals distract us from the external world (Internal/External Competition account)? Or do internal signals contribute to conscious perception, by situating the perceived external world relative to the organism (Self-related Facilitation account)? So far, both accounts - reflecting fundamentally different views of brain-body interactions - received experimental support, but have never been compared directly. We measured neural responses to heartbeats, and tested how they influenced perception in an audio-tactile reaction time task where self-relevance was manipulated. We found evidence for both accounts, reflecting independent mechanisms in distinct brain regions. Our results reconcile two hitherto independent and seemingly contradictory research programmes on the relationship between interoception and exteroception. They further highlight the multi-dimensionality of cardiac-brain interactions, and hence of internal state.