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Shared Characteristics of Intrinsic Connectivity Networks Underlying Interoceptive Awareness and Empathy

Awareness of internal bodily sensations (interoceptive awareness; IA) and its connection to complex socioemotional abilities like empathy has been postulated, yet the functional neural circuitry they share remains poorly understood. The present fMRI study employs independent component analysis (ICA)...

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Autores principales: Stoica, Teodora, Depue, Brendan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7751325/
https://www.ncbi.nlm.nih.gov/pubmed/33364926
http://dx.doi.org/10.3389/fnhum.2020.571070
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author Stoica, Teodora
Depue, Brendan
author_facet Stoica, Teodora
Depue, Brendan
author_sort Stoica, Teodora
collection PubMed
description Awareness of internal bodily sensations (interoceptive awareness; IA) and its connection to complex socioemotional abilities like empathy has been postulated, yet the functional neural circuitry they share remains poorly understood. The present fMRI study employs independent component analysis (ICA) to investigate which empathy facet (Cognitive or Affective) shares resting-state functional connectivity (rsFC) and/or BOLD variability (rsBOLD) with IA. Healthy participants viewed an abstract nonsocial movie demonstrated to evoke strong rsFC in brain networks resembling rest (InScapes), and resultant rsFC and rsBOLD data were correlated with self-reported empathy and IA questionnaires. We demonstrate a bidirectional behavioral and neurobiological relationship between empathy and IA, depending on the type of empathy interrogated: Affective empathy and IA share both rsFC and rsBOLD, while Cognitive empathy and IA only share rsBOLD. Specifically, increased rsFC in the right inferior frontal operculum (rIFO) of a larger attention network was associated with increased vicarious experience but decreased awareness of inner body sensations. Furthermore, increased rsBOLD between brain regions of an interoceptive network was related to increased sensitivity to internal sensations along with decreased Affective empathy. Finally, increased rsBOLD between brain regions subserving a mentalizing network related to not only an improved ability to take someone’s perspective, but also a better sense of mind-body interconnectedness. Overall, these findings suggest that the awareness of one’s own internal body changes (IA) is related to the socioemotional ability of feeling and understanding another’s emotional state (empathy) and critically, that this relationship is reflected in the brain’s resting state neuroarchitecture. Methodologically, this work highlights the importance of utilizing rsBOLD as a complementary window alongside rsFC to better understand neurological phenomena. Our results may be beneficial in aiding diagnosis in clinical populations such as autism spectrum disorder (ASD), where participants may be unable to complete tasks or questionnaires due to the severity of their symptoms.
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spelling pubmed-77513252020-12-22 Shared Characteristics of Intrinsic Connectivity Networks Underlying Interoceptive Awareness and Empathy Stoica, Teodora Depue, Brendan Front Hum Neurosci Human Neuroscience Awareness of internal bodily sensations (interoceptive awareness; IA) and its connection to complex socioemotional abilities like empathy has been postulated, yet the functional neural circuitry they share remains poorly understood. The present fMRI study employs independent component analysis (ICA) to investigate which empathy facet (Cognitive or Affective) shares resting-state functional connectivity (rsFC) and/or BOLD variability (rsBOLD) with IA. Healthy participants viewed an abstract nonsocial movie demonstrated to evoke strong rsFC in brain networks resembling rest (InScapes), and resultant rsFC and rsBOLD data were correlated with self-reported empathy and IA questionnaires. We demonstrate a bidirectional behavioral and neurobiological relationship between empathy and IA, depending on the type of empathy interrogated: Affective empathy and IA share both rsFC and rsBOLD, while Cognitive empathy and IA only share rsBOLD. Specifically, increased rsFC in the right inferior frontal operculum (rIFO) of a larger attention network was associated with increased vicarious experience but decreased awareness of inner body sensations. Furthermore, increased rsBOLD between brain regions of an interoceptive network was related to increased sensitivity to internal sensations along with decreased Affective empathy. Finally, increased rsBOLD between brain regions subserving a mentalizing network related to not only an improved ability to take someone’s perspective, but also a better sense of mind-body interconnectedness. Overall, these findings suggest that the awareness of one’s own internal body changes (IA) is related to the socioemotional ability of feeling and understanding another’s emotional state (empathy) and critically, that this relationship is reflected in the brain’s resting state neuroarchitecture. Methodologically, this work highlights the importance of utilizing rsBOLD as a complementary window alongside rsFC to better understand neurological phenomena. Our results may be beneficial in aiding diagnosis in clinical populations such as autism spectrum disorder (ASD), where participants may be unable to complete tasks or questionnaires due to the severity of their symptoms. Frontiers Media S.A. 2020-12-07 /pmc/articles/PMC7751325/ /pubmed/33364926 http://dx.doi.org/10.3389/fnhum.2020.571070 Text en Copyright © 2020 Stoica and Depue. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Human Neuroscience
Stoica, Teodora
Depue, Brendan
Shared Characteristics of Intrinsic Connectivity Networks Underlying Interoceptive Awareness and Empathy
title Shared Characteristics of Intrinsic Connectivity Networks Underlying Interoceptive Awareness and Empathy
title_full Shared Characteristics of Intrinsic Connectivity Networks Underlying Interoceptive Awareness and Empathy
title_fullStr Shared Characteristics of Intrinsic Connectivity Networks Underlying Interoceptive Awareness and Empathy
title_full_unstemmed Shared Characteristics of Intrinsic Connectivity Networks Underlying Interoceptive Awareness and Empathy
title_short Shared Characteristics of Intrinsic Connectivity Networks Underlying Interoceptive Awareness and Empathy
title_sort shared characteristics of intrinsic connectivity networks underlying interoceptive awareness and empathy
topic Human Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7751325/
https://www.ncbi.nlm.nih.gov/pubmed/33364926
http://dx.doi.org/10.3389/fnhum.2020.571070
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