Abstract

The somatic marker hypothesis proposes that the cortical representation of visceral signals is a crucial component of emotional processing. No previous study has investigated the information flow among brain regions that process visceral information during emotional perception. In this magnetoencephalography study of 32 healthy subjects of either sex, heartbeat-evoked responses (HERs), which reflect the cortical processing of heartbeats, were modulated by the perception of a sad face. The modulation effect was localized to the prefrontal cortices, the globus pallidus, and an interoceptive network including the right anterior insula (RAI) and dorsal anterior cingulate cortex (RdACC). Importantly, our Granger causality analysis provides the first evidence for the increased flow of heartbeat information from the RAI to the RdACC during sad face perception. Moreover, using a surrogate R-peak analysis, we have shown that this HER modulation effect was time-locked to heartbeats. These findings advance the understanding of brain-body interactions during emotional processing.

Highlights

  • According to the James-Lange theory and the somatic marker hypothesis, emotional feelings are the mental experience of bodily states[1,2]

  • The activation of the insula was not found in the text-based emoticon condition, while the other activated regions overlapped with brain regions that are typically activated by emotional faces[13]

  • Our findings provide the first evidence that the perception of a sad face modulates bottom-up interoceptive information processing from the right anterior insula (RAI) to the right dorsal anterior cingulate cortex (RdACC)

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Summary

Introduction

According to the James-Lange theory and the somatic marker hypothesis, emotional feelings are the mental experience of bodily states[1,2]. We expected that modulation of the HERs by emotional expressions would be localized to the convergence regions of interoception and emotion, such as the anterior insula and anterior cingulate cortex[16]. We expected that the bottom-up heartbeat information processing starting from the anterior insula, which represents the viscerosensory information from the posterior insula, to the anterior cingulate cortex would be enhanced by emotional expressions[12]. This pathway is hypothesized to be involved in the processing of the subjective salience of emotions using interoceptive signals[12,17,18]

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