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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Main Authors: Teodora Stoica, Brendan Depue
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-12-01
Series:Frontiers in Human Neuroscience
Subjects:
ICA
Online Access:https://www.frontiersin.org/articles/10.3389/fnhum.2020.571070/full
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spelling doaj-6cee8d2ae6a9425e9ee77671f2fef2852020-12-07T14:03:02ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612020-12-011410.3389/fnhum.2020.571070571070Shared Characteristics of Intrinsic Connectivity Networks Underlying Interoceptive Awareness and EmpathyTeodora Stoica0Brendan Depue1Brendan Depue2Department of Psychological and Brain Sciences, University of Louisville, Louisville, KY, United StatesDepartment of Psychological and Brain Sciences, University of Louisville, Louisville, KY, United StatesDepartment of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, KY, United StatesAwareness 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.https://www.frontiersin.org/articles/10.3389/fnhum.2020.571070/fullempathyinteroceptionfMRIICAresting-stateconnectivity
collection DOAJ
language English
format Article
sources DOAJ
author Teodora Stoica
Brendan Depue
Brendan Depue
spellingShingle Teodora Stoica
Brendan Depue
Brendan Depue
Shared Characteristics of Intrinsic Connectivity Networks Underlying Interoceptive Awareness and Empathy
Frontiers in Human Neuroscience
empathy
interoception
fMRI
ICA
resting-state
connectivity
author_facet Teodora Stoica
Brendan Depue
Brendan Depue
author_sort Teodora Stoica
title 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_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_sort shared characteristics of intrinsic connectivity networks underlying interoceptive awareness and empathy
publisher Frontiers Media S.A.
series Frontiers in Human Neuroscience
issn 1662-5161
publishDate 2020-12-01
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.
topic empathy
interoception
fMRI
ICA
resting-state
connectivity
url https://www.frontiersin.org/articles/10.3389/fnhum.2020.571070/full
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