Cardiac and Gastric Interoceptive Awareness Have Distinct Neural Substrates

Abstract

Interoceptive awareness, an awareness of the internal body state, guides adaptive behavior by providing ongoing information on body signals, such as heart rate and energy status. However, it is still unclear how interoceptive awareness of different body organs are represented in the human brain. Hence, we directly compared the neural activations accompanying attention to cardiac (related to heartbeat) and gastric (related to stomach) sensations, which generate cardiac and gastric interoceptive awareness, in the same population (healthy humans, N = 31). Participants were asked to direct their attention towards heart and stomach sensations and become aware of them in a magnetic resonance imaging scanner. The results indicated that the neural activations underlying gastric attention encompassed larger brain regions, including the occipitotemporal visual cortices, bilateral primary motor cortices, primary somatosensory cortex, left orbitofrontal cortex, and hippocampal regions. Cardiac attention, however, selectively activated the right anterior insula extending to the frontal operculum compared to gastric attention. Moreover, our detailed analyses focusing on the insula, the most relevant region for interoceptive awareness, revealed that the left dorsal middle insula encoded cardiac and gastric attention via different activation patterns, but the posterior insula did not. Our results demonstrate that cardiac and gastric attention evoke different brain activation patterns; in particular, the selective activation may reflect differences in the functional roles of cardiac and gastric interoceptive awareness.Significance statementInteroceptive awareness, senses that arise from within the body, play a critical role in adaptive behavior by providing ongoing information on bodily states, such as the heart rate and energy status. Although interoceptive awareness has various functions depending on its source, previous neuroimaging studies have extensively used cardiac awareness (related to the heartbeat). The present study showed that attention to cardiac and gastric (related to the stomach) sensations evoked distinct neural activation patterns by combining mass-univariate analysis with multivoxel pattern analysis using fMRI, indicating that the brain encodes attention to and thus awareness of different bodily organs in different manner. Moreover, the selective brain activation may reflect differences in the functional roles of cardiac and gastric awareness.

Interoceptive disruption in functional neurological disorder: a multimodal brain imaging study

“…In this study, we combined a state-based fMRI assessment of cardiac interoception with VBM, self-report interoceptive measures, and dimensional psychopathology scores to examine multilevel profiles linked to interoception in FND. As expected, the heartbeat counting task increased salience and ventral attention network co-activations (e.g., bilateral anterior insula, middle cingulate gyri, and TPJ) across all participants as shown in PC1 of the interoception vs. rest and interoception vs. exteroception contrasts (Haruki & Ogawa, 2023;Schulz, 2016). Concurrently, we observed co-deactivations in default mode and visual processing networks in PC1, including ventromedial, posterior medial and occipital areas.…”

“…The copyright holder for this preprint this version posted March 14, 2024. ; https://doi.org/10.1101/2024.03.13.24303546 doi: medRxiv preprint in PC1 of the interoception vs. rest and interoception vs. exteroception contrasts (Haruki & Ogawa, 2023;Schulz, 2016). Concurrently, we observed co-deactivations in default mode and visual processing networks in PC1, including ventromedial, posterior medial and occipital areas.…”

“…While we cannot exclude other possibilities, we speculate that the relatively higher occipital activations in patients with FND may be associated with reduced attentional allocation to interoceptive signals. However, recent studies also reported occipital regions activations in interoception that require further exploration (Haruki & Oqawa, 2023; Wang et al, 2019).…”

Insular volumetry in severe alcohol use disorder and Korsakoff's syndrome through an anatomical parcellation: Let us go back to basics

“…21 The rationale for using this specific insular parcellation is that, by combining both macro-anatomical landmarks and probabilistic techniques, this parcellation based on a probabilistic atlas 21 overcomes prior parcellation limits such as coarse subregions delimitation (i.e., ending up with a refined 6*2 parcellation) while taking account of between-subject variability. Moreover, while a recent cytoarchitecture parcellation focus has been observed in the insula field, 22 the current study macro-anatomical insular parcellation allows for comparisons in future research studies (e.g., used in a previous study 23 ), contrarily to the cytoarchitecture technique. 21 Indeed, due to limits inherent to the cytoarchitecture technique (i.e., developed using ex-vivo data), this parcellation technique does not allow for it to be used in neuroimaging studies.…”

Substructure of the brain’s Cingulo-Opercular network

“…Thus, the Action subnetwork may also receive fast sensory feedback from somatosensory functions about the immediate results of executed actions. Given these postulated functions, it is possible that the Action subnetwork also represents visceral sensation, which has localization in middle insula convergent with this subnetwork 65 .…”