Magnetic resonance imaging of hippocampal subfields in posttraumatic stress disorder

Archives of General Psychiatry

Volumn 67, Issue 3, 2010, Pages 296-303

  Wang, Zhen ^a,b,c   Neylan, Thomas C ^b,c   Mueller, Susanne G ^b,d   Lenoci, Maryann ^b,c   Truran, Diana ^b   Marmar, Charles R ^b,c   Weiner, Michael W ^b,d   Schuff, Norbert ^b,d  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIDEPRESSANT AGENT;

ADULT; AGE DISTRIBUTION; ARTICLE; BRAIN ATROPHY; BRAIN SIZE; CASE CONTROL STUDY; CLINICAL ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPUS; HUMAN; MALE; NEUROIMAGING; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; POSTTRAUMATIC STRESS DISORDER; VETERAN;

ADULT; AGE FACTORS; ATROPHY; CA3 REGION, HIPPOCAMPAL; CASE-CONTROL STUDIES; DENDRITIC CELLS; DENTATE GYRUS; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEUROGENESIS; STRESS DISORDERS, POST-TRAUMATIC; VETERANS;

EID: 77649226360     PISSN: 0003990X     EISSN: 15383636     Source Type: Journal    
DOI: 10.1001/archgenpsychiatry.2009.205     Document Type: Article

References (61)

1. Pine DS. Anxiety disorders: clinical features. In: Sadock BJ, Sadock VA, eds. Kaplan and Sadock's Comprehensive Textbook of Psychiatry. Philadelphia, PA: Lippincott Williams & Wilkins; 2000:1476-1490.
2. Kessler RC, Sonnega A, Bromet E, Hughes M, Nelson CB. Posttraumatic stress disorder in the National Comorbidity Survey. Arch Gen Psychiatry. 1995;52(12):1048-1060.
3. Sapolsky RM. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry. 2000;57(10):925-935.
4. Bremner JD, Randall P, Scott TM, Bronen RA, Seibyl JP, Southwick SM, Delaney RC, McCarthy G, Charney DS, Innis RB. MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. Am J Psychiatry. 1995;152(7):973-981.
5. Gurvits TV, Shenton ME, Hokama H, Ohta H, Lasko NB, Gilbertson MW, Orr SP, Kikinis R, Jolesz FA, McCarley RW, Pitman RK. Magnetic resonance imaging study of hippocampal volume in chronic, combat-related posttraumatic stress disorder. Biol Psychiatry. 1996;40(11):1091-1099.
6. Gilbertson MW, Shenton ME, Ciszewski A, Kasai K, Lasko NB, Orr SP, Pitman RK. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nat Neurosci. 2002;5(11):1242-1247.
7. Hedges DW, Allen S, Tate DF, Thatcher GW, Miller MJ, Rice SA, Cleavinger HB, Sood S, Bigler ED. Reduced hippocampal volume in alcohol and substance naive Vietnam combat veterans with posttraumatic stress disorder. Cogn Behav Neurol. 2003;16(4):219-224.
8. Bremner JD, Randall P, Vermetten E, Staib L, Bronen RA, Mazure C, Capelli S, McCarthy G, Innis RB, Charney DS. Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse: a preliminary report. Biol Psychiatry. 1997;41(1):23-32.
9. Woodward SH, Kaloupek DG, Streeter CC, Kimble MO, Reiss AL, Eliez S, Wald LL, Renshaw PF, Frederick BB, Lane B, Sheikh JI, Stegman WK, Kutter CJ, Stewart LP, Prestel RS, Arsenault NJ. Hippocampal volume, PTSD, and alcoholism in combat veterans. Am J Psychiatry. 2006;163(4):674-681.
10. Bonne O, Brandes D, Gilboa A, Gomori JM, Shenton ME, Pitman RK, Shalev AY. Longitudinal MRI study of hippocampal volume in trauma survivors with PTSD. Am J Psychiatry. 2001;158(8):1248-1251.
11. De Bellis MD, Keshavan MS, Clark DB, Casey BJ, Giedd JN, Boring AM, Frustaci K, Ryan ND. AE Bennett research award: developmental traumatology part II: brain development. Biol Psychiatry. 1999;45(10):1271-1284.
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. Biol Psychiatry. 2002;52(11):1089-1101.
13. Golier JA, Yehuda R, De Santi S, Segal S, Dolan S, de Leon MJ. Absence of hippocampal volume differences in survivors of the Nazi Holocaust with and without posttraumatic stress disorder. Psychiatry Res. 2005;139(1):53-64.
14. Schuff N, Neylan TC, Lenoci MA, Du AT, Weiss DS, Marmar CR, Weiner MW. Decreased hippocampal N-acetylaspartate in the absence of atrophy in posttraumatic stress disorder. Biol Psychiatry. 2001;50(12):952-959.
15. Yehuda R, Golier JA, Tischler L, Harvey PD, Newmark R, Yang RK, Buchsbaum MS. Hippocampal volume in aging combat veterans with and without posttraumatic stress disorder: relation to risk and resilience factors. J Psychiatr Res. 2007;41(5):435-445.
16. De Bellis MD, Hall J, Boring AM, Frustaci K, Moritz G. A pilot longitudinal study of hippocampal volumes in pediatric maltreatment-related posttraumatic stress disorder. Biol Psychiatry. 2001;50(4):305-309.
17. Vythilingam M, Luckenbaugh DA, Lam T, Morgan CA III, Lipschitz D, Charney DS, Bremner JD, Southwick SM. Smaller head of the hippocampus in Gulf Warrelated posttraumatic stress disorder. Psychiatry Res. 2005;139(2):89-99.
18. Bonne O, Vythilingam M, Inagaki M, Wood S, Neumeister A, Nugent AC, Snow J, Luckenbaugh DA, Bain EE, Drevets WC, Charney DS. Reduced posterior hippocampal volume in posttraumatic stress disorder. J Clin Psychiatry. 2008;69(7):1087-1091.
19. Duvernoy HM, Cattin F, Naidich TP, et al. The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI. 3rd ed. New York, NY: Springer-Verlag; 2005.
20. Magariños AM, McEwen BS, Flugge G, Fuchs E. Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci. 1996;16(10):3534-3540.
21. Gould E, Tanapat P, McEwen BS, Flugge G, Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci U S A. 1998;95(6):3168-3171.
22. Conrad CD, LeDoux JE, Magarinos AM, McEwen BS. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci. 1999;113(5):902-913.
23. McKittrick CR, Magarinos AM, Blanchard DC, Blanchard RJ, McEwen BS, Sakai RR. Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse. 2000;36(2):85-94.
24. Pham K, Nacher J, Hof PR, McEwen BS. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci. 2003;17(4):879-886.
25. Stewart MG, Davies HA, Sandi C, Kraev IV, Rogachevsky VV, Peddie CJ, Rodriguez JJ, Cordero MI, Donohue HS, Gabbott PL, Popov VI. Stress suppresses and learning induces plasticity in CA3 of rat hippocampus: a three-dimensional ultrastructural study of thorny excrescences and their postsynaptic densities. Neuroscience. 2005;131(1):43-54.
26. Shiryaeva NV, Vshivtseva VV, Mal'tsev NA, Sukhorukov VN, Vaido AI. Neuron density in the hippocampus in rat strains with contrasting nervous system excitability after prolonged emotional-pain stress. Neurosci Behav Physiol. 2008;38(4):355-357.
27. Duan X, Kang E, Liu CY, Ming GL, Song H. Development of neural stem cell in the adult brain. Curr Opin Neurobiol. 2008;18(1):108-115.
28. McEwen BS. Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol. 2008;583(2-3):174-185.
29. Mueller SG, Schuff N, Raptentsetsang S, Elman J, Weiner MW. Selective effect of Apo e4 on CA3 and dentate in normal aging and Alzheimer's disease using high resolution MRI at 4 T. Neuroimage. 2008;42(1):42-48.
30. Mueller SG, Stables L, Du AT, Schuff N, Truran D, Cashdollar N, Weiner MW. Measurement of hippocampal subfields and age-related changes with high resolution MRI at 4T. Neurobiol Aging. 2007;28(5):719-726.
31. Sunanda, Rao MS, Raju TR. Effect of chronic restraint stress on dendritic spines and excrescences of hippocampal CA3 pyramidal neurons: a quantitative study. Brain Res. 1995;694(1-2):312-317.
32. Sandi C, Davies HA, Cordero MI, Rodriguez JJ, Popov VI, Stewart MG. Rapid reversal of stress induced loss of synapses in CA3 of rat hippocampus following water maze training. Eur J Neurosci. 2003;17(11):2447-2456.
33. First MB, Spitzer RL, Gibbon M, Williams JBW. Structured Clinical Interview for Axis I DSM-IV Disorders. New York, NY: Biometrics Research Department, New York State Psychiatric Institute; 1994.
34. Blake DD, Weathers FW, Nagy LM, Kaloupek DG, Gusman FD, Charney DS, Keane TM. The development of a clinician-administered PTSD scale. J Trauma Stress. 1995;8(1):75-90.
35. Wolfe JW, Kimerling R, Brown PJ, Chrestman KR, Levin K. Psychometric review of The Life Stressor Checklist-Revised. In: Stamm BH, ed. Measurement of Stress, Trauma, and Adaptation. Lutherville, MD: Sidran Press; 1996:198-201.
36. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33(3):341-355.
37. Khan AR, Wang L, Beg MF. FreeSurfer-initiated fully-automated subcortical brain segmentation in MRI using large deformation diffeomorphic metric mapping. Neuroimage. 2008;41(3):735-746.
38. Abrous DN, Koehl M, Le Moal M. Adult neurogenesis: from precursors to network and physiology. Physiol Rev. 2005;85(2):523-569.
39. Cameron HA, McKay RD. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol. 2001;435(4):406-417.
40. Kee N, Teixeira CM, Wang AH, Frankland PW. Preferential incorporation of adultgenerated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci. 2007;10(3):355-362.
41. Li S, Wang C, Wang W, Dong H, Hou P, Tang Y. Chronic mild stress impairs cognition in mice: from brain homeostasis to behavior. Life Sci. 2008;82(17-18):934-942.
42. Palmer TD, Takahashi J, Gage FH. The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci. 1997;8(6):389-404.
43. De Kloet ER, Vreugdenhil E, Oitzl MS, Joels M. Brain corticosteroid receptor balance in health and disease. Endocr Rev. 1998;19(3):269-301.
44. McEwen BS. Stress and hippocampal plasticity. Annu Rev Neurosci. 1999;22:105-122.
45. McEwen BS, Gould EA, Sakai RR. The vulnerability of the hippocampus to protective and destructive effects of glucocorticoids in relation to stress. Br J Psychiatry Suppl. 1992;(15):18-23.
46. Sapolsky RM. Stress, glucocorticoids, and damage to the nervous system: the current state of confusion. Stress. 1996;1(1):1-19.
47. Magariños AM, McEwen BS. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience. 1995;69(1):89-98.
48. Sloviter RS, Valiquette G, Abrams GM, Ronk EC, Sollas AL, Paul LA, Neubort S. Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science. 1989;243(4890):535-538.
49. Neylan TC, Schuff N, Lenoci M, Yehuda R, Weiner MW, Marmar CR. Cortisol levels are positively correlated with hippocampal N-acetylaspartate. Biol Psychiatry. 2003;54(10):1118-1121.
50. Miller AH. Inflammation versus glucocorticoids as purveyors of pathology during stress: have we reached the tipping point? Biol Psychiatry. 2008;64(4):263-265.
51. Takemura NU, Kato N. Adult neurogenesis and systemic adaptation: animal experiments and clinical perspectives for PTSD. Prog Brain Res. 2008;167:99-109.
52. Pavlides C, Watanabe Y, McEwen BS. Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus. 1993;3(2):183-192.
53. Pavlides C, Nivon LG, McEwen BS. Effects of chronic stress on hippocampal long-term potentiation. Hippocampus. 2002;12(2):245-257.
54. Tata DA, Marciano VA, Anderson BJ. Synapse loss from chronically elevated glucocorticoids: relationship to neuropil volume and cell number in hippocampal area CA3. J Comp Neurol. 2006;498(3):363-374.
55. Mizoguchi K, Kunishita T, Chui DH, Tabira T. Stress induces neuronal death in the hippocampus of castrated rats. Neurosci Lett. 1992;138(1):157-160.
56. Woodward SH, Kaloupek DG, Streeter CC, Kimble MO, Reiss AL, Eliez S, Wald LL, Renshaw PF, Frederick BB, Lane B, Sheikh JI, Stegman WK, Kutter CJ, Stewart LP, Prestel RS, Arsenault NJ. Brain, skull, and cerebrospinal fluid volumes in adult posttraumatic stress disorder. J Trauma Stress. 2007;20(5):763-774.
57. Kitayama N, Vaccarino V, Kutner M, Weiss P, Bremner JD. Magnetic resonance imaging (MRI) measurement of hippocampal volume in posttraumatic stress disorder: a meta-analysis. J Affect Disord. 2005;88(1):79-86.
58. Du AT, Schuff N, Chao LL, Kornak J, Jagust WJ, Kramer JH, Reed BR, Miller BL, Norman D, Chui HC, Weiner MW. Age effects on atrophy rates of entorhinal cortex and hippocampus. Neurobiol Aging. 2006;27(5):733-740.
59. Morra JH, Tu Z, Apostolova LG, et al. Automated mapping of hippocampal atrophy in 1-year repeat MRI data from 490 subjects with Alzheimer's disease, mild cognitive impairment, and elderly controls. Neuroimage. 2009;45(1 suppl): S3-15.
60. Mahley RW, Weisgraber KH, Huang Y. Apolipoprotein E4: a causative factor and therapeutic target in neuropathology, including Alzheimer's disease. Proc Natl Acad Sci U S A. 2006;103(15):5644-5651.
61. Vermetten E, Vythilingam M, Southwick SM, Charney DS, Bremner JD. Long-term treatment with paroxetine increases verbal declarative memory and hippocampal volume in posttraumatic stress disorder. Biol Psychiatry. 2003;54(7):693-702.