Neural Network Modulation by Trauma as a Marker of Resilience: Differences Between Veterans With Posttraumatic Stress Disorder and Resilient Controls

IMPORTANCE Posttraumatic stress disorder (PTSD) and resilience reflect 2 distinct outcomes after exposure to potentially traumatic events. The neural mechanisms underlying these different outcomes are not well understood. OBJECTIVE To examine the effect of trauma on synchronous neural interactions f...

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Veröffentlicht in:JAMA psychiatry (Chicago, Ill.) Ill.), 2013-04, Vol.70 (4), p.410-418
Hauptverfasser: James, Lisa M, Engdahl, Brian E, Leuthold, Art C, Lewis, Scott M, Van Kampen, Emily, Georgopoulos, Apostolos P
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container_issue 4
container_start_page 410
container_title JAMA psychiatry (Chicago, Ill.)
container_volume 70
creator James, Lisa M
Engdahl, Brian E
Leuthold, Art C
Lewis, Scott M
Van Kampen, Emily
Georgopoulos, Apostolos P
description IMPORTANCE Posttraumatic stress disorder (PTSD) and resilience reflect 2 distinct outcomes after exposure to potentially traumatic events. The neural mechanisms underlying these different outcomes are not well understood. OBJECTIVE To examine the effect of trauma on synchronous neural interactions for veterans with PTSD and resilient controls using magnetoencephalography. DESIGN Participants underwent diagnostic interviews, a measure of exposure to potentially traumatic events, and magnetoencephalography. SETTING US Department of Veterans Affairs medical center. PARTICIPANTS Eighty-six veterans with PTSD and 113 resilient control veterans recruited from a large Midwestern medical center. MAIN OUTCOME MEASURES Multiple regression analyses were performed to examine the effect of lifetime trauma on global and local synchronous neural interactions. In analyses examining the local synchronous neural interactions, the partial regression coefficient indicates the strength and direction of the effect of trauma on the synchronous interactions between the 2 neural signals recorded by a pair of sensors. The partial regression coefficient, or slope, is the primary outcome measure for these analyses. RESULTS Global synchronous neural interactions were significantly modulated downward with increasing lifetime trauma scores in resilient control veterans (P = .003) but not in veterans with PTSD (P = .91). This effect, which was primarily characterized by negative slopes (ie, decorrelations) in small neural networks, was strongest in the right superior temporal gyrus. Significant negative slopes were more common, stronger, and observed between sensors at shorter distances than positive slopes in both hemispheres (P 
doi_str_mv 10.1001/jamapsychiatry.2013.878
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The neural mechanisms underlying these different outcomes are not well understood. OBJECTIVE To examine the effect of trauma on synchronous neural interactions for veterans with PTSD and resilient controls using magnetoencephalography. DESIGN Participants underwent diagnostic interviews, a measure of exposure to potentially traumatic events, and magnetoencephalography. SETTING US Department of Veterans Affairs medical center. PARTICIPANTS Eighty-six veterans with PTSD and 113 resilient control veterans recruited from a large Midwestern medical center. MAIN OUTCOME MEASURES Multiple regression analyses were performed to examine the effect of lifetime trauma on global and local synchronous neural interactions. In analyses examining the local synchronous neural interactions, the partial regression coefficient indicates the strength and direction of the effect of trauma on the synchronous interactions between the 2 neural signals recorded by a pair of sensors. The partial regression coefficient, or slope, is the primary outcome measure for these analyses. RESULTS Global synchronous neural interactions were significantly modulated downward with increasing lifetime trauma scores in resilient control veterans (P = .003) but not in veterans with PTSD (P = .91). This effect, which was primarily characterized by negative slopes (ie, decorrelations) in small neural networks, was strongest in the right superior temporal gyrus. Significant negative slopes were more common, stronger, and observed between sensors at shorter distances than positive slopes in both hemispheres (P &lt; .001 for all) for controls but not for veterans with PTSD. CONCLUSIONS Neural modulation involving decorrelation of neural networks in the right superior temporal gyrus and, to a lesser extent, other areas distinguishes resilient veterans from those with PTSD and is postulated to have an important role in healthy response to trauma.</description><identifier>ISSN: 2168-622X</identifier><identifier>EISSN: 2168-6238</identifier><identifier>DOI: 10.1001/jamapsychiatry.2013.878</identifier><identifier>PMID: 23426853</identifier><language>eng</language><publisher>Chicago, IL: American Medical Association</publisher><subject>Adult ; Adult and adolescent clinical studies ; Aged ; Aged, 80 and over ; Anxiety disorders. 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The neural mechanisms underlying these different outcomes are not well understood. OBJECTIVE To examine the effect of trauma on synchronous neural interactions for veterans with PTSD and resilient controls using magnetoencephalography. DESIGN Participants underwent diagnostic interviews, a measure of exposure to potentially traumatic events, and magnetoencephalography. SETTING US Department of Veterans Affairs medical center. PARTICIPANTS Eighty-six veterans with PTSD and 113 resilient control veterans recruited from a large Midwestern medical center. MAIN OUTCOME MEASURES Multiple regression analyses were performed to examine the effect of lifetime trauma on global and local synchronous neural interactions. In analyses examining the local synchronous neural interactions, the partial regression coefficient indicates the strength and direction of the effect of trauma on the synchronous interactions between the 2 neural signals recorded by a pair of sensors. The partial regression coefficient, or slope, is the primary outcome measure for these analyses. RESULTS Global synchronous neural interactions were significantly modulated downward with increasing lifetime trauma scores in resilient control veterans (P = .003) but not in veterans with PTSD (P = .91). This effect, which was primarily characterized by negative slopes (ie, decorrelations) in small neural networks, was strongest in the right superior temporal gyrus. Significant negative slopes were more common, stronger, and observed between sensors at shorter distances than positive slopes in both hemispheres (P &lt; .001 for all) for controls but not for veterans with PTSD. CONCLUSIONS Neural modulation involving decorrelation of neural networks in the right superior temporal gyrus and, to a lesser extent, other areas distinguishes resilient veterans from those with PTSD and is postulated to have an important role in healthy response to trauma.</description><subject>Adult</subject><subject>Adult and adolescent clinical studies</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Anxiety disorders. 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Psychiatry</subject><subject>Regression analysis</subject><subject>Resilience, Psychological</subject><subject>Stress Disorders, Post-Traumatic - physiopathology</subject><subject>Stress Disorders, Post-Traumatic - psychology</subject><subject>United Nations</subject><subject>Veterans</subject><subject>Veterans - psychology</subject><subject>Young Adult</subject><issn>2168-622X</issn><issn>2168-6238</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkdtu1DAQhiMEolXpC3ABlhASN7v4EMcOd7AcpbYgKIe7aNaZqN4m8eJxhPZBeF-83WUr8I1H1jffWPMXxWPB54Jz8XwFA6xp4648pLiZSy7U3Bp7pziWorKzSip791DLH0fFKdGK52M5L5W9XxxJVcrKanVc_L7AKULPLjD9CvGanYd26iH5MLLlhl1GmAZgQAzYOcRrjCx07DOS7z2ODl-w177rMG5rYq-yA3Fk3zBhhJHYd5-u2KdAKd14knfsS4pIlNsoxDbrYGwPvsQWYUwx9PSguNdBT3i6v0-Kr2_fXC7ez84-vvuweHk2A1nXaVaWVVVx23aoJVrHHRrprOKd4aVoZa05iE6glFzq1nWSV6VamvxmykpbDuqkeLbzrmP4OSGlZvDksO9hxDBRI5TMC9N5uRl98h-6ClMc8-9uKG2UrnWmzI5yMRBF7Jp19APETSN4sw2v-Te8Zhtes_M_2vun5YDtoe9vVBl4ugeAHPRd3rDzdMsZYawtTeYe7rg86HZ6pctaGPUHIRqwaw</recordid><startdate>20130401</startdate><enddate>20130401</enddate><creator>James, Lisa M</creator><creator>Engdahl, Brian E</creator><creator>Leuthold, Art C</creator><creator>Lewis, Scott M</creator><creator>Van Kampen, Emily</creator><creator>Georgopoulos, Apostolos P</creator><general>American Medical Association</general><scope>IQODW</scope><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>K9.</scope><scope>NAPCQ</scope><scope>7X8</scope></search><sort><creationdate>20130401</creationdate><title>Neural Network Modulation by Trauma as a Marker of Resilience: Differences Between Veterans With Posttraumatic Stress Disorder and Resilient Controls</title><author>James, Lisa M ; Engdahl, Brian E ; Leuthold, Art C ; Lewis, Scott M ; Van Kampen, Emily ; Georgopoulos, Apostolos P</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a299t-4466608dfe52e8c0ce72c830f7041d2950a1f1e22025dcf20643b7a1f746580a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Adult</topic><topic>Adult and adolescent clinical studies</topic><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Anxiety disorders. Neuroses</topic><topic>Biological and medical sciences</topic><topic>Brain - physiopathology</topic><topic>Case-Control Studies</topic><topic>Differences</topic><topic>Electroencephalography</topic><topic>Female</topic><topic>Humans</topic><topic>Magnetoencephalography</topic><topic>Male</topic><topic>Medical sciences</topic><topic>Middle Aged</topic><topic>Nerve Net - physiopathology</topic><topic>Neural networks</topic><topic>Post traumatic stress disorder</topic><topic>Psychiatric Status Rating Scales</topic><topic>Psychology. Psychoanalysis. Psychiatry</topic><topic>Psychopathology. Psychiatry</topic><topic>Regression analysis</topic><topic>Resilience, Psychological</topic><topic>Stress Disorders, Post-Traumatic - physiopathology</topic><topic>Stress Disorders, Post-Traumatic - psychology</topic><topic>United Nations</topic><topic>Veterans</topic><topic>Veterans - psychology</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>James, Lisa M</creatorcontrib><creatorcontrib>Engdahl, Brian E</creatorcontrib><creatorcontrib>Leuthold, Art C</creatorcontrib><creatorcontrib>Lewis, Scott M</creatorcontrib><creatorcontrib>Van Kampen, Emily</creatorcontrib><creatorcontrib>Georgopoulos, Apostolos P</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>MEDLINE - Academic</collection><jtitle>JAMA psychiatry (Chicago, Ill.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>James, Lisa M</au><au>Engdahl, Brian E</au><au>Leuthold, Art C</au><au>Lewis, Scott M</au><au>Van Kampen, Emily</au><au>Georgopoulos, Apostolos P</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neural Network Modulation by Trauma as a Marker of Resilience: Differences Between Veterans With Posttraumatic Stress Disorder and Resilient Controls</atitle><jtitle>JAMA psychiatry (Chicago, Ill.)</jtitle><addtitle>JAMA Psychiatry</addtitle><date>2013-04-01</date><risdate>2013</risdate><volume>70</volume><issue>4</issue><spage>410</spage><epage>418</epage><pages>410-418</pages><issn>2168-622X</issn><eissn>2168-6238</eissn><abstract>IMPORTANCE Posttraumatic stress disorder (PTSD) and resilience reflect 2 distinct outcomes after exposure to potentially traumatic events. The neural mechanisms underlying these different outcomes are not well understood. OBJECTIVE To examine the effect of trauma on synchronous neural interactions for veterans with PTSD and resilient controls using magnetoencephalography. DESIGN Participants underwent diagnostic interviews, a measure of exposure to potentially traumatic events, and magnetoencephalography. SETTING US Department of Veterans Affairs medical center. PARTICIPANTS Eighty-six veterans with PTSD and 113 resilient control veterans recruited from a large Midwestern medical center. MAIN OUTCOME MEASURES Multiple regression analyses were performed to examine the effect of lifetime trauma on global and local synchronous neural interactions. In analyses examining the local synchronous neural interactions, the partial regression coefficient indicates the strength and direction of the effect of trauma on the synchronous interactions between the 2 neural signals recorded by a pair of sensors. The partial regression coefficient, or slope, is the primary outcome measure for these analyses. RESULTS Global synchronous neural interactions were significantly modulated downward with increasing lifetime trauma scores in resilient control veterans (P = .003) but not in veterans with PTSD (P = .91). This effect, which was primarily characterized by negative slopes (ie, decorrelations) in small neural networks, was strongest in the right superior temporal gyrus. Significant negative slopes were more common, stronger, and observed between sensors at shorter distances than positive slopes in both hemispheres (P &lt; .001 for all) for controls but not for veterans with PTSD. CONCLUSIONS Neural modulation involving decorrelation of neural networks in the right superior temporal gyrus and, to a lesser extent, other areas distinguishes resilient veterans from those with PTSD and is postulated to have an important role in healthy response to trauma.</abstract><cop>Chicago, IL</cop><pub>American Medical Association</pub><pmid>23426853</pmid><doi>10.1001/jamapsychiatry.2013.878</doi><tpages>9</tpages></addata></record>
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subjects Adult
Adult and adolescent clinical studies
Aged
Aged, 80 and over
Anxiety disorders. Neuroses
Biological and medical sciences
Brain - physiopathology
Case-Control Studies
Differences
Electroencephalography
Female
Humans
Magnetoencephalography
Male
Medical sciences
Middle Aged
Nerve Net - physiopathology
Neural networks
Post traumatic stress disorder
Psychiatric Status Rating Scales
Psychology. Psychoanalysis. Psychiatry
Psychopathology. Psychiatry
Regression analysis
Resilience, Psychological
Stress Disorders, Post-Traumatic - physiopathology
Stress Disorders, Post-Traumatic - psychology
United Nations
Veterans
Veterans - psychology
Young Adult
title Neural Network Modulation by Trauma as a Marker of Resilience: Differences Between Veterans With Posttraumatic Stress Disorder and Resilient Controls
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