Psychiatry Research: Neuroimaging
Volume 174, Issue 3 , Pages 210-216 , 30 December 2009

Smaller amygdala volume and reduced anterior cingulate gray matter density associated with history of post-traumatic stress disorder

  • Mark A. Rogers

      Affiliations

    • Department of Psychology, Monash University, Clayton 3800, Victoria, Australia
    • Corresponding Author InformationCorresponding author. Tel.: +61 3 99053976; fax: +61 3 9905 3948.
  • ,
  • Hidenori Yamasue

      Affiliations

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

      Affiliations

    • Department of Radiology, 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
  • ,
  • Toshiyuki Ohtani

      Affiliations

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

      Affiliations

    • Department of Neuropsychiatry, Showa University School of Medicine, 1-5-8 Hatanodai, Shinagawa-ku, Tokyo, 142-8666, Japan
  • ,
  • Shigeki Aoki

      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, Showa University School of Medicine, 1-5-8 Hatanodai, Shinagawa-ku, Tokyo, 142-8666, Japan
  • ,
  • Kiyoto Kasai

      Affiliations

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

Received 2 October 2007 ,Revised 23 February 2009 ,Accepted 4 June 2009.

References 

  1. Abe O, Yamasue H, Kasai K, Yamada H, Aoki S, Iwanami A, et al. Voxel-based diffusion tensor analysis reveals aberrant anterior cingulum integrity in posttraumatic stress disorder due to terrorism. Psychiatry Research: Neuroimaging. 2006;146:231–242
  2. Asukai N, Ashizono-Maher A. The Japanese Version of Clinician Administered PTSD scale. Tokyo: Tokyo Institute of Psychiatry; 1998;
  3. Asukai N, Kato H, Kawamura N, Kim Y, Yamamoto K, Kishimoto J, et al. Reliability and validity of the Japanese-language version of the Impact of Event Scale-Revised (IES-R-J): four studies of different traumatic events. Journal of Nervous and Mental Disease. 2002;190:175–182
  4. Beckham JC, Lytle BL, Feldman MD. Caregiver burden in partners of Vietnam veterans with posttraumatic stress disorder. Journal of Consulting and Clinical Psychology. 1996;64:1068–1072
  5. Berretta S, Pantazopoulos H, Lange N. Neuron numbers and volume of the amygdala in subjects diagnosed with bipolar disorder or schizophrenia. Biological Psychiatry. 2007;62:884–893
  6. Bonne O, Brandes D, Gilboa A. Longitudinal MRI study of hippocampal volume in trauma survivors with PTSD. American Journal of Psychiatry. 2001;158:1248–1251
  7. Bossini L, Tavanti M, Calossi S, Lombardelli A, Polizzotto NR, Galli R, et al. Magnetic resonance imaging volumes of the hippocampus in drug-naïve patients with post-traumatic stress disorder without comorbidity conditions. Journal of Psychiatric Research. 2008;42:752–762
  8. Bouton ME, Westbrook RF, Corcoran KA, Maren S. Contextual and temporal modulation of extinction: behavioral and biological mechanisms. Biological Psychiatry. 2006;60:352–360
  9. Bremner JD, Randall P, Vermetten E, Staib L, Bronen RA, Mazure C, et al. Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse—a preliminary report. Biological Psychiatry. 1997;41:23–32
  10. Corbo V, Clement MH, Armony JL, Pruessner JC, Brunet A. Size versus shape differences: contrasting voxel-based and volumetric analyses of the anterior cingulate cortex in individuals with acute posttraumatic stress disorder. Biological Psychiatry. 2005;58:119–124
  11. Callicott JH, Bertolino A, Mattay VS, Langheim FJ, Duyn J, Coppola R, et al. Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited. Cerebral Cortex. 2000;10:1078–1092
  12. 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
  13. Friston KJ, Frith CD, Liddle PF, Dolan RJ, Lammertsma AA, Frackowiak RS. The relationship between global and local changes in PET scans. Journal of Cerebral Blood Flow and Metabolism. 1990;10:458–466
  14. Ganzel BL, Kim P, Glover GH, Temple E. Resilience after 9/11: multimodal neuroimaging evidence for stress-related change in the healthy adult brain. Neuroimage. 2008;40:788–795
  15. Geuze E, Vermetten E, Bremner JD. MR-based in vivo hippocampal volumetrics: 2. Findings in neuropsychiatric disorders. Molecular Psychiatry. 2005;10:160–184
  16. Good CD, Johnsrude IS, Ashburner J, Henson RNA, Friston KJ, Frackowiak RSJ. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage. 2001;14:21–36
  17. 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
  18. Herry C, Garcia R. Prefrontal cortex long-term potentiation, but not long-term depression, is associated with the maintenance of extinction of learned fear in mice. Journal of Neuroscience. 2002;22:577–583
  19. Herry C, Mons N. Resistance to extinction is associated with impaired immediate early gene induction in medial prefrontal cortex and amygdala. European Journal of Neuroscience. 2004;20:781–790
  20. Kalisch R, Korenfeld E, Stephan KE, Weiskopf N, Seymour B, Dolan RJ. Context-dependent human extinction memory is mediated by a ventromedial prefrontal and hippocampal network. Journal of Neuroscience. 2006;26:9503–9511
  21. Kitayama N, Quinn S, Bremner JD. Smaller volume of anterior cingulate cortex in abuse-related posttraumatic stress disorder. Journal of Affective Disorders. 2006;90:171–174
  22. Kosten TR, Mason JW, Giller EL, Ostroff RB, Harkness L. Sustained urinary norepinephrine and epinephrine elevation in post-traumatic stress disorder. Psychoneuroendocrinology. 1987;12:13–20
  23. Letizia B, Andrea F, Paolo C. Neuroanatomical changes after eye movement desensitization and reprocessing (EMDR) treatment in posttraumatic stress disorder. Journal of Neuropsychiatry & Clinical Neurosciences. 2007;19:475–476
  24. Lindauer RJL, Vlieger EJ, Jalink M, Olff M, Carlier IVE, Majoie CBLM, et al. Smaller hippocampal volume in Dutch police officers with posttraumatic stress disorder. Biological Psychiatry. 2004;56:356–363
  25. Maes M, Lin A, Bonaccorso S, van Hunsel F, Van Gastel A, Delmeire L, et al. Increased 24-hour urinary cortisol excretion in patients with post-traumatic stress disorder and patients with major depression, but not in patients with fibromyalgia. Acta Psychiatrica Scandinavica. 1998;98:328–335
  26. Massana G, Serra-Grabulosa JM, Salgado-Pineda P, Gasto C, Junque C, Massana J, et al. Amygdalar atrophy in panic disorder patients detected by volumetric magnetic resonance imaging. Neuroimage. 2003;19:80–90
  27. Matsuoka Y, Yamawaki S, Inagaki M, Akechi T, Uchitomi Y. A volumetric study of amygdala in cancer survivors with intrusive recollections. Biological Psychiatry. 2003;54:736–743
  28. Milad MR, Quirk GJ. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature. 2002;420:70–74
  29. Milad MR, Quinn BT, Pitman RK, Orr SP, Fischl B, Rauch SL. Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory. Proceedings of the National Academy of Sciences of the United States of America. 2005;102:10706–10711
  30. Milad MR, Wright CI, Orr SP, Pitman RK, Quirk GJ, Rauch SL. Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biological Psychiatry. 2007;62:446–454
  31. Milad MR, Quirk GJ, Pitman RK, Orr SP, Fischl B, Rauch SL. A role for the human dorsal anterior cingulate cortex in fear expression. Biological Psychiatry. 2007;62:1191–1194
  32. Milham MP, Nugent AC, Drevets WC, Dickstein DP, Leibenluft E, Ernst M, et al. Selective reduction in amygdala volume in pediatric anxiety disorders: a voxel-based morphometry investigation. Biological Psychiatry. 2005;57:961–966
  33. Mitra R, Jadhav S, McEwen BS, Vyas A, Chattarji S. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proceedings of the National Academy of Sciences of the United States of America. 2005;102:9371–9376
  34. Myers K, Davis M. Mechanisms of fear extinction. Molecular Psychiatry. 2007;12:120–150
  35. Perry BD, Giller EL, Southwick SM. Altered platelet alpha 2-adrenergic binding sites in posttraumatic stress disorder. American Journal of Psychiatry. 1987;144:1511–1512
  36. Phelps EA, Delgado MR, Nearing KI, Le Doux . Extinction learning in humans: role of the amygdala and vmPFC. Neuron. 2004;43:897–905
  37. Pitman RK, Shin LM, Rauch SL. Investigating the pathogenesis of post-traumatic stress disorder with neuroimaging. Journal of Clinical Psychiatry. 2001;62:47–54
  38. 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
  39. Rauch SL, Shin LM, Phelps EA. Neurocircuitry: models of posttraumatic stress disorder and extinction: human neuroimaging research—past, present, and future. Biological Psychiatry. 2006;60:376–382
  40. 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
  41. Schumann CM, Hamstra J, Goodlin-Jones BL, Lotspeich LJ, Kwon H, Buonocore MH, et al. The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. Journal of Neuroscience. 2004;24:6392–6401
  42. Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, et al. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry. 1998;59:22–33
  43. Sheline YI, Barch DM, Donnelly JK, Ollinger JM, Snyder AZ, Mintun MA. Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biological Psychiatry. 2001;50:651–658
  44. Shenton ME, Dickey CC, Frumin M, McCarley RW. A review of MRI findings in schizophrenia. Schizophrenia Research. 2001;49:1–52
  45. 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
  46. Southwick SM, Paige S, Morgan CA, Bremner JD, Krystal JH, Charney DS. Neurotransmitter alterations in PTSD: catecholamines and serotonin. Seminars in Clinical Neuropsychiatry. 1999;4:242–248
  47. Talairach J, Tournoux P. Co-Planar Stereotaxic Atlas of the Human Brain. Stuttgart: George Thieme; 1988;
  48. van Erp TGM, Saleh PA, Rosso IM, Huttunen M, Lonnqvist J, Pirkola T, et al. Contributions of genetic risk and fetal hypoxia to hippocampal volume in patients with schizophrenia or schizoaffective disorder, their unaffected siblings, and healthy unrelated volunteers. American Journal of Psychiatry. 2002;159:1514–1520
  49. Vermetten E, Schmahl C, Lindner S, Loewenstein RJ, Bremner JD. Hippocampal and amygdalar volumes in dissociative identity disorder. American Journal of Psychiatry. 2006;163:630–636
  50. Villarreal G, King CY. Brain imaging in post traumatic stress disorder. Seminars in Clinical Neuropsychiatry. 2001;6:131–145
  51. Vogt BA. Pain and emotion interactions in subregions of the cingulate gyrus. Nature Reviews Neuroscience. 2005;6:533–544
  52. Vyas A, Bernal S, Chattarji S. Effects of chronic stress on dendritic arborization in the central and extended amygdala. Brain Research. 2003;965:290–294
  53. 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
  54. Woodward SH, Kaloupek DG, Streeter CC, Martinez C, Schaer M, Eliez S. Decreased anterior cingulate volume in combat-related PTSD. Biological Psychiatry. 2006;59:582–587
  55. Woon FL, Hedges DW. Hippocampal and amygdala volumes in children and adults with childhood maltreatment-related posttraumatic stress disorder: a meta-analysis. Hippocampus. 2008;18:729–736
  56. Wright IC, Ellison ZR, Sharma T, Friston KJ, Murray R, McGuire PK. Mapping of gray matter changes in schizophrenia. Schizophrenia Research. 1999;35:1–14
  57. Yamasue H, Kasai K, Iwanami A, Ohtani T, Abe O, Kuroki N, et al. Voxel-based analysis of MRI reveals anterior cingulated gray-matter volume reduction in post traumatic stress disorder due to terrorism. Proceedings of the National Academy of Sciences of the United States of America. 2003;100:9039–9043
  58. Yamasue H, Iwanami A, Hirayasu Y, Yamada H, Abe O, Kuroki N, et al. Localized volume reduction in prefrontal, temporolimbic, and paralimbic regions in schizophrenia: an MRI parcellation study. Psychiatry Research: Neuroimaging. 2004;131:195–207
  59. Yamasue H, Abe O, Kasai K, Suga M, Iwanami A, Yamada H, et al. Human brain structural change related to acute single exposure to sarin. Annals of Neurology. 2007;61:37–46
  60. Yehuda R, Kahana B, Binder-Brynes K, Southwick SM, Mason JW, Giller EL. Low urinary cortisol excretion in Holocaust survivors with posttraumatic stress disorder. American Journal of Psychiatry. 1995;152:982–986

PII: S0925-4927(09)00144-9

doi: 10.1016/j.pscychresns.2009.06.001

Psychiatry Research: Neuroimaging
Volume 174, Issue 3 , Pages 210-216 , 30 December 2009