Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-26T04:01:08.858Z Has data issue: false hasContentIssue false
  • English
  • Français

Increased white matter integrity of posterior cingulate gyrus in the evolution of post-traumatic stress disorder

Published online by Cambridge University Press:  24 June 2014

Li Zhang ,
Weihui Li ,
Ni Shu ,
Huirong Zheng ,
Zhijun Zhang ,
Yan Zhang ,
Zhong He ,
Cailan Hou ,
Zexuan Li  and
Jun Liu
...Show all authors
Li Zhang
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Changsha, China
Weihui Li
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Changsha, China
Ni Shu
Affiliation:
National Laboratory of Pattern Recognition, Automation Institute, Chinese Academy of Sciences, Beijing, China
Huirong Zheng
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Changsha, China Guangdong Mental Health Institute, Guangdong General Hospital, Guangdong Academy of Medical Sciences, Guangzhou, China
Zhijun Zhang
Affiliation:
Department of Neurology, Affiliated Zhongda Hospital and Institute of the Neuropsychiatry of Southeast University, Nanjing, China
Yan Zhang
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Changsha, China
Zhong He
Affiliation:
Department of Radiology, The Second Xiangya Hospital of Central South University, Changsha, China
Cailan Hou
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Changsha, China Guangdong Mental Health Institute, Guangdong General Hospital, Guangdong Academy of Medical Sciences, Guangzhou, China
Zexuan Li
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Changsha, China
Jun Liu
Affiliation:
Department of Radiology, The Second Xiangya Hospital of Central South University, Changsha, China
Lifeng Wang
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Changsha, China
Lian Duan
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Changsha, China
Tianzi Jiang
Affiliation:
National Laboratory of Pattern Recognition, Automation Institute, Chinese Academy of Sciences, Beijing, China
Lingjiang Li
Affiliation:
Mental Health Institute, The Second Xiangya Hospital of Central South University, Changsha, China Chinese University of Hong Kong, Hong Kong, China
Get access Rights & Permissions [Opens in a new window]

Extract

Objective: Functional imaging studies of post-traumatic stress disorder (PTSD) have shown an increased activation of posterior cingulate gyrus (PCG) of the brain. The aim of this study was to explore white matter integrity of PCG in PTSD subjects.

Methods: White matter integrity, as determined from fractional anisotropy (FA) value using diffusion tensor imaging, was assessed for PCG in subjects with and without PTSD from a severe mine accident. All subjects were also measured by the PTSD Checklist Civilian Version (PCL-C), the State-Trait Anxiety Inventory (STAI), the logical memory subtest and the visual reproduction subtest of the Wechsler Memory Scale-Revised in China. Sixteen PTSD subjects (8 subjects in each group) in the longitudinal study and 13 PTSD subjects as well as 14 non-PTSD controls in the cross-sectional case–control study were respectively recruited.

Results: In the longitudinal study, subjects with PTSD showed increased FA values in left PCG during the follow-up scan. In the cross-sectional study, FA values in bilateral PCG in PTSD subjects were higher than controls. Within the PTSD group (n = 13), FA values in the left PCG correlated positively with logical memory and negatively with PCL-C intrusion and STAI-trait (STAI-t) subscores. FA values in right PCG correlated negatively with STAI-t and STAI-state subscores.

Conclusion: These findings suggest that alterations of white matter integrity in PCG link to mnemonic and affective processing in PTSD over the long-term follow-up period.

Keywords

anxietydiffusion tensor imagingmemorypost-traumatic stress disorder
Type
Research Article
Information
Acta Neuropsychiatrica , Volume 24 , Issue 1 , February 2012 , pp. 34 - 42
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Lanius, RA, Frewen, PA, Girotti, M, Neufeld, RW, Stevens, TK, Densmore, M.Neural correlates of trauma script-imagery in posttraumatic stress disorder with and without comorbid major depression: a functional MRI investigation. Psychiatry Res 2007;155:45–56.CrossRefGoogle ScholarPubMed
2.Lanius, RA, Bluhm, R, Lanius, U, Pain, C.A review of neuroimaging studies in PTSD: heterogeneity of response to symptom provocation. J Psychiatr Res 2006;40:709–729.CrossRefGoogle ScholarPubMed
3.Fonzo, GA, Simmons, AN, Thorp, SR, Norman, SB, Paulus, MP, Stein, MB.Exaggerated and disconnected insular-amygdalar blood oxygenation level-dependent response to threat-related emotional faces in women with intimate-partner violence posttraumatic stress disorder. Biol Psychiatry 2010;68:433–441.CrossRefGoogle ScholarPubMed
4.Schuff, N, Zhang, Y, Zhan, W et al. Patterns of altered cortical perfusion and diminished subcortical integrity in posttraumatic stress disorder: an MRI study. Neuroimage 2011;54:S62–68.CrossRefGoogle ScholarPubMed
5.Landre, L, Destrieux, C, Baudry, M et al. Preserved subcortical volumes and cortical thickness in women with sexual abuse-related PTSD. Psychiatry Res 2010;183:181–186.CrossRefGoogle ScholarPubMed
6.Bremner, JD, Narayan, M, Staib, LH, Southwick, SM, McGlashan, T, Charney, DS.Neural correlates of memories of childhood sexual abuse in women with and without posttraumatic stress disorder. Am J Psychiatry 1999;156:1787–1795.CrossRefGoogle ScholarPubMed
7.Hou, C, Liu, J, Wang, K et al. Brain responses to symptom provocation and trauma-related short-term memory recall in coal mining accident survivors with acute severe PTSD. Brain Res 2007;1144:165–174.CrossRefGoogle ScholarPubMed
8.Armony, JL, Corbo, V, Clement, MH, Brunet, A.Amygdala response in patients with acute PTSD to masked and unmasked emotional facial expressions. Am J Psychiatry 2005;162:1961–1963.CrossRefGoogle ScholarPubMed
9.Bremner, JD.Effects of traumatic stress on brain structure and function: relevance to early responses to trauma. J Trauma Dissociation 2005;6:51–68.CrossRefGoogle ScholarPubMed
10.Bremner, JD.Neuroimaging in posttraumatic stress disorder and other stress-related disorders. Neuroimaging Clin N Am 2007;17:523–538.CrossRefGoogle ScholarPubMed
11.Brunetti, M, Sepede, G, Mingoia, G et al. Elevated response of human amygdala to neutral stimuli in mild post traumatic stress disorder: neural correlates of generalized emotional response. Neuroscience 2010;168:670–679.CrossRefGoogle ScholarPubMed
12.van den Heuvel, M, Mandl, R, Luigjes, J, Hulshoff Pol, H.Microstructural organization of the cingulum tract and the level of default mode functional connectivity. J Neurosci 2008;28:10844–10851.CrossRefGoogle ScholarPubMed
13.Bremner, JD.Functional neuroimaging in post-traumatic stress disorder. Expert Rev Neurother 2007;7:393–405.CrossRefGoogle ScholarPubMed
14.Meunier, M, Jaffard, R, Destrade, C.Differential involvement of anterior and posterior cingulate cortices in spatial discriminative learning in a T-maze in mice. Behav Brain Res 1991;44:133–143.CrossRefGoogle Scholar
15.Vogt, BA, Finch, DM, Olson, CR.Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb Cortex 1992;2:435–443.Google ScholarPubMed
16.Maddock, RJ, Buonocore, MH.Activation of left posterior cingulate gyrus by the auditory presentation of threat-related words: an fMRI study. Psychiatry Res 1997;75:1–14.CrossRefGoogle ScholarPubMed
17.Sutherland, RJ, Whishaw, IQ, Kolb, B.Contributions of cingulate cortex to two forms of spatial learning and memory. J Neurosci 1988;8:1863–1872.CrossRefGoogle ScholarPubMed
18.Whishaw, IQ, Maaswinkel, H, Gonzalez, CL, Kolb, B.Deficits in allothetic and idiothetic spatial behavior in rats with posterior cingulate cortex lesions. Behav Brain Res 2001;118:67–76.CrossRefGoogle ScholarPubMed
19.Katayama, K, Takahashi, N, Ogawara, K, Hattori, T.Pure topographical disorientation due to right posterior cingulate lesion. Cortex 1999;35:279–282.CrossRefGoogle ScholarPubMed
20.Richter-Levin, G.Acute and long-term behavioral correlates of underwater trauma – potential relevance to stress and post-stress syndromes. Psychiatry Res 1998;79:73–83.CrossRefGoogle ScholarPubMed
21.Basser, PJ, Mattiello, J, LeBihan, D.MR diffusion tensor spectroscopy and imaging. Biophys J 1994;66:259–267.CrossRefGoogle ScholarPubMed
22.Moseley, ME, Cohen, Y, Kucharczyk, J et al. Diffusion-weighted MR imaging of anisotropic water diffusion in cat central nervous system. Radiology 1990;176:439–445.CrossRefGoogle ScholarPubMed
23.Beaulieu, C.The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 2002;15:435–455.CrossRefGoogle ScholarPubMed
24.Abe, O, Yamasue, H, Kasai, K et al. Voxel-based diffusion tensor analysis reveals aberrant anterior cingulum integrity in posttraumatic stress disorder due to terrorism. Psychiatry Res 2006;146:231–242.CrossRefGoogle ScholarPubMed
25.Kim, MJ, Lyoo, IK, Kim, SJ et al. Disrupted white matter tract integrity of anterior cingulate in trauma survivors. Neuroreport 2005;16:1049–1053.CrossRefGoogle ScholarPubMed
26.Kim, SJ, Jeong, DU, Sim, ME et al. Asymmetrically altered integrity of cingulum bundle in posttraumatic stress disorder. Neuropsychobiology 2006;54:120–125.CrossRefGoogle ScholarPubMed
27.Wang, HH, Zhang, ZJ, Tan, QR et al. Psychopathological, biological, and neuroimaging characterization of posttraumatic stress disorder in survivors of a severe coal mining disaster in China. J Psychiatr Res 2010;44:385–392.CrossRefGoogle ScholarPubMed
28.Sachinvala, N, Kling, A, Suffin, S, Lake, R, Cohen, M.Increased regional cerebral perfusion by 99mTc hexamethyl propylene amine oxime single photon emission computed tomography in post-traumatic stress disorder. Mil Med 2000;165:473–479.CrossRefGoogle ScholarPubMed
29.Bremner, JD, Staib, LH, Kaloupek, D, Southwick, SM, Soufer, R, Charney, DS.Neural correlates of exposure to traumatic pictures and sound in Vietnam combat veterans with and without posttraumatic stress disorder: a positron emission tomography study. Biol Psychiatry 1999;45:806–816.CrossRefGoogle ScholarPubMed
30.Frewen, PA, Lanius, RA, Dozois, DJ et al. Clinical and neural correlates of alexithymia in posttraumatic stress disorder. J Abnorm Psychol 2008;117:171–181.CrossRefGoogle ScholarPubMed
31.Whalley, MG, Rugg, MD, Smith, AP, Dolan, RJ, Brewin, CR.Incidental retrieval of emotional contexts in post-traumatic stress disorder and depression: an fMRI study. Brain Cogn 2009;69:98–107.CrossRefGoogle ScholarPubMed
32.Peterlin, B, Tietjen, G, Meng, S, Lidicker, J, Bigal, M.Post-traumatic stress disorder in episodic and chronic migraine. Headache 2008;48:517–522.CrossRefGoogle ScholarPubMed
33.Barnes, L, Harp, D, Jung, W.Reliability generalization of scores on the Spielberger state-trait anxiety inventory. Educ Psychol Meas 2002;62:603.CrossRefGoogle Scholar
34.Beck, AT.Depression: causes and treatment. Philadelphia: University of Pennsylvania Press, 1967.Google Scholar
35.Ma, N, Li, L, Shu, N et al. White matter abnormalities in first-episode, treatment-naive young adults with major depressive disorder. Am J Psychiatry 2007;164:823–826.CrossRefGoogle ScholarPubMed
36.Basser, PJ, Mattiello, J, LeBihan, D.Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson 1994;103:247–254.CrossRefGoogle ScholarPubMed
37.Hao, Y, Yan, Q, Liu, H, Xu, L, Xue, Z, Song, X.Schizophrenia patients and their healthy siblings share disruption of white matter integrity in the left prefrontal cortex and the hippocampus but not the anterior cingulate cortex. Schizophr Res 2009;114:128–135.CrossRefGoogle Scholar
38.Assaf, Y, Pasternak, O.Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 2008;34:51–61.CrossRefGoogle ScholarPubMed
39.Reading, S, Yassa, M, Bakker, A et al. Regional white matter change in pre-symptomatic Huntington's disease: a diffusion tensor imaging study. Psychiatry Res 2005;140: 55–62.CrossRefGoogle ScholarPubMed
40.Villain, N, Fouquet, M, Baron, J et al. Sequential relationships between grey matter and white matter atrophy and brain metabolic abnormalities in early Alzheimer's disease. Brain 2010;133:3301–3314.CrossRefGoogle ScholarPubMed
41.Fouquet, M, Desgranges, B, Landeau, B et al. Longitudinal brain metabolic changes from amnestic mild cognitive impairment to Alzheimer's disease. Brain 2009;132:2058.CrossRefGoogle ScholarPubMed
42.Chetelat, G, Landeau, B, Eustache, F et al. Using voxel-based morphometry to map the structural changes associated with rapid conversion in MCI: a longitudinal MRI study. Neuroimage 2005;27:934–946.CrossRefGoogle ScholarPubMed
43.Han, DH, Renshaw, PF, Dager, SR et al. Altered cingulate white matter connectivity in panic disorder patients. J Psychiatr Res 2008;42:399–407.CrossRefGoogle ScholarPubMed
44.Sui, SG, Wu, MX, King, ME et al. Abnormal grey matter in victims of rape with PTSD in Mainland China: a voxel-based morphometry study. Acta Neuropsychiatrica 2010;22:118–126.CrossRefGoogle ScholarPubMed
45.Tuerk, PW, Grubaugh, AL, Hamner, MB, Foa, EB.Diagnosis and treatment of PTSD-related compulsive checking behaviors in veterans of the Iraq war: the influence of military context on the expression of PTSD symptoms. Am J Psychiatry 2009;166:762–767.CrossRefGoogle ScholarPubMed
46.Bremner, JD, Vythilingam, M, Vermetten, E et al. Neural correlates of declarative memory for emotionally valenced words in women with posttraumatic stress disorder related to early childhood sexual abuse. Biol Psychiatry 2003;53:879–889.CrossRefGoogle ScholarPubMed
47.Souza, MM, Mello e Souza, T, Vinade, ER et al. Effects of posttraining treatments in the posterior cingulate cortex on short- and long-term memory for inhibitory avoidance in rats. Neurobiol Learn Mem 2002;77:202–210.CrossRefGoogle Scholar
48.Driessen, M, Beblo, T, Mertens, M et al. Posttraumatic stress disorder and fMRI activation patterns of traumatic memory in patients with borderline personality disorder. Biol Psychiatry 2004;55:603–611.CrossRefGoogle ScholarPubMed
49.Lanius, RA, Williamson, PC, Densmore, M et al. The nature of traumatic memories: a 4-T FMRI functional connectivity analysis. Am J Psychiatry 2004;161:36–44.CrossRefGoogle ScholarPubMed
50.Geuze, E, Vermetten, E, Ruf, M, de Kloet, CS, Westenberg, HG.Neural correlates of associative learning and memory in veterans with posttraumatic stress disorder. J Psychiatr Res 2008;42:659–669.CrossRefGoogle ScholarPubMed
51.Masaki, Y, Nishikawa, T, Ikejiri, Y et al. Neural substrates of emotionally valenced episodic memory: a PET study using film stimuli. Psychiatry Clin Neurosci 2006;60:S46–S51.CrossRefGoogle Scholar
52.Lanius, R.Dr. Lanius replies. Am J Psychiatry 2004;161: 1927.CrossRefGoogle Scholar
53.Hull, A.Neuroimaging findings in post-traumatic stress disorder: systematic review. Br J Psychiatry 2002;181:102–110.Google ScholarPubMed
54.Garieballa, SS, Schauer, M, Neuner, F et al. Traumatic events, PTSD, and psychiatric comorbidity in forensic patients – assessed by questionnaires and diagnostic interview. Clin Pract Epidemol Ment Health 2006;2:7.CrossRefGoogle ScholarPubMed
55.Mayou, R, Bryant, B, Ehlers, A.Prediction of psychological outcomes one year after a motor vehicle accident. Am J Psychiatry 2001;158:1231–1238.CrossRefGoogle ScholarPubMed
56.Marshall, RD, Olfson, M, Hellman, F, Blanco, C, Guardino, M, Struening, EL.Comorbidity, impairment, and suicidality in subthreshold PTSD. Am J Psychiatry 2001;158:1467–1473.CrossRefGoogle ScholarPubMed
57.Etkin, A, Klemenhagen, KC, Dudman, JT et al. Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces. Neuron 2004;44:1043–1055.CrossRefGoogle ScholarPubMed
58.Bench, C, Friston, K, Brown, R, Frackowiak, R, Dolan, R.Regional cerebral blood flow in depression measured by positron emission tomography: the relationship with clinical dimensions. Psychol Med 1993;23:579–590.CrossRefGoogle ScholarPubMed
59.Neumeister, A, Bain, E, Nugent, AC et al. Reduced serotonin type 1A receptor binding in panic disorder. J Neurosci 2004;24:589–591.CrossRefGoogle ScholarPubMed
60.Kim, J, Gorman, J.The psychobiology of anxiety. Clin Neurosci Res 2005;4:335–347.CrossRefGoogle Scholar
61.Spindelegger, C, Lanzenberger, R, Wadsak, W et al. Influence of escitalopram treatment on 5-HT 1A receptor binding in limbic regions in patients with anxiety disorders. Mol Psychiatry 2009;14:1040–1050.CrossRefGoogle ScholarPubMed
62.Etkin, A, Pittenger, C, Polan, H, Kandel, E.Toward a neurobiology of psychotherapy: basic science and clinical applications. J Neuropsychiatry Clin Neurosci 2005;17:145.CrossRefGoogle Scholar
63.Phillips, M, Marks, I, Senior, C et al. A differential neural response in obsessive–compulsive disorder patients with washing compared with checking symptoms to disgust. Psychol Med 2000;30:1037–1050.CrossRefGoogle ScholarPubMed
64.Ochsner, KN, Ludlow, DH, Knierim, K et al. Neural correlates of individual differences in pain-related fear and anxiety. Pain 2006;120:69–77.CrossRefGoogle ScholarPubMed
65.Tillfors, M, Furmark, T, Marteinsdottir, I et al. Cerebral blood flow in subjects with social phobia during stressful speaking tasks: a PET study. Am J Psychiatry 2001;158:1220–1226.CrossRefGoogle ScholarPubMed