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Original Article |

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

Lisa M. James, PhD; Brian E. Engdahl, PhD; Art C. Leuthold, PhD; Scott M. Lewis, MD, PhD; Emily Van Kampen, MS; Apostolos P. Georgopoulos, MD, PhD
JAMA Psychiatry. 2013;70(4):410-418. doi:10.1001/jamapsychiatry.2013.878.
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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 < .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.

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Figures

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Figure 1. Frequency distributions of trauma scores. A, Control group (n = 113). B, Posttraumatic stress group (n = 86).

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Figure 2. The mean absolute value of the zero-lag z -transformed correlation is plotted against trauma score. A, Control group. B, Posttraumatic stress group.

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Figure 3. Two-dimensional sensor-space plots depicting the negative modulation of local synchronous neural interactions. A, Control group. B, Posttraumatic stress group. The radius of the ellipses and color intensity are proportional to the maximum trauma vs |z0ij| slope for a specific sensor (of 247 possible). A indicates anterior; P, posterior; L, left; and R, right. Approximate location of cortical networks: 1, right superior temporal; 2, right inferior frontal; 3, left parietal; 4, left temporal; and 5, left inferior frontal.

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Figure 4. Two-dimensional sensor-space plots depicting the positive modulation of local synchronous neural interactions. A, Control group. B, Posttraumatic stress disorder group. The radius of the ellipses and color intensity are proportional to the maximum trauma vs |z0ij| slope for a specific sensor (of 247 possible). A indicates anterior; P, posterior; L, left; and R, right. Approximate location of cortical networks: 1, right inferior parietal; 2, right occipital; 3, left parietal; and 4, left temporal.

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Figure 5. Two-dimensional and 3-dimensional contour plots. A, 2-Dimensional contour plot of color-coded negative trauma vs |z0ij| slopes interpolated linearly in sensor space in the control group. B, The same data are shown in a 3-dimensional surface plot using Delaunay triangulation of magnetoencephalography sensor coordinates. A indicates anterior; P, posterior; L, left; and R, right.

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Figure 6. Mean intersensor distances by kind of effect, hemisphere, and group. N indicates negative slope; P, positive slope; PTSD, posttraumatic stress disorder. Control group (both hemispheres): N < P (P < .001); PTSD group (left hemisphere): N vs P (P = .11); PTSD group (right hemisphere): N < P (P = .03).

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