Sensing the heart, seeing the world: Neural mechanisms of attentional allocation between interoception and exteroception

Abstract

Adaptive behaviour requires the flexible allocation of attention between sensory information arising from the external environment (exteroception) and signals originating within the body (interoception). While the neural mechanisms supporting exteroceptive attention have been extensively characterised, considerably less is known about how attention is allocated between competing interoceptive and exteroceptive sources of information. To address this question, we used functional magnetic resonance imaging (fMRI) to compare cardiac interoceptive attention during heartbeat counting with a carefully matched visual target counting task. Importantly, external visual input was held constant during both tasks, and behavioural accuracy and subjective confidence ratings for task difficulty did not differ significantly between conditions. This provided a controlled comparison in which attention was selectively allocated between internal bodily signals and external sensory information. Cardiac interoceptive and visual exteroceptive attention engaged largely distinct cortical networks. Cardiac interoceptive attention recruited a distributed insula-centred network supporting interoceptive processing and cognitive control. In contrast, visual target counting engaged a dorsal frontoparietal attention network and selectively shaped activity within visual cortex, enhancing regions representing task-relevant central visual information while suppressing regions representing task-irrelevant peripheral visual information. Despite this functional segregation, activity within these systems was not independent of where attention was directed. Exteroceptive attention suppressed activity within the posterior insula, suggesting down-regulation of interoceptive processing. Conversely, peripheral visual regions remained suppressed during interoceptive attention, suggesting that externally directed sensory processing is also down-regulated when attention is directed towards the body. More accurate heartbeat counting was additionally associated with less engagement of the right inferior parietal lobule, consistent with reduced bottom-up attentional capture by external sensory information. Together, these findings are consistent with competitive allocation of attentional resources between neural systems supporting internal bodily signals and external sensory information. More broadly, they provide a system-level account of how the human brain flexibly balances internal and external information during goal-directed behaviour.