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The embodiment of emotional feelings in the brain.

ABSTRACT: Central to Walter Cannon's challenge to peripheral theories of emotion was that bodily arousal responses are too undifferentiated to account for the wealth of emotional feelings. Despite considerable evidence to the contrary, this remains widely accepted and for nearly a century has left the issue of whether visceral afferent signals are essential for emotional experience unresolved. Here we combine functional magnetic resonance imaging and multiorgan physiological recording to dissect experience of two distinct disgust forms and their relationship to peripheral and central physiological activity. We show that experience of core and body-boundary-violation disgust are dissociable in both peripheral autonomic and central neural responses and also that emotional experience specific to anterior insular activity encodes these different underlying patterns of peripheral physiological responses. These findings demonstrate that organ-specific physiological responses differentiate emotional feeling states and support the hypothesis that central representations of organism physiological homeostasis constitute a critical aspect of the neural basis of feelings.

SUBMITTER: Harrison NA

PROVIDER: S-EPMC3044882 | biostudies-literature | 2010 Sep

REPOSITORIES: biostudies-literature

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The embodiment of emotional feelings in the brain.

Harrison Neil A NA Gray Marcus A MA Gianaros Peter J PJ Critchley Hugo D HD

The Journal of neuroscience : the official journal of the Society for Neuroscience 20100901 38

Central to Walter Cannon's challenge to peripheral theories of emotion was that bodily arousal responses are too undifferentiated to account for the wealth of emotional feelings. Despite considerable evidence to the contrary, this remains widely accepted and for nearly a century has left the issue of whether visceral afferent signals are essential for emotional experience unresolved. Here we combine functional magnetic resonance imaging and multiorgan physiological recording to dissect experienc ...[more]

PMID: 20861391

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Project description:The anterior insula (AI) maps visceral states and is active during emotional experiences, a functional confluence that is central to neurobiological accounts of feelings. Yet, it is unclear how AI activity correlates with feelings during social emotions, and whether this correlation may be influenced by culture, as studies correlating real-time AI activity with visceral states and feelings have focused on Western subjects feeling physical pain or basic disgust. Given psychological evidence that social-emotional feelings are cognitively constructed within cultural frames, we asked Chinese and American participants to report their feeling strength to admiration and compassion-inducing narratives during fMRI with simultaneous electrocardiogram recording. Trial-by-trial, cardiac arousal and feeling strength correlated with ventral and dorsal AI activity bilaterally but predicted different variance, suggesting that interoception and social-emotional feeling construction are concurrent but dissociable AI functions. Further, although the variance that correlated with cardiac arousal did not show cultural effects, the variance that correlated with feelings did. Feeling strength was especially associated with ventral AI activity (the autonomic modulatory sector) in the Chinese group but with dorsal AI activity (the visceral-somatosensory/cognitive sector) in an American group not of Asian descent. This cultural group difference held after controlling for posterior insula (PI) activity and was replicated. A bi-cultural East-Asian American group showed intermediate results. The findings help elucidate how the AI supports feelings and suggest that previous reports that dorsal AI activation reflects feeling strength are culture related. More broadly, the results suggest that the brain's ability to construct conscious experiences of social emotion is less closely tied to visceral processes than neurobiological models predict and at least partly open to cultural influence and learning.

Dataset Information

The embodiment of emotional feelings in the brain.

Publications

The embodiment of emotional feelings in the brain.

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