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Utility of the cumulative stress and mismatch hypotheses in understanding the neurobiological impacts of childhood abuse and recent stress in youth with emerging mental disorder
Childhood abuse has an enduring impact on the brain's stress system. Whether the effects of childhood abuse and adulthood stress are additive (cumulative stress hypothesis) or interactive (mismatch hypothesis) is widely disputed, however. The primary aim of this study was to test the utility of...
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Published in: | Human brain mapping 2017-05, Vol.38 (5), p.2709-2721 |
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description | Childhood abuse has an enduring impact on the brain's stress system. Whether the effects of childhood abuse and adulthood stress are additive (cumulative stress hypothesis) or interactive (mismatch hypothesis) is widely disputed, however. The primary aim of this study was to test the utility of the cumulative stress and mismatch hypotheses in understanding brain and behaviour. We recruited 64 individuals (aged 14–26) from a specialised clinic for assessment and early intervention of mental health problems in young people. A T1‐weighted MRI, a resting state fMRI and clinical assessment were acquired from each participant. Grey matter estimates and resting state functional connectivity (rsFC) of the hippocampus, amygdala and anterior cingulate cortex (ACC) were determined using segmentation and seed‐to‐voxel rsFC analyses. We explored the effects of childhood abuse and recent stress on the structure and function of the regions of interest within general linear models. Worse psychiatric symptoms were significantly related to higher levels of life time stress. Individuals with mismatched childhood and recent stress levels had reduced left hippocampal volume, reduced ACC‐ventrolateral prefrontal cortex rsFC and greater ACC‐hippocampus rsFC, compared to individuals with matched childhood and recent stress levels. These results show specific utility of the cumulative stress hypothesis in understanding psychiatric symptomatology and of the mismatch hypothesis in modelling hippocampal grey matter, prefrontal rsFC, and prefrontal‐hippocampal rsFC. We provide novel evidence for the enduring impact of childhood abuse on stress reactivity in a clinical population, and demonstrate the distinct effects of stress in different systems. Hum Brain Mapp 38:2709–2721, 2017. © 2017 Wiley Periodicals, Inc. |
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Worse psychiatric symptoms were significantly related to higher levels of life time stress. Individuals with mismatched childhood and recent stress levels had reduced left hippocampal volume, reduced ACC‐ventrolateral prefrontal cortex rsFC and greater ACC‐hippocampus rsFC, compared to individuals with matched childhood and recent stress levels. These results show specific utility of the cumulative stress hypothesis in understanding psychiatric symptomatology and of the mismatch hypothesis in modelling hippocampal grey matter, prefrontal rsFC, and prefrontal‐hippocampal rsFC. We provide novel evidence for the enduring impact of childhood abuse on stress reactivity in a clinical population, and demonstrate the distinct effects of stress in different systems. 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Whether the effects of childhood abuse and adulthood stress are additive (cumulative stress hypothesis) or interactive (mismatch hypothesis) is widely disputed, however. The primary aim of this study was to test the utility of the cumulative stress and mismatch hypotheses in understanding brain and behaviour. We recruited 64 individuals (aged 14–26) from a specialised clinic for assessment and early intervention of mental health problems in young people. A T1‐weighted MRI, a resting state fMRI and clinical assessment were acquired from each participant. Grey matter estimates and resting state functional connectivity (rsFC) of the hippocampus, amygdala and anterior cingulate cortex (ACC) were determined using segmentation and seed‐to‐voxel rsFC analyses. We explored the effects of childhood abuse and recent stress on the structure and function of the regions of interest within general linear models. Worse psychiatric symptoms were significantly related to higher levels of life time stress. Individuals with mismatched childhood and recent stress levels had reduced left hippocampal volume, reduced ACC‐ventrolateral prefrontal cortex rsFC and greater ACC‐hippocampus rsFC, compared to individuals with matched childhood and recent stress levels. These results show specific utility of the cumulative stress hypothesis in understanding psychiatric symptomatology and of the mismatch hypothesis in modelling hippocampal grey matter, prefrontal rsFC, and prefrontal‐hippocampal rsFC. We provide novel evidence for the enduring impact of childhood abuse on stress reactivity in a clinical population, and demonstrate the distinct effects of stress in different systems. Hum Brain Mapp 38:2709–2721, 2017. © 2017 Wiley Periodicals, Inc.</description><subject>Adolescent</subject><subject>Adult</subject><subject>Brain - diagnostic imaging</subject><subject>Child Abuse - psychology</subject><subject>childhood abuse</subject><subject>Female</subject><subject>grey matter</subject><subject>Humans</subject><subject>Image Processing, Computer-Assisted</subject><subject>Linear Models</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Mental Disorders - diagnostic imaging</subject><subject>MRI</subject><subject>Rest</subject><subject>resting state</subject><subject>stress</subject><subject>Stress, Psychological - diagnostic imaging</subject><subject>Surveys and Questionnaires</subject><subject>Young Adult</subject><issn>1065-9471</issn><issn>1097-0193</issn><issn>1097-0193</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNqNks9qFTEUhwdRbK0ufAEJuNHFtMlMZpJsBC1qhYobuw6Z5MydlMzkmj8t97F8QzP3tkUFQQhJIF--cxJ-VfWS4FOCcXM2DfNp03YdfVQdEyxYjYloH6_7vqsFZeSoehbjNcaEdJg8rY4a3nQ9Y-y4-nmVrLNph_yI0gRI5zk7lewNoJgCxIjUYtBs46ySntC02_qCRYjILigvBkJMhbDLZn99gRz8YL3zG6uVQ3beKp3iateTdWby3iA15Ah7bwANS7qvVIw7n9OEbm2ZYIawWb1zQYrK2OhDqfe8ejIqF-HF3XpSXX36-P38or789vnL-fvLWlPW07rThjFOoWeEDq1RnNGBc4ZHwM1Iu150Rg2U49Fo0XJBiOCGE6VGGBtjDG1PqncH7zYPM5i10aCc3AY7q7CTXln558liJ7nxN7LnfRmkCN7cCYL_kSEmWb5Rg3NqAZ-jJKUqL63i5j9QRilte9YX9PVf6LXPYSk_USjeEd4JIQr19kDp4GMMMD70TbBcMyNLZuQ-M4V99ftDH8j7kBTg7ADcWge7f5vkxYevB-UvVXDQyQ</recordid><startdate>201705</startdate><enddate>201705</enddate><creator>Paquola, Casey</creator><creator>Bennett, Maxwell R</creator><creator>Hatton, Sean N</creator><creator>Hermens, Daniel F.</creator><creator>Lagopoulos, Jim</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0190-4103</orcidid><orcidid>https://orcid.org/0000-0002-9149-8726</orcidid></search><sort><creationdate>201705</creationdate><title>Utility of the cumulative stress and mismatch hypotheses in understanding the neurobiological impacts of childhood abuse and recent stress in youth with emerging mental disorder</title><author>Paquola, Casey ; Bennett, Maxwell R ; Hatton, Sean N ; Hermens, Daniel F. ; Lagopoulos, Jim</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4764-5cd7784e6714b3da874b8870fe02f45695dab480fdc93891198d81aafef2ddd43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Adolescent</topic><topic>Adult</topic><topic>Brain - diagnostic imaging</topic><topic>Child Abuse - psychology</topic><topic>childhood abuse</topic><topic>Female</topic><topic>grey matter</topic><topic>Humans</topic><topic>Image Processing, Computer-Assisted</topic><topic>Linear Models</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Mental Disorders - diagnostic imaging</topic><topic>MRI</topic><topic>Rest</topic><topic>resting state</topic><topic>stress</topic><topic>Stress, Psychological - diagnostic imaging</topic><topic>Surveys and Questionnaires</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Paquola, Casey</creatorcontrib><creatorcontrib>Bennett, Maxwell R</creatorcontrib><creatorcontrib>Hatton, Sean N</creatorcontrib><creatorcontrib>Hermens, Daniel F.</creatorcontrib><creatorcontrib>Lagopoulos, Jim</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Human brain mapping</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Paquola, Casey</au><au>Bennett, Maxwell R</au><au>Hatton, Sean N</au><au>Hermens, Daniel F.</au><au>Lagopoulos, Jim</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Utility of the cumulative stress and mismatch hypotheses in understanding the neurobiological impacts of childhood abuse and recent stress in youth with emerging mental disorder</atitle><jtitle>Human brain mapping</jtitle><addtitle>Hum Brain Mapp</addtitle><date>2017-05</date><risdate>2017</risdate><volume>38</volume><issue>5</issue><spage>2709</spage><epage>2721</epage><pages>2709-2721</pages><issn>1065-9471</issn><issn>1097-0193</issn><eissn>1097-0193</eissn><abstract>Childhood abuse has an enduring impact on the brain's stress system. Whether the effects of childhood abuse and adulthood stress are additive (cumulative stress hypothesis) or interactive (mismatch hypothesis) is widely disputed, however. The primary aim of this study was to test the utility of the cumulative stress and mismatch hypotheses in understanding brain and behaviour. We recruited 64 individuals (aged 14–26) from a specialised clinic for assessment and early intervention of mental health problems in young people. A T1‐weighted MRI, a resting state fMRI and clinical assessment were acquired from each participant. Grey matter estimates and resting state functional connectivity (rsFC) of the hippocampus, amygdala and anterior cingulate cortex (ACC) were determined using segmentation and seed‐to‐voxel rsFC analyses. We explored the effects of childhood abuse and recent stress on the structure and function of the regions of interest within general linear models. Worse psychiatric symptoms were significantly related to higher levels of life time stress. Individuals with mismatched childhood and recent stress levels had reduced left hippocampal volume, reduced ACC‐ventrolateral prefrontal cortex rsFC and greater ACC‐hippocampus rsFC, compared to individuals with matched childhood and recent stress levels. These results show specific utility of the cumulative stress hypothesis in understanding psychiatric symptomatology and of the mismatch hypothesis in modelling hippocampal grey matter, prefrontal rsFC, and prefrontal‐hippocampal rsFC. We provide novel evidence for the enduring impact of childhood abuse on stress reactivity in a clinical population, and demonstrate the distinct effects of stress in different systems. 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subjects | Adolescent Adult Brain - diagnostic imaging Child Abuse - psychology childhood abuse Female grey matter Humans Image Processing, Computer-Assisted Linear Models Magnetic Resonance Imaging Male Mental Disorders - diagnostic imaging MRI Rest resting state stress Stress, Psychological - diagnostic imaging Surveys and Questionnaires Young Adult |
title | Utility of the cumulative stress and mismatch hypotheses in understanding the neurobiological impacts of childhood abuse and recent stress in youth with emerging mental disorder |
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