Psychiatry Research: Neuroimaging
Volume 146, Issue 3 , Pages 231-242 , 30 April 2006

Voxel-based diffusion tensor analysis reveals aberrant anterior cingulum integrity in posttraumatic stress disorder due to terrorism

  • Osamu Abe

      Affiliations

    • Department of Radiology, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan
    • Corresponding Author InformationCorresponding author. Tel.: +81 3 5800 8666; fax: +81 3 5800 8935.
    • ,
  • Hidenori Yamasue

      Affiliations

    • Department of Neuropsychiatry, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan
    • ,
  • Kiyoto Kasai

      Affiliations

    • Department of Neuropsychiatry, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan
    • ,
  • Haruyasu Yamada

      Affiliations

    • Department of Radiology, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan
    • ,
  • Shigeki Aoki

      Affiliations

    • Department of Radiology, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan
    • ,
  • Akira Iwanami

      Affiliations

    • Department of Medical Technology, Aino University, 4-5-4 Higashioda, Ibaraki, Osaka 567-0012, Japan
    • ,
  • Toshiyuki Ohtani

      Affiliations

    • Department of Neuropsychiatry, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan
    • ,
  • Yoshitaka Masutani

      Affiliations

    • Department of Radiology, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan
    • ,
  • Nobumasa Kato

      Affiliations

    • Department of Neuropsychiatry, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan
    • ,
  • Kuni Ohtomo

      Affiliations

    • Department of Radiology, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan

Received 17 August 2005 ,Revised 28 December 2005 ,Accepted 2 January 2006.

References 

  1. Abe O, Aoki S, Hayashi N, Yamada H, Kunimatsu A, Mori H, et al. Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis. Neurobiology of Aging. 2002;23:433–441
  2. Abe O, Yamada H, Masutani Y, Aoki S, Kunimatsu A, Yamasue H, et al. Amyotrophic lateral sclerosis: diffusion tensor tractography and voxel-based analysis. NMR in Biomedicine. 2004;17:411–416
  3. Agartz I, Momenan R, Rawlings RR, Kerich MJ, Hommer DW. Hippocampal volume in patients with alcohol dependence. Archives of General Psychiatry. 1999;56:356–363
  4. Alexander DC, Pierpaoli C, Basser PJ, Gee JC. Spatial transformations of diffusion tensor magnetic resonance images. IEEE Transactions on Medical Imaging. 2001;20:1131–1139
  5. Armony JL, LeDoux JE. How the brain processes emotional information. Annals of the New York Academy of Sciences. 1997;821:259–270
  6. Asukai N, Nishizono-Maher A. The Japanese Version of Clinician-Administered PTSD Scale. Tokyo: Tokyo Institute of Psychiatry; 1998;
  7. Basser PJ, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophysical Journal. 1994;66:259–267
  8. Bhagat YA, Beaulieu C. Diffusion anisotropy in subcortical white matter and cortical gray matter: changes with aging and the role of CSF-suppression. Journal of Magnetic Resonance Imaging. 2004;20:216–227
  9. Blake DD, Weathers FW, Nagy LM, Kaloupek DG, Gusman FD, Charney DS, et al. The development of a Clinician-Administered PTSD Scale. Journal of Traumatic Stress. 1995;8:75–90
  10. Bonne O, Brandes D, Gilboa A, Gomori JM, Shenton ME, Pitman RK, et al. Longitudinal MRI study of hippocampal volume in trauma survivors with PTSD. American Journal of Psychiatry. 2001;158:1248–1251
  11. Bremner JD, Krystal JH, Southwick SM, Charney DS. Functional neuroanatomical correlates of the effects of stress on memory. Journal of Traumatic Stress. 1995;8:527–553
  12. Bremner JD, Randall P, Scott TM, Bronen RA, Seibyl JP, Southwick SM, et al. MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. American Journal of Psychiatry. 1995;152:973–981
  13. 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. American Journal of Psychiatry. 1999;156:1787–1795
  14. 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. Biological Psychiatry. 1999;45:806–816
  15. Burns J, Job D, Bastin ME, Whalley H, Macgillivray T, Johnstone EC, et al. Structural disconnectivity in schizophrenia: a diffusion tensor magnetic resonance imaging study. British Journal of Psychiatry. 2003;182:439–443
  16. Charney DS, Deutch AY, Krystal JH, Southwick SM, Davis M. Psychobiologic mechanisms of posttraumatic stress disorder. Archives of General Psychiatry. 1993;50:295–305
  17. Eriksson SH, Rugg-Gunn FJ, Symms MR, Barker GJ, Duncan JS. Diffusion tensor imaging in patients with epilepsy and malformations of cortical development. Brain. 2001;124:617–626
  18. Fennema-Notestine C, Stein MB, Kennedy CM, Archibald SL, Jernigan TL. Brain morphometry in female victims of intimate partner violence with and without posttraumatic stress disorder. Biological Psychiatry. 2002;52:1089–1101
  19. Foong J, Symms MR, Barker GJ, Maier M, Miller DH, Ron MA. Investigating regional white matter in schizophrenia using diffusion tensor imaging. NeuroReport. 2002;13:333–336
  20. Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapping. 1995;2:189–210
  21. Gilbertson MW, Shenton ME, Ciszewski A, Kasai K, Lasko NB, Orr SP, et al. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nature Neuroscience. 2002;5:1242–1247
  22. Gilboa A, Shalev AY, Laor L, Lester H, Louzoun Y, Chisin R, et al. Functional connectivity of the prefrontal cortex and the amygdala in posttraumatic stress disorder. Biological Psychiatry. 2004;55:263–272
  23. Gispert JD, Pascau J, Reig S, Martinez-Lazaro R, Molina V, Garcia-Barreno P, et al. Influence of the normalization template on the outcome of statistical parametric mapping of PET scans. NeuroImage. 2003;19:601–612
  24. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS. A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage. 2001;14:21–36
  25. Grillon C, Southwick SM, Charney DS. The psychobiological basis of posttraumatic stress disorder. Molecular Psychiatry. 1996;1:278–297
  26. Gurvits TV, Shenton ME, Hokama H, Ohta H, Lasko NB, Gilbertson MW, et al. Magnetic resonance imaging study of hippocampal volume in chronic, combat-related posttraumatic stress disorder. Biological Psychiatry. 1996;40:1091–1099
  27. Haselgrove JC, Moore JR. Correction for distortion of echo-planar images used to calculate the apparent diffusion coefficient. Magnetic Resonance in Medicine. 1996;36:960–964
  28. Hollingshead AB. Two-Factor Index of Social Position. New Haven, CT: Yale University Press; 1965;
  29. Hunsche S, Moseley ME, Stoeter P, Hedehus M. Diffusion-tensor MR imaging at 1.5 and 3.0 T: initial observations. Radiology. 2001;221:550–556
  30. Jinkins J. Atlas of Neuroradiologic Embryology, Anatomy, and Variants. Philadelphia: Lippincott Williams and Wilkins; 2000;
  31. Jones DK, Symms MR, Cercignani M, Howard RJ. The effect of filter size on VBM analyses of DT-MRI data. NeuroImage. 2005;26:546–554
  32. Klingberg T, Hedehus M, Temple E, Salz T, Gabrieli JD, Moseley ME, et al. Microstructure of temporo-parietal white matter as a basis for reading ability: evidence from diffusion tensor magnetic resonance imaging. Neuron. 2000;25:493–500
  33. Kubicki M, Shenton ME, Salisbury DF, Hirayasu Y, Kasai K, Kikinis R, et al. Voxel-based morphometric analysis of gray matter in first episode schizophrenia. NeuroImage. 2002;17:1711–1719
  34. Lanius RA, Williamson PC, Densmore M, Boksman K, Gupta MA, Neufeld RW, et al. Neural correlates of traumatic memories in posttraumatic stress disorder: a functional MRI investigation. American Journal of Psychiatry. 2001;158:1920–1922
  35. Lanius RA, Williamson PC, Densmore M, Boksman K, Neufeld RW, Gati JS, et al. The nature of traumatic memories: a 4-T FMRI functional connectivity analysis. American Journal of Psychiatry. 2004;161:36–44
  36. Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology. 1986;161:401–407
  37. Lindauer RJ, Vlieger EJ, Jalink M, Olff M, Carlier IV, Majoie CB, et al. Smaller hippocampal volume in Dutch police officers with posttraumatic stress disorder. Biological Psychiatry. 2004;56:356–363
  38. Mangin J, Poupon C, Clark C, Le Bihan D, Bloch I. Eddy–current distortion correction and robust tensor estimation for MR diffusion imaging. In: MICCAI (Medical Image Computing and Computer-assisted Intervention). LNCS2208. 2001;p. 186–194
  39. Minami T, Nobuhara K, Okugawa G, Takase K, Yoshida T, Sawada S, et al. Diffusion tensor magnetic resonance imaging of disruption of regional white matter in schizophrenia. Neuropsychobiology. 2003;47:141–145
  40. Moseley ME, Cohen Y, Kucharczyk J, Mintorovitch J, Asgari HS, Wendland MF, et al. Diffusion-weighted MR imaging of anisotropic water diffusion in cat central nervous system. Radiology. 1990;176:439–445
  41. Mulkern RV, Gudbjartsson H, Westin CF, Zengingonul HP, Gartner W, Guttmann CR, et al. Multi-component apparent diffusion coefficients in human brain. NMR in Biomedicine. 1999;12:51–62
  42. Neil JJ, Shiran SI, McKinstry RC, Schefft GL, Snyder AZ, Almli CR, et al. Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. Radiology. 1998;209:57–66
  43. Niendorf T, Dijkhuizen RM, Norris DG, van Lookeren Campagne M, Nicolay K. Biexponential diffusion attenuation in various states of brain tissue: implications for diffusion-weighted imaging. Magnetic Resonance in Medicine. 1996;36:847–857
  44. Nobuhara K, Okugawa G, Minami T, Takase K, Yoshida T, Yagyu T, et al. Effects of electroconvulsive therapy on frontal white matter in late-life depression: a diffusion tensor imaging study. Neuropsychobiology. 2004;50:48–53
  45. Nurnberger JI, Blehar MC, Kaufmann CA, York-Cooler C, Simpson SG, Harkavy-Friedman J, et al. Diagnostic Interview for Genetic Studies. Rationale, unique features, and training. NIMH Genetics Initiative. Archives of General Psychiatry. 1994;51:849–859
  46. Okugawa G, Nobuhara K, Minami T, Tamagaki C, Takase K, Sugimoto T, et al. Subtle disruption of the middle cerebellar peduncles in patients with schizophrenia. Neuropsychobiology. 2004;50:119–123
  47. Oldfield RC. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia. 1971;9:97–113
  48. Papadakis NG, Xing D, Houston GC, Smith JM, Smith MI, James MF, et al. A study of rotationally invariant and symmetric indices of diffusion anisotropy. Magnetic Resonance Imaging. 1999;17:881–892
  49. Pfefferbaum A, Sullivan EV. Increased brain white matter diffusivity in normal adult aging: relationship to anisotropy and partial voluming. Magnetic Resonance in Medicine. 2003;49:953–961
  50. Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G. Diffusion tensor MR imaging of the human brain. Radiology. 1996;201:637–648
  51. Pitman RK. Post-traumatic stress disorder, hormones, and memory. Biological Psychiatry. 1989;26:221–223
  52. Rauch SL, Whalen PJ, Shin LM, McInerney SC, Macklin ML, Lasko NB, et al. Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biological Psychiatry. 2000;47:769–776
  53. Rauch SL, Shin LM, Segal E, Pitman RK, Carson MA, McMullin K, et al. Selectively reduced regional cortical volumes in post-traumatic stress disorder. NeuroReport. 2003;14:913–916
  54. Richardson MP, Friston KJ, Sisodiya SM, Koepp MJ, Ashburner J, Free SL, et al. Cortical grey matter and benzodiazepine receptors in malformations of cortical development. A voxel-based comparison of structural and functional imaging data. Brain. 1997;120:1961–1973
  55. Rovaris M, Iannucci G, Cercignani M, Sormani MP, De Stefano N, Gerevini S, et al. Age-related changes in conventional, magnetization transfer, and diffusion-tensor MR imaging findings: study with whole-brain tissue histogram analysis. Radiology. 2003;227:731–738
  56. Rugg-Gunn FJ, Eriksson SH, Symms MR, Barker GJ, Duncan JS. Diffusion tensor imaging of cryptogenic and acquired partial epilepsies. Brain. 2001;124:627–636
  57. Sach M, Winkler G, Glauche V, Liepert J, Heimbach B, Koch MA, et al. Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain. 2004;127:340–350
  58. Schuff N, Neylan TC, Lenoci MA, Du AT, Weiss DS, Marmar CR, et al. Decreased hippocampal N-acetylaspartate in the absence of atrophy in posttraumatic stress disorder. Biological Psychiatry. 2001;50:952–959
  59. Shaw ME, Strother SC, McFarlane AC, Morris P, Anderson J, Clark CR, et al. Abnormal functional connectivity in posttraumatic stress disorder. NeuroImage. 2002;15:661–674
  60. Shimony JS, McKinstry RC, Akbudak E, Aronovitz JA, Snyder AZ, Lori NF, et al. Quantitative diffusion-tensor anisotropy brain MR imaging: normative human data and anatomic analysis. Radiology. 1999;212:770–784
  61. Shin LM, McNally RJ, Kosslyn SM, Thompson WL, Rauch SL, Alpert NM, et al. Regional cerebral blood flow during script-driven imagery in childhood sexual abuse-related PTSD: a PET investigation. American Journal of Psychiatry. 1999;156:575–584
  62. Shin LM, Whalen PJ, Pitman RK, Bush G, Macklin ML, Lasko NB, et al. An fMRI study of anterior cingulate function in posttraumatic stress disorder. Biological Psychiatry. 2001;50:932–942
  63. Shin LM, Orr SP, Carson MA, Rauch SL, Macklin ML, Lasko NB, et al. 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. 2004;61:168–176
  64. Stejskal EO, Tanner JE. Spin diffusion measurements: spin-echoes in the presence of a time-dependent field gradient. Journal of Chemical Physics. 1965;42:288–292
  65. Suzuki M, Nohara S, Hagino H, Kurokawa K, Yotsutsuji T, Kawasaki Y, et al. Regional changes in brain gray and white matter in patients with schizophrenia demonstrated with voxel-based analysis of MRI. Schizophrenia Research. 2002;55:41–54
  66. Tisserand DJ, Pruessner JC, Sanz Arigita EJ, van Boxtel MP, Evans AC, Jolles J, et al. Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approaches and voxel-based morphometry. NeuroImage. 2002;17:657–669
  67. Vargha-Khadem F, Watkins KE, Price CJ, Ashburner J, Alcock KJ, Connelly A, et al. Neural basis of an inherited speech and language disorder. Proceedings of the National Academy of Sciences of the United States of America. 1998;95:12695–12700
  68. Villarreal G, Hamilton DA, Petropoulos H, Driscoll I, Rowland LM, Griego JA, et al. Reduced hippocampal volume and total white matter volume in posttraumatic stress disorder. Biological Psychiatry. 2002;52:119–125
  69. Werring DJ, Brassat D, Droogan AG, Clark CA, Symms MR, Barker GJ, et al. The pathogenesis of lesions and normal-appearing white matter changes in multiple sclerosis: a serial diffusion MRI study. Brain. 2000;123:1667–1676
  70. Wignall EL, Dickson JM, Vaughan P, Farrow TF, Wilkinson ID, Hunter MD, et al. Smaller hippocampal volume in patients with recent-onset posttraumatic stress disorder. Biological Psychiatry. 2004;56:832–836
  71. Wright IC, Ellison ZR, Sharma T, Friston KJ, Murray RM, McGuire PK. Mapping of grey matter changes in schizophrenia. Schizophrenia Research. 1999;35:1–14
  72. Yamasue H, Kasai K, Iwanami A, Ohtani T, Yamada H, Abe O, et al. 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. 2003;100:9039–9043
  73. Yoshiura T, Wu O, Zaheer A, Reese TG, Sorensen AG. Highly diffusion-sensitized MRI of brain: dissociation of gray and white matter. Magnetic Resonance in Medicine. 2001;45:734–740

PII: S0925-4927(06)00005-9

doi: 10.1016/j.pscychresns.2006.01.004

Psychiatry Research: Neuroimaging
Volume 146, Issue 3 , Pages 231-242 , 30 April 2006

Article Tools

* Image Usage & Resolution