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Pain Processing after Social Exclusion and Its Relation to Rejection Sensitivity in Borderline Personality Disorder

OBJECTIVE: There is a general agreement that physical pain serves as an alarm signal for the prevention of and reaction to physical harm. It has recently been hypothesized that “social pain,” as induced by social rejection or abandonment, may rely on comparable, phylogenetically old brain structures...

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Autores principales: Bungert, Melanie, Koppe, Georgia, Niedtfeld, Inga, Vollstädt-Klein, Sabine, Schmahl, Christian, Lis, Stefanie, Bohus, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4524681/
https://www.ncbi.nlm.nih.gov/pubmed/26241850
http://dx.doi.org/10.1371/journal.pone.0133693
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author Bungert, Melanie
Koppe, Georgia
Niedtfeld, Inga
Vollstädt-Klein, Sabine
Schmahl, Christian
Lis, Stefanie
Bohus, Martin
author_facet Bungert, Melanie
Koppe, Georgia
Niedtfeld, Inga
Vollstädt-Klein, Sabine
Schmahl, Christian
Lis, Stefanie
Bohus, Martin
author_sort Bungert, Melanie
collection PubMed
description OBJECTIVE: There is a general agreement that physical pain serves as an alarm signal for the prevention of and reaction to physical harm. It has recently been hypothesized that “social pain,” as induced by social rejection or abandonment, may rely on comparable, phylogenetically old brain structures. As plausible as this theory may sound, scientific evidence for this idea is sparse. This study therefore attempts to link both types of pain directly. We studied patients with borderline personality disorder (BPD) because BPD is characterized by opposing alterations in physical and social pain; hyposensitivity to physical pain is associated with hypersensitivity to social pain, as indicated by an enhanced rejection sensitivity. METHOD: Twenty unmedicated female BPD patients and 20 healthy participants (HC, matched for age and education) played a virtual ball-tossing game (cyberball), with the conditions for exclusion, inclusion, and a control condition with predefined game rules. Each cyberball block was followed by a temperature stimulus (with a subjective pain intensity of 60% in half the cases). The cerebral responses were measured by functional magnetic resonance imaging. The Adult Rejection Sensitivity Questionnaire was used to assess rejection sensitivity. RESULTS: Higher temperature heat stimuli had to be applied to BPD patients relative to HCs to reach a comparable subjective experience of painfulness in both groups, which suggested a general hyposensitivity to pain in BPD patients. Social exclusion led to a subjectively reported hypersensitivity to physical pain in both groups that was accompanied by an enhanced activation in the anterior insula and the thalamus. In BPD, physical pain processing after exclusion was additionally linked to enhanced posterior insula activation. After inclusion, BPD patients showed reduced amygdala activation during pain in comparison with HC. In BPD patients, higher rejection sensitivity was associated with lower activation differences during pain processing following social exclusion and inclusion in the insula and in the amygdala. DISCUSSION: Despite the similar behavioral effects in both groups, BPD patients differed from HC in their neural processing of physical pain depending on the preceding social situation. Rejection sensitivity further modulated the impact of social exclusion on neural pain processing in BPD, but not in healthy controls.
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spelling pubmed-45246812015-08-06 Pain Processing after Social Exclusion and Its Relation to Rejection Sensitivity in Borderline Personality Disorder Bungert, Melanie Koppe, Georgia Niedtfeld, Inga Vollstädt-Klein, Sabine Schmahl, Christian Lis, Stefanie Bohus, Martin PLoS One Research Article OBJECTIVE: There is a general agreement that physical pain serves as an alarm signal for the prevention of and reaction to physical harm. It has recently been hypothesized that “social pain,” as induced by social rejection or abandonment, may rely on comparable, phylogenetically old brain structures. As plausible as this theory may sound, scientific evidence for this idea is sparse. This study therefore attempts to link both types of pain directly. We studied patients with borderline personality disorder (BPD) because BPD is characterized by opposing alterations in physical and social pain; hyposensitivity to physical pain is associated with hypersensitivity to social pain, as indicated by an enhanced rejection sensitivity. METHOD: Twenty unmedicated female BPD patients and 20 healthy participants (HC, matched for age and education) played a virtual ball-tossing game (cyberball), with the conditions for exclusion, inclusion, and a control condition with predefined game rules. Each cyberball block was followed by a temperature stimulus (with a subjective pain intensity of 60% in half the cases). The cerebral responses were measured by functional magnetic resonance imaging. The Adult Rejection Sensitivity Questionnaire was used to assess rejection sensitivity. RESULTS: Higher temperature heat stimuli had to be applied to BPD patients relative to HCs to reach a comparable subjective experience of painfulness in both groups, which suggested a general hyposensitivity to pain in BPD patients. Social exclusion led to a subjectively reported hypersensitivity to physical pain in both groups that was accompanied by an enhanced activation in the anterior insula and the thalamus. In BPD, physical pain processing after exclusion was additionally linked to enhanced posterior insula activation. After inclusion, BPD patients showed reduced amygdala activation during pain in comparison with HC. In BPD patients, higher rejection sensitivity was associated with lower activation differences during pain processing following social exclusion and inclusion in the insula and in the amygdala. DISCUSSION: Despite the similar behavioral effects in both groups, BPD patients differed from HC in their neural processing of physical pain depending on the preceding social situation. Rejection sensitivity further modulated the impact of social exclusion on neural pain processing in BPD, but not in healthy controls. Public Library of Science 2015-08-04 /pmc/articles/PMC4524681/ /pubmed/26241850 http://dx.doi.org/10.1371/journal.pone.0133693 Text en © 2015 Bungert et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Bungert, Melanie
Koppe, Georgia
Niedtfeld, Inga
Vollstädt-Klein, Sabine
Schmahl, Christian
Lis, Stefanie
Bohus, Martin
Pain Processing after Social Exclusion and Its Relation to Rejection Sensitivity in Borderline Personality Disorder
title Pain Processing after Social Exclusion and Its Relation to Rejection Sensitivity in Borderline Personality Disorder
title_full Pain Processing after Social Exclusion and Its Relation to Rejection Sensitivity in Borderline Personality Disorder
title_fullStr Pain Processing after Social Exclusion and Its Relation to Rejection Sensitivity in Borderline Personality Disorder
title_full_unstemmed Pain Processing after Social Exclusion and Its Relation to Rejection Sensitivity in Borderline Personality Disorder
title_short Pain Processing after Social Exclusion and Its Relation to Rejection Sensitivity in Borderline Personality Disorder
title_sort pain processing after social exclusion and its relation to rejection sensitivity in borderline personality disorder
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4524681/
https://www.ncbi.nlm.nih.gov/pubmed/26241850
http://dx.doi.org/10.1371/journal.pone.0133693
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