Role of anatomical insular subdivisions in interoception: Interoceptive attention and accuracy have dissociable substrates

Abstract

Prior neuroimaging studies have supported the idea that the human insular cortex plays an important role in processing and representing internal bodily states, also termed “interoception.” According to recent theoretical studies, interoception includes several aspects such as attention and accuracy. However, there is no consensus on the laterality and location of the insula to support each aspect of interoception. Thus, we aimed to identify the anatomical insular subdivisions involved in interoceptive attention and accuracy; we examined 28 healthy volunteers who completed the behavioral heartbeat counting task and interoceptive attention paradigm using functional magnetic resonance imaging. First, interoceptive attention induced significant activation in the bilateral frontal operculum, precentral gyrus, middle insula, middle cingulate cortex, and supplementary motor area. Then, we compared the activation in anatomically predefined insular subdivisions during interoceptive attention. The highest activation of the middle short gyrus was noted within the insular cortex, followed by the anterior short gyrus and posterior short gyrus, while no significant hemispheric differences were observed. Finally, the interoceptive accuracy index, measured using the heartbeat counting task, strongly correlated with the activity of the right dorsal anterior insula/frontal operculum. These findings suggest that interoceptive attention is associated with the bilateral dorsal mid‐anterior insula, which supports the processing and representation of bodily signals. In contrast, the more dorsal anterior portion of the right insula plays a key role in obtaining accurate interoception.

Untangling Self-Reported Interoceptive Attention and Accuracy: Evidence from the European Portuguese Validation of the Body Perception Questionnaire and the Interoceptive Accuracy Scale

“…First, this non-linear association suggests that self-reported interoceptive attention and accuracy are indeed separate constructs, although likely influenced by each other. This is in line with recent evidence that found that interoceptive attention and accuracy are associated with dissociable insular subdivisions (bilateral dorsal mid-anterior insula vs. dorsal anterior portion of the right insula, respectively) which are vastly interconnected (Haruki & Ogawa, 2021). Secondly, it is important to further refine what is driving this association, that is, whether it may be a true non-linear association between selfreported interoceptive attention and accuracy or if these results are due to differences across both questionnaires (e.g., each measure assesses somewhat different interoceptive signals).…”

Cardiac and gastric interoception have distinct neural substrates

“…One possible explanation is that the primary interoceptive cortex would respond to changes in bodily states, rather than subjective experience of them: a recent study using rodents revealed that almost all neurons in the posterior insula responded to physiological changes (Cechetto and Saper, 1987; Gehrlach et al, 2019). In fact, interoceptive attention task where participants focus on their ongoing bodily sensations has been found to consistently activate the middle insula but the posterior (Haruki and Ogawa, 2021; Simmons et al, 2013). Rather, the posterior insula has been found to be functionally disconnected from other brain regions when people with accurate interoception performed the interoceptive attention task (Kuehn et al, 2015).…”

“…Even when the brain activation of another modality of interoception (such as gastric or urinary) was measured, direct comparison of brain activation within the modality of interoception has not been discussed (Deville et al, 2020; Kerr et al, 2016; Simmons et al, 2013). Therefore, understanding of how the brain encodes and represents different types of interoception is still limited; for example, the right anterior insula has been suggested as the most relevant region for the subjective experience of cardiac interoception (Caseras et al, 2013; Pollatos et al, 2007) but some studies have questioned the generalizability of this relationship for another modality of interoception (Baltazar et al, 2021; Haruki and Ogawa, 2021).…”

Interoception and Obsessive-Compulsive Disorder: A Review of Current Evidence and Future Directions

“…Neuroimaging studies of heartbeat detection have linked individual differences in the functioning of several regions including the midbrain, ventral striatum, anterior cingulate cortex, somatosensory cortex, and the insula to greater interoceptive accuracy [e.g., ( 41 , 63 , 67 , 94 )]. From among these areas, the right dorsal anterior insula appears to be the most reliably positively associated with interoceptive accuracy across studies ( 41 , 63 , 95 ). It has been proposed that this insular subregion may contribute to instantaneous subjective feelings from the body that generate a sense of the present moment ( 40 , 67 ).…”