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Disturbed effective connectivity patterns in an intrinsic triple network model are associated with posttraumatic stress disorder

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Abstract

Background

Disturbance of the triple network model was recently proposed to be associated with the occurrence of posttraumatic stress disorder (PTSD) symptoms. Based on resting-state dynamic causal modeling (rs-DCM) analysis, we investigated the neurobiological model at a neuronal level along with potential neuroimaging biomarkers for identifying individuals with PTSD.

Methods

We recruited survivors of a devastating typhoon including 27 PTSD patients, 33 trauma-exposed controls (TECs), and 30 healthy controls without trauma exposure. All subjects underwent resting-state functional magnetic resonance imaging. Independent components analysis was used to identify triple networks. Detailed effective connectivity patterns were estimated by rs-DCM analysis. Spearman correlation analysis was performed on aberrant DCM parameters with clinical assessment results relevant to PTSD diagnosis. We also carried out step-wise binary logistic regression and receiver operating characteristic curve (ROC) analysis to confirm the capacity of altered effective connectivity parameters to distinguish PTSD patients.

Results

Within the executive control network, enhanced positive connectivity from the left posterior parietal cortex to the left dorsolateral prefrontal cortex was correlated with intrusion symptoms and showed good performance (area under the receiver operating characteristic curve = 0.879) in detecting PTSD patients. In the salience network, we observed a decreased causal flow from the right amygdala to the right insula and a lower transit value for the right amygdala in PTSD patients relative to TECs.

Conclusion

Altered effective connectivity patterns in the triple network may reflect the occurrence of PTSD symptoms, providing a potential biomarker for detecting patients. Our findings shed new insight into the neural pathophysiology of PTSD.

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Funding

This work was supported by the grants from the National Nature Science Foundation of China [Grant Numbers 81671672, 81301209, 81301155, 81460261, and 81201077]; the Key Science and Technology Project of Hainan Province [grant number ZDYF2016156]; and the Chinese Key Grant [Grant Number BWS11J063]; Jiangsu Provincial Medical Youth Talent [grant number QNRC2016888]; Foundations of Commission of Health and Family Planning of Wuxi and Jiangsu Province [grant number Z201610, H201656].

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Author notes

  1. Yifei Weng, Rongfeng Qi and Li Zhang contributed equally to this work.

Authors and Affiliations

  1. Department of Medical Imaging, Jinling Hospital, Medical School of Nanjing University, 305 Zhongshan East Road, Xuanwu District, Nanjing, 210002, Jiangsu Province, China

    Yifei Weng, Rongfeng Qi, Jun Ke, Qiang Xu, Yuan Zhong & Guangming Lu

  2. Mental Health Institute, the Second Xiangya Hospital, National Technology Institute of Psychiatry, Key Laboratory of Psychiatry and Mental Health of Hunan Province, Central South University, No.139 Middle Renmin Road, Changsha, 410011, Hunan Province, China

    Li Zhang

  3. Department of Radiology, The Affiliated Yixing Hospital of Jiangsu University, 75 Tongzhenguan Road, Wuxi, 214200, Jiangsu Province, China

    Yifeng Luo & Zhihong Cao

  4. Department of Radiology, Hainan General Hospital, Haikou, 570311, China

    Jianjun Li & Feng Chen

Authors
  1. Yifei Weng
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  2. Rongfeng Qi
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  3. Li Zhang
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  4. Yifeng Luo
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  5. Jun Ke
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  7. Yuan Zhong
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  9. Feng Chen
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  10. Zhihong Cao
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  11. Guangming Lu
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Contributions

YW was involved in the experimental design, data analysis, and writing of the manuscript. RQ, ZC, FC, and GL designed the study. JK, QX, and YZ analyzed the data. YL, JL, and LZ acquired the data.

Corresponding authors

Correspondence to Feng Chen, Zhihong Cao or Guangming Lu.

Ethics declarations

All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. It was approved by the ethics committee of Jinling Hospital, People’s Hospital of Hainan Province, and the Second Xiangya Hospital of Central South University. All participants provided written informed consent after a detailed description of this study.

Conflict of interest

The authors declare that they have no conflicts of interest.

Electronic supplementary material

Supplemental Table 1

(DOCX 65 kb)

Appendix Figure 1

Results of the post-hoc model selection procedure. In each network model of per group, both the log-posterior and model posterior probabilities are examined. The full model is the winning model in each group with a maximum posterior probability of almost 1. (PNG 271 kb)

High resolution image

(TIF 365 kb)

Appendix Figure 2

Result of neural and hemodynamic parameters. All the detailed neural and hemodynamic parameters are displayed in the form of bar chart. The transit values in right amygdala of PTSD group are lower than that of TEC group. * Significant different (P < 0.05); error bar, standard error (S.E.). (PNG 307 kb)

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(TIF 631 kb)

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Weng, Y., Qi, R., Zhang, L. et al. Disturbed effective connectivity patterns in an intrinsic triple network model are associated with posttraumatic stress disorder. Neurol Sci 40, 339–349 (2019). https://doi.org/10.1007/s10072-018-3638-1

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