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

  • Shun Qi
  • Yun-Feng Mu
  • Long-Biao Cui
  • Jian Zhang
  • Fan Guo
  • Qing-Rong Tan
  • Mei Shi
  • Kang Liu
  • Yi-Bin Xi
  • Nan-Yin Zhang
  • Xiao-Liang Zhang
  • Yong He
  • Jian Yang
  • Hong Yin
Original Research

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.

Keywords

Post-traumatic stress disorder Gray matter Structural networks Small world networks Cortex thickness 

Supplementary material

11682_2017_9693_MOESM1_ESM.doc (474 kb)
ESM 1(DOC 474 kb)

References

  1. 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.CrossRefPubMedGoogle Scholar
  2. 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.CrossRefPubMedGoogle Scholar
  3. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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.CrossRefPubMedGoogle Scholar
  5. 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.
  6. 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.CrossRefPubMedGoogle Scholar
  7. 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.CrossRefPubMedGoogle Scholar
  8. 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.
  9. 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.CrossRefPubMedGoogle Scholar
  10. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedGoogle Scholar
  14. 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.CrossRefPubMedGoogle Scholar
  15. 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.CrossRefPubMedGoogle Scholar
  16. 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.CrossRefPubMedGoogle Scholar
  17. 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.CrossRefPubMedGoogle Scholar
  18. 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.CrossRefPubMedGoogle Scholar
  19. 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.CrossRefPubMedGoogle Scholar
  20. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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.CrossRefPubMedGoogle Scholar
  22. 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.CrossRefPubMedGoogle Scholar
  23. 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.CrossRefPubMedGoogle Scholar
  24. 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.PubMedGoogle Scholar
  25. 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.CrossRefPubMedGoogle Scholar
  26. 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
  27. 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.CrossRefPubMedGoogle Scholar
  28. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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.CrossRefPubMedGoogle Scholar
  30. 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.CrossRefPubMedGoogle Scholar
  31. 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.CrossRefPubMedGoogle Scholar
  32. 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.CrossRefPubMedGoogle Scholar
  33. 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.
  34. 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.CrossRefPubMedGoogle Scholar
  35. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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.CrossRefPubMedGoogle Scholar
  37. Stam, C. J. (2004). Functional connectivity patterns of human magnetoencephalographic recordings: A 'small-world' network? Neuroscience Letters, 355(1–2), 25–28.CrossRefPubMedGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. 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.CrossRefPubMedGoogle Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. Watts, D. J., & Strogatz, S. H. (1998). Collective dynamics of 'small-world' networks. Nature, 393(6684), 440–442. doi:10.1038/30918.CrossRefPubMedGoogle Scholar
  42. 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.CrossRefPubMedGoogle Scholar
  43. 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.CrossRefPubMedGoogle Scholar
  44. 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.CrossRefPubMedGoogle Scholar
  45. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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.CrossRefPubMedGoogle Scholar
  48. 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.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Shun Qi
    • 1
    • 2
  • Yun-Feng Mu
    • 3
  • Long-Biao Cui
    • 1
  • Jian Zhang
    • 4
  • Fan Guo
    • 1
  • Qing-Rong Tan
    • 5
  • Mei Shi
    • 3
  • Kang Liu
    • 1
  • Yi-Bin Xi
    • 1
  • Nan-Yin Zhang
    • 6
  • Xiao-Liang Zhang
    • 7
  • Yong He
    • 8
  • Jian Yang
    • 2
  • Hong Yin
    • 1
  1. 1.Department of RadiologyXijing Hospital, Fourth Military Medical UniversityXi’anChina
  2. 2.Department of RadiologyThe First Affiliated Hospital of Xi’an Jiaotong UniversityXi’anChina
  3. 3.Department of RadiotherapyXijing Hospital, Fourth Military Medical UniversityXi’anChina
  4. 4.Department of Respiratory MedicineXijing Hospital, Fourth Military Medical UniversityXi’anChina
  5. 5.Department of PsychiatryXijing Hospital, Fourth Military Medical UniversityXi’anChina
  6. 6.Department of PsychiatryUniversity of Massachusetts Medical SchoolWorcesterUSA
  7. 7.Department of Radiology and Program in BioengineeringUC San FranciscoSan FranciscoUSA
  8. 8.State Key Laboratory of Cognitive Neuroscience and LearningBeijing Normal UniversityBeijingChina

Personalised recommendations