Skip to main content
SpringerLink
Log in

Anomalous gray matter structural networks in recent onset post-traumatic stress disorder

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Alterations of the topological organization of abnormal regions or network-level structural aberrations are still poorly understood for post-traumatic stress disorder (PTSD). Herein, we investigated brain structural networks in recent-onset PTSD patients, all affected by the coalmine-flood disaster. Cortical networks were studied in recent onset PTSD patients (n = 15) and matched healthy controls (n = 25). Cortical networks were constructed by thresholding correlation matrices of 150 regions and quantified using graph theoretical approaches. Contributions of high-degree nodes, and regional and global network measures, including degree and betweenness, were studied. Compared with healthy controls, PTSD patients showed altered quantitative values in global network properties, characterized by shorter path length and higher clustering. Moreover, PTSD patients exhibited decreased connectivity in the right lingual gyrus, parahippocampal gyrus, left supramarginal gyrus, parahippocampal gyrus, bilateral superior and inferior frontal gyrus, superior frontal gyrus, and posterior cingulate gyrus. Nodal centrality decreased predominantly in the occipital regions (lingual gyrus) and default-mode regions, while increased correlations and centralities were observed in the medial temporal lobe and posterior cingulate cortex. PTSD-related networks exhibited a less efficient organization and regional connectivity. According to these findings, we conclude that regional connections involving fear-processing and re-experiential-processing cortex may play a role in maintaining or adapting to PTSD pathology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bremner, J. D., Vermetten, E., Vythilingam, M., Afzal, N., Schmahl, C., Elzinga, B., & Charney, D. S. (2004). Neural correlates of the classic color and emotional stroop in women with abuse-related posttraumatic stress disorder. Biological Psychiatry, 55(6), 612–620. doi:10.1016/j.biopsych.2003.10.001.

    Article  PubMed  Google Scholar 

  • Chen, S., Xia, W., Li, L., Liu, J., He, Z., Zhang, Z., Yan, L., Zhang, J., & Hu, D. (2006). Gray matter density reduction in the insula in fire survivors with posttraumatic stress disorder: A voxel-based morphometric study. Psychiatry Research, 146(1), 65–72. doi:10.1016/j.pscychresns.2005.09.006.

    Article  PubMed  Google Scholar 

  • Chen, Y., Fu, K., Feng, C., Tang, L., Zhang, J., Huan, Y., Cui, J., Mu, Y., Qi, S., Xiong, L., Ma, C., Wang, H., Tan, Q., & Yin, H. (2012). Different regional gray matter loss in recent onset PTSD and non PTSD after a single prolonged trauma exposure. PloS One, 7(11), e48298. doi:10.1371/journal.pone.0048298.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung, Y. A., Kim, S. H., Chung, S. K., Chae, J.-H., Yang, D. W., Sohn, H. S., & Jeong, J. (2006). Alterations in cerebral perfusion in posttraumatic stress disorder patients without re-exposure to accident-related stimuli. Clinical Neurophysiology, 117(3), 637–642. doi:10.1016/j.clinph.2005.10.020.

    Article  PubMed  Google Scholar 

  • Cloutman, L. L., & Lambon Ralph, M. A. (2012). Connectivity-based structural and functional parcellation of the human cortex using diffusion imaging and tractography. Frontiers in Neuroanatomy, 6(34). doi:10.3389/fnana.2012.00034.

  • Daniels, J. K., Lamke, J. P., Gaebler, M., Walter, H., & Scheel, M. (2013). White matter integrity and its relationship to PTSD and childhood trauma--a systematic review and meta-analysis. Depression and Anxiety, 30(3), 207–216. doi:10.1002/da.22044.

    Article  PubMed  Google Scholar 

  • Davis, M., Walker, D. L., & Lee, Y. (1997). Roles of the amygdala and bed nucleus of the stria terminalis in fear and anxiety measured with the acoustic startle reflex. Possible relevance to PTSD. Ann N Y Acad Sci, 821, 305–331.

    Article  CAS  PubMed  Google Scholar 

  • Dickie, E. W., Brunet, A., Akerib, V., & Armony, J. L. (2012). Anterior cingulate cortical thickness is a stable predictor of recovery from post-traumatic stress disorder. Psychological Medicine, 1–9. doi:10.1017/S0033291712001328.

  • Engdahl, B., Leuthold, A. C., Tan, H. R., Lewis, S. M., Winskowski, A. M., Dikel, T. N., & Georgopoulos, A. P. (2010). Post-traumatic stress disorder: A right temporal lobe syndrome? Journal of Neural Engineering, 7(6), 066005. doi:10.1088/1741-2560/7/6/066005.

    Article  CAS  PubMed  Google Scholar 

  • Etkin, A., & Wager, T. D. (2007). Functional neuroimaging of anxiety: A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. The American Journal of Psychiatry, 164(10), 1476–1488. doi:10.1176/appi.ajp.2007.07030504.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fischl, B., & Dale, A. M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America, 97(20), 11050–11055. doi:10.1073/pnas.200033797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greicius, M. D., Krasnow, B., Reiss, A. L., & Menon, V. (2003). Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences of the United States of America, 100(1), 253–258. doi:10.1073/pnas.0135058100.

    Article  CAS  PubMed  Google Scholar 

  • He, Y., Chen, Z. J., & Evans, A. C. (2007). Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cerebral Cortex, 17(10), 2407–2419. doi:10.1093/cercor/bhl149.

    Article  PubMed  Google Scholar 

  • He, Y., Chen, Z., & Evans, A. (2008). Structural insights into aberrant topological patterns of large-scale cortical networks in Alzheimer's disease. The Journal of Neuroscience, 28(18), 4756–4766. doi:10.1523/JNEUROSCI.0141-08.2008.

    Article  CAS  PubMed  Google Scholar 

  • Jelicic, M., & Merckelbach, H. (2004). Traumatic stress, brain changes, and memory deficits: A critical note. The Journal of Nervous and Mental Disease, 192(8), 548–553.

    Article  PubMed  Google Scholar 

  • Jin, C., Qi, R., Yin, Y., Hu, X., Duan, L., Xu, Q., Zhang, Z., Zhong, Y., Feng, B., Xiang, H., Gong, Q., Liu, Y., Lu, G., & Li, L. (2014). Abnormalities in whole-brain functional connectivity observed in treatment-naive post-traumatic stress disorder patients following an earthquake. Psychological Medicine, 44(9), 1927–1936. doi:10.1017/S003329171300250X.

    Article  CAS  PubMed  Google Scholar 

  • Landre, L., Destrieux, C., Baudry, M., Barantin, L., Cottier, J. P., Martineau, J., Hommet, C., Isingrini, M., Belzung, C., Gaillard, P., Camus, V., & El Hage, W. (2010). Preserved subcortical volumes and cortical thickness in women with sexual abuse-related PTSD. Psychiatry Research, 183(3), 181–186. doi:10.1016/j.pscychresns.2010.01.015.

    Article  PubMed  Google Scholar 

  • Lanius, R. A., Williamson, P. C., Hopper, J., Densmore, M., Boksman, K., Gupta, M. A., Neufeld, R. W., Gati, J. S., & Menon, R. S. (2003). Recall of emotional states in posttraumatic stress disorder: An fMRI investigation. Biological Psychiatry, 53(3), 204–210.

    Article  PubMed  Google Scholar 

  • Liberzon, I., & Sripada, C. S. (2008). The functional neuroanatomy of PTSD: a critical review. Progress in Brain Research, 167, 151–169. doi:10.1016/S0079-6123(07)67011-3.

    Article  PubMed  Google Scholar 

  • Liu, Y., Li, Y. J., Luo, E. P., Lu, H. B., & Yin, H. (2012). Cortical thinning in patients with recent onset post-traumatic stress disorder after a single prolonged trauma exposure. PloS One, 7(6), e39025. doi:10.1371/journal.pone.0039025.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Long, Z., Duan, X., Xie, B., Du, H., Li, R., Xu, Q., Wei, L., Zhang, S. X., Wu, Y., Gao, Q., & Chen, H. (2013). Altered brain structural connectivity in post-traumatic stress disorder: A diffusion tensor imaging tractography study. Journal of Affective Disorders, 150(3), 798–806. doi:10.1016/j.jad.2013.03.004.

    Article  PubMed  Google Scholar 

  • Lyoo, I. K., Kim, J. E., Yoon, S. J., Hwang, J., Bae, S., & Kim, D. J. (2011). The neurobiological role of the dorsolateral prefrontal cortex in recovery from trauma. Longitudinal brain imaging study among survivors of the south Korean subway disaster. Archives of General Psychiatry, 68(7), 701–713. doi:10.1001/archgenpsychiatry.2011.70.

    Article  PubMed  Google Scholar 

  • Marrelec, G., Krainik, A., Duffau, H., Pelegrini-Issac, M., Lehericy, S., Doyon, J., & Benali, H. (2006). Partial correlation for functional brain interactivity investigation in functional MRI. NeuroImage, 32(1), 228–237. doi:10.1016/j.neuroimage.2005.12.057.

    Article  PubMed  Google Scholar 

  • Mcalonan, G. M., Cheung, V., Cheung, C., Suckling, J., Lam, G. Y., Tai, K. S., Yip, L., Murphy, D. G., & Chua, S. E. (2005). Mapping the brain in autism. A voxel-based MRI study of volumetric differences and intercorrelations in autism. Brain, 128(Pt 2), 268–276. doi:10.1093/brain/awh332.

    PubMed  Google Scholar 

  • Mitelman, S. A., Buchsbaum, M. S., Brickman, A. M., & Shihabuddin, L. (2005). Cortical intercorrelations of frontal area volumes in schizophrenia. NeuroImage, 27(4), 753–770. doi:10.1016/j.neuroimage.2005.05.024.

    Article  PubMed  Google Scholar 

  • Moher, D., Liberati, A., Tetzlaff, J., & Altman, D.G. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339 b2535. doi: 10.1136/bmj.b2535

  • Noppeney, U., Friston, K. J., Ashburner, J., Frackowiak, R., & Price, C. J. (2005). Early visual deprivation induces structural plasticity in gray and white matter. Current Biology, 15(13), R488–R490. doi:10.1016/j.cub.2005.06.053.

    Article  CAS  PubMed  Google Scholar 

  • Qi, S., Mu, Y., Liu, K., Zhang, J., Huan, Y., Tan, Q., Shi, M., Wang, Q., Chen, Y., Wang, H., Zhang, N., Zhang, X., Xiong, L., & Yin, H. (2013). Cortical inhibition deficits in recent onset PTSD after a single prolonged trauma exposure. Neuroimage Clin, 3, 226–233. doi:10.1016/j.nicl.2013.08.013.

    Article  PubMed  PubMed Central  Google Scholar 

  • Qin, L. D., Wang, Z., Sun, Y. W., Wan, J. Q., Su, S. S., Zhou, Y., & Xu, J. R. (2012). A preliminary study of alterations in default network connectivity in post-traumatic stress disorder patients following recent trauma. Brain Research, 1484, 50–56. doi:10.1016/j.brainres.2012.09.029.

    Article  CAS  PubMed  Google Scholar 

  • Rauch, S. L., Shin, L. M., Segal, E., Pitman, R. K., Carson, M. A., Mcmullin, K., Whalen, P. J., & Makris, N. (2003). Selectively reduced regional cortical volumes in post-traumatic stress disorder. Neuroreport, 14(7), 913–916. doi:10.1097/01.wnr.0000071767.24455.10.

    Article  PubMed  Google Scholar 

  • Rogers, M. A., Yamasue, H., Abe, O., Yamada, H., Ohtani, T., Iwanami, A., Aoki, S., Kato, N., & Kasai, K. (2009). Smaller amygdala volume and reduced anterior cingulate gray matter density associated with history of post-traumatic stress disorder. Psychiatry Research, 174(3), 210–216. doi:10.1016/j.pscychresns.2009.06.001.

    Article  PubMed  Google Scholar 

  • Rossi, S., Cappa, S. F., Ulivelli, M., De Capua, A., Bartalini, S., & Rossini, P. M. (2006). rTMS for PTSD: Induced merciful oblivion or elimination of abnormal hypermnesia? Behavioural Neurology, 17(3–4), 195–199.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rougemont-Bucking, A., Linnman, C., Zeffiro, T.A., Zeidan, M.A., Lebron-Milad, K., Rodriguez-Romaguera, J., Rauch, S.L., Pitman, R.K., & Milad, M.R. (2010). Altered processing of contextual information during fear extinction in PTSD: An fMRI Study. CNS Neurosci Ther. doi: 10.1111/j.1755-5949.2010.00152.x.

  • Sanabria-Diaz, G., Melie-Garcia, L., Iturria-Medina, Y., Aleman-Gomez, Y., Hernandez-Gonzalez, G., Valdes-Urrutia, L., Galan, L., & Valdes-Sosa, P. (2010). Surface area and cortical thickness descriptors reveal different attributes of the structural human brain networks. NeuroImage, 50(4), 1497–1510. doi:10.1016/j.neuroimage.2010.01.028.

    Article  PubMed  Google Scholar 

  • Sanz-Arigita, E. J., Schoonheim, M. M., Damoiseaux, J. S., Rombouts, S. A., Maris, E., Barkhof, F., Scheltens, P., & Stam, C. J. (2010). Loss of 'small-world' networks in Alzheimer's disease: Graph analysis of FMRI resting-state functional connectivity. PloS One, 5(11), e13788. doi:10.1371/journal.pone.0013788.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schuff, N., Zhang, Y., Zhan, W., Lenoci, M., Ching, C., Boreta, L., Mueller, S. G., Wang, Z., Marmar, C. R., Weiner, M. W., & Neylan, T. C. (2011). Patterns of altered cortical perfusion and diminished subcortical integrity in posttraumatic stress disorder: an MRI study. NeuroImage, 54(1), S62–S68. doi:10.1016/j.neuroimage.2010.05.024.

    Article  PubMed  Google Scholar 

  • Stam, C. J. (2004). Functional connectivity patterns of human magnetoencephalographic recordings: A 'small-world' network? Neuroscience Letters, 355(1–2), 25–28.

    Article  CAS  PubMed  Google Scholar 

  • Stam, R. (2007). PTSD and stress sensitisation: A tale of brain and body part 2: Animal models. Neuroscience and Biobehavioral Reviews, 31(4), 558–584. doi:10.1016/j.neubiorev.2007.01.001.

    Article  PubMed  Google Scholar 

  • Van Den Heuvel, M. P., & Sporns, O. (2011). Rich-club organization of the human connectome. The Journal of Neuroscience, 31(44), 15775–15786. doi:10.1523/JNEUROSCI.3539-11.2011.

    Article  CAS  PubMed  Google Scholar 

  • Vincent, J. L., Patel, G. H., Fox, M. D., Snyder, A. Z., Baker, J. T., Van Essen, D. C., Zempel, J. M., Snyder, L. H., Corbetta, M., & Raichle, M. E. (2007). Intrinsic functional architecture in the anaesthetized monkey brain. Nature, 447(7140), 83–86. doi:10.1038/nature05758.

    Article  CAS  PubMed  Google Scholar 

  • Watts, D. J., & Strogatz, S. H. (1998). Collective dynamics of 'small-world' networks. Nature, 393(6684), 440–442. doi:10.1038/30918.

    Article  CAS  PubMed  Google Scholar 

  • Williams, L. M., Kemp, A. H., Felmingham, K., Barton, M., Olivieri, G., Peduto, A., Gordon, E., & Bryant, R. A. (2006). Trauma modulates amygdala and medial prefrontal responses to consciously attended fear. NeuroImage, 29(2), 347–357. doi:10.1016/j.neuroimage.2005.03.047.

    Article  PubMed  Google Scholar 

  • Woodward, S. H., Kaloupek, D. G., Grande, L. J., Stegman, W. K., Kutter, C. J., Leskin, L., Prestel, R., Schaer, M., Reiss, A. L., & Eliez, S. (2009a). Hippocampal volume and declarative memory function in combat-related PTSD. Journal of the International Neuropsychological Society, 15(6), 830–839. doi:10.1017/S1355617709990476.

    Article  PubMed  Google Scholar 

  • Woodward, S. H., Schaer, M., Kaloupek, D. G., Cediel, L., & Eliez, S. (2009b). Smaller global and regional cortical volume in combat-related posttraumatic stress disorder. Archives of General Psychiatry, 66(12), 1373–1382. doi:10.1001/archgenpsychiatry.2009.160.

    Article  PubMed  Google Scholar 

  • Yamasue, H., Kasai, K., Iwanami, A., Ohtani, T., Yamada, H., Abe, O., Kuroki, N., Fukuda, R., Tochigi, M., Furukawa, S., Sadamatsu, M., Sasaki, T., Aoki, S., Ohtomo, K., Asukai, N., & Kato, N. (2003). Voxel-based analysis of MRI reveals anterior cingulate gray-matter volume reduction in posttraumatic stress disorder due to terrorism. Proceedings of the National Academy of Sciences of the United States of America, 100(15), 9039–9043. doi:10.1073/pnas.1530467100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan, C., & He, Y. (2011). Driving and driven architectures of directed small-world human brain functional networks. PloS One, 6(8), e23460. doi:10.1371/journal.pone.0023460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, J., Tan, Q., Yin, H., Zhang, X., Huan, Y., Tang, L., Wang, H., Xu, J., & Li, L. (2011a). Decreased gray matter volume in the left hippocampus and bilateral calcarine cortex in coal mine flood disaster survivors with recent onset PTSD. Psychiatry Research, 192(2), 84–90. doi:10.1016/j.pscychresns.2010.09.001.

    Article  PubMed  Google Scholar 

  • Zhang, J., Wang, J., Wu, Q., Kuang, W., Huang, X., He, Y., & Gong, Q. (2011b). Disrupted brain connectivity networks in drug-naive, first-episode major depressive disorder. Biological Psychiatry, 70(4), 334–342. doi:10.1016/j.biopsych.2011.05.018.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Radiology, Xijing Hospital, Fourth Military Medical University, No.127 West Changle Road, Xi’an, Shaanxi Province, 710032, China

    Shun Qi, Long-Biao Cui, Fan Guo, Kang Liu, Yi-Bin Xi & Hong Yin

  2. Department of Radiology, The First Affiliated Hospital of Xi’an Jiaotong University, No. 277 West Yanta Road, Xi’an, Shaanxi, 710061, China

    Shun Qi & Jian Yang

  3. Department of Radiotherapy, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, 710032, China

    Yun-Feng Mu & Mei Shi

  4. Department of Respiratory Medicine, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, 710032, China

    Jian Zhang

  5. Department of Psychiatry, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, 710032, China

    Qing-Rong Tan

  6. Department of Psychiatry, University of Massachusetts Medical School, 55 Lake Avenue North, Worcester, MA, 01655, USA

    Nan-Yin Zhang

  7. Department of Radiology and Program in Bioengineering, UC San Francisco, Byers Hall, Room 102D, 1700 4th Street, San Francisco, CA, 94158-2330, USA

    Xiao-Liang Zhang

  8. State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, 100875, China

    Yong He

Authors
  1. Shun Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yun-Feng Mu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Long-Biao Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jian Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fan Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qing-Rong Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mei Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yi-Bin Xi
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Nan-Yin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Xiao-Liang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yong He
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Jian Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Hong Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jian Yang or Hong Yin.

Ethics declarations

Funding

This study was funded by the National Natural Science Foundation of China (81171278) and National Key Technology R&D Program in the 11th Five-year Plan of China (2007BA117B02).

Conflict of interest

Shun Qi declares that he has no conflict of interest. Yun-Feng Mu declares that she has no conflict of interest. Long-Biao Cui declares that he has no conflict of interest. Jian Zhang declares that she has no conflict of interest. Fan Guo declares that she has no conflict of interest. Qing-Rong Tan declares that she has no conflict of interest. Mei Shi declares that she has no conflict of interest. Kang Liu declares that he has no conflict of interest. Yi-Bin Xi declares that he has no conflict of interest. Nan-Yin Zhang declares that he has no conflict of interest. Xiao-Liang Zhang declares that he has no conflict of interest. Yong He declares that he has no conflict of interest. Jian Yang declares that he has no conflict of interest. Hong Yin declares that he has no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Shun Qi, Yun-Feng Mu, Long-Biao Cui and Jian Zhang contributed equally to this work.

Electronic supplementary material

ESM 1

(DOC 474 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qi, S., Mu, YF., Cui, LB. et al. Anomalous gray matter structural networks in recent onset post-traumatic stress disorder. Brain Imaging and Behavior 12, 390–401 (2018). https://doi.org/10.1007/s11682-017-9693-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-017-9693-z

Keywords

Search

Navigation