Early adverse life events are associated with altered brain network architecture in a sex- dependent manner

Introduction: Early adverse life events (EALs) increase the risk for chronic medical and psychiatric disorders by altering early neurodevelopment. The aim of this study was to examine associations between EALs and network properties of core brain regions in the emotion regulation and salience networ...

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Main Authors: Arpana Gupta, PhD, Emeran A. Mayer, MD, PhD, Jonathan R. Acosta, BSc, Kareem Hamadani, BSc, Carinna Torgerson, BA, John D. van Horn, PhD, Lin Chang, MD, Bruce Naliboff, PhD, Kirsten Tillisch, MD, Jennifer S. Labus, PhD
Format: Article
Language:English
Published: Elsevier 2017-12-01
Series:Neurobiology of Stress
Online Access:http://www.sciencedirect.com/science/article/pii/S2352289516300273
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author Arpana Gupta, PhD
Emeran A. Mayer, MD, PhD
Jonathan R. Acosta, BSc
Kareem Hamadani, BSc
Carinna Torgerson, BA
John D. van Horn, PhD
Lin Chang, MD
Bruce Naliboff, PhD
Kirsten Tillisch, MD
Jennifer S. Labus, PhD
spellingShingle Arpana Gupta, PhD
Emeran A. Mayer, MD, PhD
Jonathan R. Acosta, BSc
Kareem Hamadani, BSc
Carinna Torgerson, BA
John D. van Horn, PhD
Lin Chang, MD
Bruce Naliboff, PhD
Kirsten Tillisch, MD
Jennifer S. Labus, PhD
Early adverse life events are associated with altered brain network architecture in a sex- dependent manner
Neurobiology of Stress
author_facet Arpana Gupta, PhD
Emeran A. Mayer, MD, PhD
Jonathan R. Acosta, BSc
Kareem Hamadani, BSc
Carinna Torgerson, BA
John D. van Horn, PhD
Lin Chang, MD
Bruce Naliboff, PhD
Kirsten Tillisch, MD
Jennifer S. Labus, PhD
author_sort Arpana Gupta, PhD
title Early adverse life events are associated with altered brain network architecture in a sex- dependent manner
title_short Early adverse life events are associated with altered brain network architecture in a sex- dependent manner
title_full Early adverse life events are associated with altered brain network architecture in a sex- dependent manner
title_fullStr Early adverse life events are associated with altered brain network architecture in a sex- dependent manner
title_full_unstemmed Early adverse life events are associated with altered brain network architecture in a sex- dependent manner
title_sort early adverse life events are associated with altered brain network architecture in a sex- dependent manner
publisher Elsevier
series Neurobiology of Stress
issn 2352-2895
publishDate 2017-12-01
description Introduction: Early adverse life events (EALs) increase the risk for chronic medical and psychiatric disorders by altering early neurodevelopment. The aim of this study was to examine associations between EALs and network properties of core brain regions in the emotion regulation and salience networks, and to test the influence of sex on these associations. Methods: Resting-state functional and diffusion tensor magnetic resonance imaging were obtained in healthy individuals (61 men, 63 women). Functional and anatomical network properties of centrality and segregation were calculated for the core regions of the two networks using graph theory. Moderator analyses were applied to test hypotheses. Results: The type of adversity experienced influences brain wiring differently, as higher general EALs were associated with decreased functional and anatomical centrality in salience and emotion regulation regions, while physical and emotional EALs were associated with increased anatomical centrality and segregation in emotion regulation regions. Sex moderated the associations between EALs and measures of centrality; with decreased centrality of salience and emotion regulation regions with increased general EALs in females, and increased centrality in salience regions with higher physical and emotional EALs in males. Increased segregation of salience regions was associated with increased general EALs in males. Centrality of the amygdala was associated with physical symptoms, and segregation of salience regions was correlated with higher somatization in men only. Conclusions: Emotion regulation and salience regions are susceptible to topological brain restructuring associated with EALs. The male and female brains appear to be differently affected by specific types of EALs. Keywords: Early adverse traumatic life events, Centrality, Segregation, Network metrics, Moderating effects of sex, Emotion regulation network, Salience network
url http://www.sciencedirect.com/science/article/pii/S2352289516300273
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spelling doaj-1cfbcc0d9b8a4f5c975ab04989bfb4e72020-11-24T22:02:44ZengElsevierNeurobiology of Stress2352-28952017-12-0171626Early adverse life events are associated with altered brain network architecture in a sex- dependent mannerArpana Gupta, PhD0Emeran A. Mayer, MD, PhD1Jonathan R. Acosta, BSc2Kareem Hamadani, BSc3Carinna Torgerson, BA4John D. van Horn, PhD5Lin Chang, MD6Bruce Naliboff, PhD7Kirsten Tillisch, MD8Jennifer S. Labus, PhD9G. Oppenheimer Center for Neurobiology of Stress and Resilience, UCLA, Los Angeles, CA, United States; Department of Medicine, UCLA, Los Angeles, CA, United States; UCLA Vatche and Tamar Manoukian Division of Digestive Diseases, UCLA, Los Angeles, CA, United States; Corresponding author. The G. Oppenheimer Center for Neurobiology of Stress and Resilience, Division of Digestive Diseases, David School of Medicine at UCLA, CHS 42-210 MC737818, 10833 Le Conte Avenue, United States.G. Oppenheimer Center for Neurobiology of Stress and Resilience, UCLA, Los Angeles, CA, United States; Department of Medicine, UCLA, Los Angeles, CA, United States; Department of Psychiatry, UCLA, Los Angeles, CA, United States; UCLA Vatche and Tamar Manoukian Division of Digestive Diseases, UCLA, Los Angeles, CA, United States; Ahmanson-Lovelace Brain Mapping Center, UCLA, Los Angeles, CA, United StatesG. Oppenheimer Center for Neurobiology of Stress and Resilience, UCLA, Los Angeles, CA, United StatesG. Oppenheimer Center for Neurobiology of Stress and Resilience, UCLA, Los Angeles, CA, United StatesThe Institute for Neuroimaging and Informatics (INI) and Laboratory of NeuroImaging (LONI), Keck School of Medicine at USC, Los Angeles, CA, United StatesThe Institute for Neuroimaging and Informatics (INI) and Laboratory of NeuroImaging (LONI), Keck School of Medicine at USC, Los Angeles, CA, United StatesG. Oppenheimer Center for Neurobiology of Stress and Resilience, UCLA, Los Angeles, CA, United States; Department of Medicine, UCLA, Los Angeles, CA, United States; UCLA Vatche and Tamar Manoukian Division of Digestive Diseases, UCLA, Los Angeles, CA, United StatesG. Oppenheimer Center for Neurobiology of Stress and Resilience, UCLA, Los Angeles, CA, United States; Department of Medicine, UCLA, Los Angeles, CA, United States; Department of Psychiatry, UCLA, Los Angeles, CA, United States; UCLA Vatche and Tamar Manoukian Division of Digestive Diseases, UCLA, Los Angeles, CA, United States; UCLA Brain Research Institute, Los Angeles, CA, United StatesG. Oppenheimer Center for Neurobiology of Stress and Resilience, UCLA, Los Angeles, CA, United States; Department of Medicine, UCLA, Los Angeles, CA, United States; UCLA Vatche and Tamar Manoukian Division of Digestive Diseases, UCLA, Los Angeles, CA, United States; Department of Integrative Medicine, GLA VHA, Los Angeles, CA, United StatesG. Oppenheimer Center for Neurobiology of Stress and Resilience, UCLA, Los Angeles, CA, United States; Department of Medicine, UCLA, Los Angeles, CA, United States; Department of Psychiatry, UCLA, Los Angeles, CA, United States; UCLA Vatche and Tamar Manoukian Division of Digestive Diseases, UCLA, Los Angeles, CA, United States; UCLA Brain Research Institute, Los Angeles, CA, United StatesIntroduction: Early adverse life events (EALs) increase the risk for chronic medical and psychiatric disorders by altering early neurodevelopment. The aim of this study was to examine associations between EALs and network properties of core brain regions in the emotion regulation and salience networks, and to test the influence of sex on these associations. Methods: Resting-state functional and diffusion tensor magnetic resonance imaging were obtained in healthy individuals (61 men, 63 women). Functional and anatomical network properties of centrality and segregation were calculated for the core regions of the two networks using graph theory. Moderator analyses were applied to test hypotheses. Results: The type of adversity experienced influences brain wiring differently, as higher general EALs were associated with decreased functional and anatomical centrality in salience and emotion regulation regions, while physical and emotional EALs were associated with increased anatomical centrality and segregation in emotion regulation regions. Sex moderated the associations between EALs and measures of centrality; with decreased centrality of salience and emotion regulation regions with increased general EALs in females, and increased centrality in salience regions with higher physical and emotional EALs in males. Increased segregation of salience regions was associated with increased general EALs in males. Centrality of the amygdala was associated with physical symptoms, and segregation of salience regions was correlated with higher somatization in men only. Conclusions: Emotion regulation and salience regions are susceptible to topological brain restructuring associated with EALs. The male and female brains appear to be differently affected by specific types of EALs. Keywords: Early adverse traumatic life events, Centrality, Segregation, Network metrics, Moderating effects of sex, Emotion regulation network, Salience networkhttp://www.sciencedirect.com/science/article/pii/S2352289516300273