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

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Abstract

Internal bodily signals, notably the heartbeat, influence our perception of the external world - but the nature of this influence remains unclear. One line of evidence (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, that might also include computing the self-relevance of exteroceptive inputs. We tested these seemingly opposing views within a single experimental task. Measuring heartbeat-evoked potentials (HEPs, a measure of cardiac interoception) with EEG, we 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. This design ensured that Competition and Self-related Facilitation accounts yielded contrasting predictions. On the 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 subsequent self-relevance encoding, both in reaction times and audio-tactile stimulus evoked responses. Importantly, Competition and Facilitation effects were spatially and statistically independent from each other. We thereby 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 as neurophysiological markers, and thus of internal states more generally.

Significance Statement

Do internal bodily signals distract us from the external world (Competition account)? Or do internal signals contribute to conscious perception by situating the perceived external world relative to the organism (Self-related Facilitation)? So far, both accounts received experimental support, but have not been compared directly. We measured how the brain responds to heartbeats in an audio-tactile reaction time task where self-relevance was manipulated. We find evidence for both accounts, but in different brain regions. Our results thus reconcile two hitherto largely 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.

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