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Abnormalities in whole-brain functional connectivity observed in treatment-naive post-traumatic stress disorder patients following an earthquake

Published online by Cambridge University Press:  29 October 2013

C. Jin ,
R. Qi ,
Y. Yin ,
X. Hu ,
L. Duan ,
Q. Xu ,
Z. Zhang ,
Y. Zhong ,
B. Feng  and
H. Xiang
...Show all authors
C. Jin
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Hunan, People's Republic of China
R. Qi
Affiliation:
Department of Medical Imaging, Jinling Hospital, Clinical School of Medical College, Nanjing University, Nanjing. People's Republic of China
Y. Yin
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Hunan, People's Republic of China The Seventh People's Hospital of Hangzhou, Hangzhou, Zhejiang, People's Republic of China
X. Hu
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Hunan, People's Republic of China
L. Duan
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Hunan, People's Republic of China
Q. Xu
Affiliation:
Department of Medical Imaging, Jinling Hospital, Clinical School of Medical College, Nanjing University, Nanjing. People's Republic of China
Z. Zhang
Affiliation:
Department of Medical Imaging, Jinling Hospital, Clinical School of Medical College, Nanjing University, Nanjing. People's Republic of China
Y. Zhong
Affiliation:
Department of Medical Imaging, Jinling Hospital, Clinical School of Medical College, Nanjing University, Nanjing. People's Republic of China
B. Feng
Affiliation:
Mianzhu Psychiatric Hospital, Erhuan Road and Mianzun Road, Deyang, Sichuan, People's Republic of China
H. Xiang
Affiliation:
Mental Health Center of Sichuan Province, Mianyang, Sichuan, People's Republic of China
Q. Gong
Affiliation:
Huaxi MR Research Center, Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan, People's Republic of China
Y. Liu
Affiliation:
Department of Psychiatry, University of Florida, Gainesville, FL, USA
G. Lu*
Affiliation:
Department of Medical Imaging, Jinling Hospital, Clinical School of Medical College, Nanjing University, Nanjing. People's Republic of China
L. Li*
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Hunan, People's Republic of China
*
(Email: cjr.luguangming@vip.163.com)
*Address for correspondence: L. Li, M.D., Mental Health Institute, The Second Xiangya Hospital of Central South University, 139# Renmin Zhong Road, Changsha 410011, Hunan, People's Republic of China. (Email: llj2920@163.com)
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Abstract

Background

Convergent studies have highlighted the dysfunction of the amygdala, prefrontal cortex and hippocampus in post-traumatic stress disorder (PTSD). However, only a few studies have investigated the functional connectivity between brain regions in PTSD patients during the resting state, which may improve our understanding of the neuropathophysiology of PTSD. The aim of this study was to investigate patterns of whole-brain functional connectivity in treatment-naive PTSD patients without co-morbid conditions who experienced the 8.0-magnitude earthquake in the Sichuan province of China.

Method

A total of 72 PTSD patients and 86 trauma-exposed non-PTSD controls participated in the resting-state functional magnetic resonance imaging study. All these subjects were recruited from the disaster zone of the 2008 Sichuan earthquake. Functional connectivities between 90 paired brain regions in PTSD patients were compared with those in trauma-exposed non-PTSD controls. Furthermore, Pearson correlation analysis was performed between significantly abnormal connectivities in PTSD patients and their clinician-administered PTSD scale (CAPS) scores.

Results

Compared with non-PTSD controls, PTSD patients showed weaker positive connectivities between the middle prefrontal cortex (mPFC) and the amygdala, hippocampus, parahippocampal gyrus and rectus, as well as between the inferior orbitofrontal cortex and the hippocampus. In addition, PTSD patients showed stronger negative connectivity between the posterior cingulate cortex (PCC) and the insula. The CAPS scores in PTSD patients correlated negatively with the connectivity between the amygdala and the mPFC.

Conclusions

PTSD patients showed abnormalities in whole-brain functional connectivity, primarily affecting the connectivities between the mPFC and limbic system, and connectivity between the PCC and insula.

Keywords

Functional connectivitypost-traumatic stress disorderresting-state functional magnetic resonance imaging
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 9 , July 2014 , pp. 1927 - 1936
Copyright
Copyright © Cambridge University Press 2013 

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References

Blake, DD, Weathers, FW, Nagy, LM, Kaloupek, DG, Gusman, FD, Charney, DS, Keane, TM (1995). The development of a clinician-administered PTSD scale. Journal of Traumatic Stress 8, 75–90.Google Scholar
Blanchard, EB, Jones-Alexander, J, Buckley, TC, Forneris, CA (1996). Psychometric properties of the PTSD Checklist (PCL). Behaviour Research and Therapy 34, 669–673.Google Scholar
Bluhm, RL, Williamson, PC, Osuch, EA, Frewen, PA, Steven, TK, Boksman, K, Neufeld, RW, Theberge, J, Lanius, RA (2009). Alterations in default network connectivity in posttraumatic stress disorder related to early-life trauma. Journal of Psychiatry and Neuroscience 34, 187–194.Google ScholarPubMed
Brady, K, Pearlstein, T, Asnis, GM, Baker, D, Rothbaum, B, Sikes, CR, Farfel, GM (2000). Efficacy and safety of sertraline treatment of posttraumatic stress disorder: a randomized controlled trial. Journal of the American Medical Association 283, 1837–1844.Google Scholar
Braun, K (2011). The prefrontal–limbic system: development, neuroanatomy, function, and implications for socioemotional development. Clinics in Perinatology 38, 685–702.CrossRefGoogle ScholarPubMed
Bremner, JD (2007). Functional neuroimaging in post-traumatic stress disorder. Expert Review of Neurotherapeutics 7, 393–405.Google Scholar
Chung, YA, Kim, SH, Chung, SK, Chae, JH, Yang, DW, Sohn, HS, Jeong, J (2006). Alterations in cerebral perfusion in posttraumatic stress disorder patients without re-exposure to accident-related stimuli. Clinical Neurophysiology 117, 637–642.CrossRefGoogle ScholarPubMed
Damoiseaux, JS, Rombouts, SA, Barkhof, F, Scheltens, P, Stam, CJ, Smith, SM, Beckmann, CF (2006). Consistent resting-state networks across healthy subjects. Proceedings of the National Academy of Sciences USA 103, 13848–13853.Google Scholar
Ding, J, Chen, H, Qiu, C, Liao, W, Warwick, JM, Duan, X, Zhang, W, Gong, Q (2011). Disrupted functional connectivity in social anxiety disorder: a resting-state fMRI study. Magnetic Resonance Imaging 29, 701–711.Google Scholar
Etkin, A, Wager, TD (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry 164, 1476–1488.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JB (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition. Biometrics Research, New York State Psychiatric Institute: New York.Google Scholar
Fornito, A, Yoon, J, Zalesky, A, Bullmore, ET, Carter, CS (2011). General and specific functional connectivity disturbances in first-episode schizophrenia during cognitive control performance. Biological Psychiatry 70, 64–72.Google Scholar
Fox, MD, Greicius, M (2010). Clinical applications of resting state functional connectivity. Frontiers in Systems Neuroscience 4, 19.Google Scholar
Fox, MD, Raichle, ME (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews Neuroscience 8, 700–711.Google Scholar
Fox, MD, Snyder, AZ, Vincent, JL, Corbetta, M, Van Essen, DC, Raichle, ME (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences USA 102, 9673–9678.CrossRefGoogle ScholarPubMed
Garrett, AS, Carrion, V, Kletter, H, Karchemskiy, A, Weems, CF, Reiss, A (2012). Brain activation to facial expressions in youth with PTSD symptoms. Depression and Anxiety 29, 449–459.Google Scholar
Ghashghaei, HT, Hilgetag, CC, Barbas, H (2007). Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 34, 905–923.Google Scholar
Greicius, MD, Srivastava, G, Reiss, AL, Menon, V (2004). Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proceedings of the National Academy of Sciences USA 101, 4637–4642.Google Scholar
Hughes, KC, Shin, LM (2011). Functional neuroimaging studies of post-traumatic stress disorder. Expert Review of Neurotherapeutics 11, 275–285.Google Scholar
Jao, T, Vertes, PE, Alexander-Bloch, AF, Tang, IN, Yu, YC, Chen, JH, Bullmore, ET (2013). Volitional eyes opening perturbs brain dynamics and functional connectivity regardless of light input. Neuroimage 69, 21–34.Google Scholar
Lanius, RA, Bluhm, RL, Coupland, NJ, Hegadoren, KM, Rowe, B, Theberge, J, Neufeld, RW, Williamson, PC, Brimson, M (2010). Default mode network connectivity as a predictor of post-traumatic stress disorder symptom severity in acutely traumatized subjects. Acta Psychiatrica Scandinavica 121, 33–40.Google Scholar
Lee, MH, Smyser, CD, Shimony, JS (2012). Resting-state fMRI: a review of methods and clinical applications. American Journal of Neuroradiology. Published online 30 August 2012 . doi:10.3174/anjr.A3263.Google Scholar
Levin, P, Lazrove, S, van der Kolk, B (1999). What psychological testing and neuroimaging tell us about the treatment of posttraumatic stress disorder by eye movement desensitization and reprocessing. Journal of Anxiety Disorders 13, 159–172.Google Scholar
Liao, W, Chen, H, Feng, Y, Mantini, D, Gentili, C, Pan, Z, Ding, J, Duan, X, Qiu, C, Lui, S, Gong, Q, Zhang, W (2010). Selective aberrant functional connectivity of resting state networks in social anxiety disorder. Neuroimage 52, 1549–1558.Google Scholar
Liberzon, I, Phan, KL (2003). Brain-imaging studies of posttraumatic stress disorder. CNS Spectrums 8, 641–650.Google Scholar
Lowe, MJ, Dzemidzic, M, Lurito, JT, Mathews, VP, Phillips, MD (2000). Correlations in low-frequency BOLD fluctuations reflect cortico-cortical connections. Neuroimage 12, 582–587.Google Scholar
Maldjian, JA, Laurienti, PJ, Kraft, RA, Burdette, JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19, 1233–1239.Google Scholar
Mantini, D, Perrucci, MG, Del Gratta, C, Romani, GL, Corbetta, M (2007). Electrophysiological signatures of resting state networks in the human brain. Proceedings of the National Academy of Sciences USA 104, 13170–13175.Google Scholar
Pessoa, L (2008). On the relationship between emotion and cognition. Nature Reviews Neuroscience 9, 148–158.Google Scholar
Rabinak, CA, Angstadt, M, Welsh, RC, Kenndy, AE, Lyubkin, M, Martis, B, Phan, KL (2011). Altered amygdala resting-state functional connectivity in post-traumatic stress disorder. Frontiers in Psychiatry 2, 62.Google Scholar
Raichle, ME, MacLeod, AM, Snyder, AZ, Powers, WJ, Gusnard, DA, Shulman, GL (2001). A default mode of brain function. Proceedings of the National Academy of Sciences USA 98, 676–682.CrossRefGoogle ScholarPubMed
Shin, LM, Orr, SP, Carson, MA, Rauch, SL, Macklin, ML, Lasko, NB, Peters, PM, Metzger, LJ, Dougherty, DD, Cannistraro, PA, Alpert, NM, Fischman, AJ, Pitman, RK (2004). Regional cerebral blood flow in the amygdala and medial prefrontal cortex during traumatic imagery in male and female Vietnam veterans with PTSD. Archives of General Psychiatry 61, 168–176.CrossRefGoogle ScholarPubMed
Shin, LM, Wright, CI, Cannistraro, PA, Wedig, MM, McMullin, K, Martis, B, Macklin, ML, Lasko, NB, Cavanagh, SR, Krangel, TS, Orr, SP, Pitman, RK, Whalen, PJ, Rauch, SL (2005). A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Archives of General Psychiatry 62, 273–281.Google Scholar
Sripada, RK, King, AP, Garfinkel, SN, Wang, X, Sripada, CS, Welsh, RC, Liberzon, I (2012 a). Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder. Journal of Psychiatry and Neuroscience 37, 241–249.Google Scholar
Sripada, RK, King, AP, Welsh, RC, Garfinkel, SN, Wang, X, Sripada, CS, Liberzon, I (2012 b). Neural dysregulation in posttraumatic stress disorder: evidence for disrupted equilibrium between salience and default mode brain networks. Psychosomatic Medicine 74, 904–911.Google Scholar
Tamminga, CA, Buchsbaum, MS (2004). Frontal cortex function. American Journal of Psychiatry 161, 2178.Google ScholarPubMed
Williams, LM, Kemp, AH, Felmingham, K, Barton, M, Olivieri, G, Peduto, A, Gordon, E, Bryant, RA (2006). Trauma modulates amygdala and medial prefrontal responses to consciously attended fear. Neuroimage 29, 347–357.Google Scholar
Woodward, ND, Karbasforoushan, H, Heckers, S (2012). Thalamocortical dysconnectivity in schizophrenia. American Journal of Psychiatry 169, 1092–1099.Google Scholar
Yin, Y, Jin, C, Hu, X, Duan, L, Li, Z, Song, M, Chen, H, Feng, B, Jiang, T, Jin, H, Wong, C, Gong, Q, Li, L (2011 a). Altered resting-state functional connectivity of thalamus in earthquake-induced posttraumatic stress disorder: a functional magnetic resonance imaging study. Brain Research 1411, 98–107.Google Scholar
Yin, Y, Li, L, Jin, C, Hu, X, Duan, L, Eyler, LT, Gong, Q, Song, M, Jiang, T, Liao, M, Zhang, Y, Li, W (2011 b). Abnormal baseline brain activity in posttraumatic stress disorder: a resting-state functional magnetic resonance imaging study. Neuroscience Letters 498, 185–189.Google Scholar
Zhang, LJ, Zheng, G, Zhang, L, Zhong, J, Wu, S, Qi, R, Li, Q, Wang, L, Lu, G (2012). Altered brain functional connectivity in patients with cirrhosis and minimal hepatic encephalopathy: a functional MR imaging study. Radiology 265, 528–536.Google Scholar
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