Hierarchical integration of interoception and exteroception in the anterior insula during naturalistic emotional experience

      Background: While external events frame emotional experience, interoception - the sensing of internal physiological states - is fundamental to feeling and emotion. Despite growing evidence that the insula plays a key role in representing interoceptive signals (Craig, 2009), its role in emotional experience during naturalistic conditions remains largely unknown. Using high-resolution 7 T neuroimaging and simultaneous physiological recordings, we investigated the neurophysiological processes whilst participants listened to a dramatic narrative, and applied effective connectivity analysis to delineate the neural circuits underlying interoceptive processing and integration. Methods: Functional magnetic resonance imaging (fMRI) data with simultaneous pulse recordings were acquired from 18 participants whilst they listened to the ‘Forrest Gump’ audio (Hanke, 2014). Heart rate activity was decomposed into high and low frequency components to estimate the cardiac autonomic signals. We used dynamic causal modelling (DCM) to infer the causal relationship between brain regions implicated by the GLM (Friston, 2003). Results: We found that the high frequency heart rate variability was robustly synchronized across participants and correlated with neural activity in the posterior insula. The anterior insula, on the other hand, was locked specifically to the emotionally salient moments of the audio streams. Effective connectivity analysis further reveals the insular hierarchy for interoceptive processing: While the posterior insula represents interoceptive states, the anterior insula integrates them with extroceptive representations. Conclusion: Our analysis offers novel insights in formulating the computational framework of cortical interoceptive processing, and an ecologically-valid tool to elucidate neural underpinnings of interoceptive and emotional deficits in brain disorders.
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