Reduced cortical thickness in veterans exposed to early life trauma

Psychiatry Research - Neuroimaging

Volumn 223, Issue 2, 2014, Pages 53-60

  Corbo, Vincent ^a,b,c   Salat, David H ^a,c,d   Amick, Melissa M ^a,b   Leritz, Elizabeth C ^a,f   Milberg, William P ^a,e   McGlinchey, Regina E ^a,e  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Neuroimaging Research for Veterans (NeRVe) Center VA Boston Healthcare   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Amygdala; Cortical thickness; Posterior cingulate; Posttraumatic stress disorder (PTSD); Trauma

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); DISEASE ASSOCIATION; EARLY LIFE STRESS; FEMALE; HIPPOCAMPUS; HUMAN; IRAQ; MALE; MENTAL DISEASE; MILITARY DEPLOYMENT; MORPHOMETRICS; NUCLEAR MAGNETIC RESONANCE IMAGING; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; SOCIAL ENVIRONMENT; TRAUMATIC BRAIN INJURY; VETERAN; BRAIN CORTEX; CHILD; CINGULATE GYRUS; LIFE EVENT; MIDDLE AGED; ORGAN SIZE; PATHOLOGY; PRESCHOOL CHILD; PSYCHOLOGY; QUESTIONNAIRE; UNITED STATES; WAR;

ADULT; AFGHAN CAMPAIGN 2001-; AMYGDALA; CEREBRAL CORTEX; CHILD; CHILD, PRESCHOOL; FEMALE; GYRUS CINGULI; HIPPOCAMPUS; HUMANS; IRAQ WAR, 2003-2011; LIFE CHANGE EVENTS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; ORGAN SIZE; QUESTIONNAIRES; STRESS DISORDERS, POST-TRAUMATIC; UNITED STATES; VETERANS;

EID: 84903754642     PISSN: 09254927     EISSN: 18727506     Source Type: Journal    
DOI: 10.1016/j.pscychresns.2014.04.013     Document Type: Article

References (68)

1. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 2004, APA, Washington DC, (text revision). 4th ed.
2. Andersen S.L., Tomada A., Vincow E.S., Valente E., Polcari A., Teicher M.H. Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. Journal of Neuropsychiatry and Clinical Neurosciences 2008, 20:292-301.
3. Beckmann M., Johansen-Berg H., Rushworth M.F. Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. Journal of Neurosciences 2009, 29:1175-1190.
4. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of Royal Statistical Society Series B: Methodological 1995, 57:289-300.
5. Blake D.D., Weathers F.W., Nagy L.M., Kaloupek D.G., Gusman F.D., Charney D.S., Keane T.M. The development of a clinician administered PTSD scale. Journal of Traumatic Stress 1995, 8:75-90.
6. Bremner J.D., Narayan M., Staib L., Southwick S., McGlashan T., Charney D.S. Neural correlates of memories of childhood sexual abuse in women with and without posttraumatic stress disorder. American Journal of Psychiatry 1999, 156:1787-1795.
7. Breslau N. The epidemiology of posttraumatic stress disorder: what is the extent of the problem?. Journal of Clinical Psychiatry 2001, 62:16-22.
8. Breslau N., Kessler R.C., Chilcoat H.D., Schultz L.R., Davis G.C., Andreski P. Trauma and posttraumatic stress disorder in the community: the 1996 Detroit Area Survey of Trauma. Archives of General Psychiatry 1998, 55:626-632.
9. Brunson K.L., Eghbal-Ahmadi M., Bender R., Chen Y., Baram T.Z. Long-term, progressive hippocampal cell loss and dysfunction induced by early-life administration of corticotropin-releasing hormone reproduce the effects of early-life stress. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:8856-8861.
10. Buckner R.L., Head D., Parker J., Fotenos A.F., Marcus D., Morris J.C., Snyder A.Z. A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage 2004, 23:724-738.
11. Buss C., Lord C., Wadiwalla M., Hellhammer D.H., Lupien S.J., Meaney M.J., Pruessner J.C. Maternal care modulates the relationship between prenatal risk and hippocampal volume in women but not in men. Journal of Neurosciences 2007, 27:2592-2595.
12. Carpenter L.L., Tyrka A.R., McDougle C.J., Malison R.T., Owens M.J., Nemeroff C.B., Price L.H. Cerebrospinal fluid corticotropin-releasing factor and perceived early-life stress in depressed patients and healthy control subjects. Neuropsychopharmacology 2004, 29:777-784.
13. Carrion V.G., Weems C.F., Reiss A.L. Stress predicts brain changes in children: a pilot longitudinal study on youth stress, posttraumatic stress disorder, and the hippocampus. Pediatrics 2007, 119:509-516.
14. Chen Y., Bender R.A., Brunson K.L., Pomper J.K., Grigoriadis D.E., Wurst W., Baram T.Z. Modulation of dendritic differentiation by corticotropin-releasing factor in the developing hippocampus. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:15782-15787.
15. Cohen R.A., Grieve S., Hoth K.F., Paul R.H., Sweet L., Tate D., Gunstad J., Stroud L., McCaffery J., Hitsman B., Niaura R., Clark C.R., McFarlane A., Bryant R., Gordon E., Williams L.M. Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biological Psychiatry 2006, 59:975-982.
16. Corrigan J.D., Bogner J. Initial reliability and validity of the Ohio State University TBI Identification Method. Journal of Head Trauma and Rehabilitation 2007, 22:318-329.
17. Dale A.M., Fischl B., Sereno M.I. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 1999, 9:179-194.
18. Dannlowski U., Stuhrmann A., Beutelmann V., Zwanzger P., Lenzen T., Grotegerd D., Domschke K., Hohoff C., Ohrmann P., Bauer J., Lindner C., Postert C., Konrad C., Arolt V., Heindel W., Suslow T., Kugel H. Limbic scars: long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biological Psychiatry 2012, 71:286-293.
19. Desikan R.S., Segonne F., Fischl B., Quinn B.T., Dickerson B.C., Blacker D., Buckner R.L., Dale A.M., Maguire R.P., Hyman B.T., Albert M.S., Killiany R.J. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006, 31:968-980.
20. Dickerson B.C., Bakkour A., Salat D.H., Feczko E., Pacheco J., Greve D.N., Grodstein F., Wright C.I., Blacker D., Rosas H.D., Sperling R.A., Atri A., Growdon J.H., Hyman B.T., Morris J.C., Fischl B., Buckner R.L. The cortical signature of Alzheimer[U+05F3]s disease: regionally specific cortical thinning relates to symptom severity in very mild to mild AD dementia and is detectable in asymptomatic amyloid-positive individuals. Cerebral Cortex 2009, 19:497-510.
21. Dickie E.W., Brunet A., Akerib V., Armony J.L. Anterior cingulate cortical thickness is a stable predictor of recovery from post-traumatic stress disorder. Psychological Medicine 2013, 43(3):645-653.
22. Fischl B., Dale A.M. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:11050-11055.
23. Fischl B., Salat D.H., 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 A.M. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002, 33:341-355.
24. Fischl B., Sereno M.I., Dale A.M. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 1999, 9:195-207.
25. Fortier C.B., Amick M., Grande L., McGlynn S., Kenna A., Morra L., Clark B.A., Milberg W.P., McGlinchey R.E. The Boston Assessment of Traumatic Brain Injury-Lifetime (BAT-L) semi-structured interview: evidence of research utility and validity. Journal of Head Trauma Rehabilitation 2013, 66:1373-1382.
26. Fortier C.B., Amick M., Kenna A., Milberg W.P., McGlinchey R.E. Correspondence of the Boston Assessment of Traumatic Brain Injury-Lifetime (BAT-L) Clinical Interview and the VA TBI Screening Instrument. Journal of Head Trauma Rehabilitation 2014, 29(1):89-98. http://dx.doi.org/10.1097/HTR.0b013e3182865859.
27. Geuze E., Westenberg H.G., Heinecke A., de Kloet C.S., Goebel R., Vermetten E. Thinner prefrontal cortex in veterans with posttraumatic stress disorder. Neuroimage 2008, 41:675-681.
28. Gilbertson M.W., Shenton M., Ciszewski A., Kasai K., Lasko N.B., Orr S.P., Pitman R.K. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nature Neuroscience 2002, 5:1242-1247.
29. Gronenschild E.H., Habets P., Jacobs H.I., Mengelers R., Rozendaal N., van Os J., Marcelis M. The effects of FreeSurfer version, workstation type, and Macintosh operating system version on anatomical volume and cortical thickness measurements. PLoS One 2012, 7:e38234.
30. Hagler D.J., Saygin A.P., Sereno M.I. Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data. Neuroimage 2006, 33:1093-1103.
31. Hartley C.A., Fischl B., Phelps E.A. Brain structure correlates of individual differences in the acquisition and inhibition of conditioned fear. Cerebral Cortex 2011, 21:1954-1962.
32. Hayes J.P., Hayes S.M., Mikedis A.M. Quantitative meta-analysis of neural activity in posttraumatic stress disorder. Biology of Mood and Anxiety Disorders 2012, 2(1):9.
33. Heim C., Newport D.J., Wagner D., Wilcox M.M., Miller A.H., Nemeroff C.B. The role of early adverse experience and adulthood stress in the prediction of neuroendocrine stress reactivity in women: a multiple regression analysis. Depression and Anxiety 2002, 15:117-125.
34. Heim C.M., Mayberg H.S., Mletzko T., Nemeroff C.B., Pruessner J.C. Decreased cortical representation of genital somatosensory field after childhood sexual abuse. American Journal of Psychiatry 2013, 170:616-623.
35. Hellstrom I.C., Dhir S.K., Diorio J.C., Meaney M.J. Maternal licking regulates hippocampal glucocorticoid receptor transcription through a thyroid hormone-serotonin-NGFI-A signalling cascade. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 2012, 367:2495-2510.
36. Jarnum H., Eskildsen S.F., Steffensen E.G., Lundbye-Christensen S., Simonsen C.W., Thomsen I.S., Frund E.T., Theberge J., Larsson E.M. Longitudinal MRI study of cortical thickness, perfusion, and metabolite levels in major depressive disorder. Acta Psychiatrica Scandinavia 2011, 124:435-446.
37. Kasai K., Yamasue H., Gilbertson M.W., Shenton M.E., Rauch S.L., Pitman R.K. Evidence for acquired pregenual anterior cingulate gray matter loss from a twin study of combat-related posttraumatic stress disorder. Biological Psychiatry 2008, 63:550-556.
38. Kitayama N., Quinn S., Bremner J.D. Smaller volume of anterior cingulate cortex in abuse-related posttraumatic stress disorder. Journal of Affective Disorders 2006, 90:171-174.
39. Koenig L.B., Jacob T., Haber J.R. Validity of the lifetime drinking history: a comparison of retrospective and prospective quantity-frequency measures. Journal of Studies on Alcohol and Drugs 2009, 70:296-303.
40. Kubany E.S., Haynes S.N., Leisen M.B., Owens J.A., Kaplan A.S., Watson S.B., Burns K. Development and preliminary validation of a brief broad-spectrum measure of trauma exposure: the Traumatic Life Events Questionnaire. Psychological Assessment 2000, 12:210-224.
41. Kuo J.R., Kaloupek D.G., Woodward S.H. Amygdala volume in combat-exposed veterans with and without posttraumatic stress disorder: a cross-sectional study. Archives of General Psychiatry 2012, 69:1080-1086.
42. Landre L., Destrieux C., Baudry M., Barantin L., Cottier J.P., Martineau J., Hommet C., Isingrini M., Belzung C., Gaillard P., Camus V., El Hage W. Preserved subcortical volumes and cortical thickness in women with sexual abuse-related PTSD. Psychiatry Research: Neuroimaging 2010, 183:181-186.
43. LeDoux J.E. Emotion circuits in the brain. Annual Review of Neuroscience 2000, 23:155-184.
44. Leritz E.C., Salat D.H., Williams V.J., Schnyer D.M., Rudolph J.L., Lipsitz L., Fischl B., McGlinchey R.E., Milberg W.P. Thickness of the human cerebral cortex is associated with metrics of cerebrovascular health in a normative sample of community dwelling older adults. Neuroimage 2011, 54:2659-2671.
45. Liu Y., Li Y.J., Luo E.P., Lu H.B., Yin H. Cortical thinning in patients with recent onset post-traumatic stress disorder after a single prolonged trauma exposure. PLoS One 2012, 7:e39025.
46. Lupien S.J., Parent S., Evans A.C., Tremblay R.E., Zelazo P.D., Corbo V., Pruessner J.C., Seguin J.R. Larger amygdala but no change in hippocampal volume in 10-year-old children exposed to maternal depressive symptomatology since birth. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:14324-14329.
47. Milad M.R., Quinn B.T., Pitman R.K., Orr S.P., Fischl B., Rauch S.L. 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.
48. Nichols T.E. Multiple testing corrections, nonparametric methods, and random field theory. Neuroimage 2012, 62:811-815.
49. Phan K.L., Wager T., Taylor S.F., Liberzon I. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 2002, 16:331-348.
50. Pitman R.K., Shin L.M., Rauch S.L. Investigating the pathogenesis of posttraumatic stress disorder with neuroimaging. Journal of Clinical Psychiatry 2001, 62:47-54.
51. Rauch S.L., Shin L.M., Segal E., Pitman R., Carson M.A., McMullin K., Whalen P.J., Makris N. Selectively reduced regional cortical volumes in post-traumatic stress disorder. Neuroreport 2003, 14:913-916.
52. Rimol L.M., Hartberg C.B., Nesvag R., Fennema-Notestine C., Hagler D.J., Pung C.J., Jennings R.G., Haukvik U.K., Lange E., Nakstad P.H., Melle I., Andreassen O.A., Dale A.M., Agartz I. Cortical thickness and subcortical volumes in schizophrenia and bipolar disorder. Biological Psychiatry 2010, 68:41-50.
53. Salat D.H., Buckner R.L., Snyder A.Z., Greve D.N., Desikan R.S., Busa E., Morris J.C., Dale A.M., Fischl B. Thinning of the cerebral cortex in aging. Cerebral Cortex 2004, 14:721-730.
54. Shackman A.J., Salomons T.V., Slagter H.A., Fox A.S., Winter J.J., Davidson R.J. The integration of negative affect, pain and cognitive control in the cingulate cortex. Nature Reviews Neuroscience 2011, 12:154-167.
55. Shin L.M., McNally R.J., Kosslyn S.M., Thompson W.L., Rauch S.L., Alpert N.M., Metzger L.J., Lasko N.B., Orr S.P., Piman R.K. 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.
56. Smith M.E. Bilateral hippocampal volume reduction in adults with posttraumatic stress disorder: a meta-analysis of structural MRI studies. Hippocampus 2005, 15:798-807.
57. Stein M.B., Koverola C., Hanna C., Torchia M.G. Hippocampal volume in women victimized by childhood sexual abuse. Psychological Medicine 1997, 27:951-959.
58. Tottenham N., Sheridan M.A. A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing. Frontiers in Human Neuroscience 2009, 3:68.
59. van der Kolk B.A. The neurobiology of childhood trauma and abuse. Child and Adolescent Psychiatric Clinics of North America 2003, 12:293-317. (ix).
60. Vogt B.A. Pain and emotion interactions in subregions of the cingulate gyrus. Nature Reviews Neuroscience 2005, 6:533-544.
61. Vogt B.A., Berger G.R., Derbyshire S.W. Structural and functional dichotomy of human midcingulate cortex. European Journal of Neuroscience 2003, 18:3134-3144.
62. Vogt D.S., Proctor S.P., King D.W., King L.A., Vasterling J.J. Validation of scales from the Deployment Risk and Resilience Inventory in a sample of operation Iraqi Freedom veterans. Assessment 2008, 15:391-403.
63. Vyas A., Mitra R., Shankaranarayana Rao B.S., Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. Journal of Neuroscience 2002, 22:6810-6818.
64. Wignall E.L., Dickson J.M., Vaughan P., Farrow T.F.D., Wilkinson I.D., Hunter M.D., Woodruff P.W.R. Smaller hippocampal volume in patients with recent-onset posttraumatic stress disorder. Biological Psychiatry 2004, 56:832-836.
65. Woodward S.H., Kaloupek D.G., Streeter C.C., Martinez C., Schaer M., Eliez S. Decreased anterior cingulate volume in combat-related PTSD. Biological Psychiatry 2006, 59:582-587.
66. Woon F.L., Hedges D.W. Hippocampal and amygdala volumes in children and adults with childhood maltreatment-related posttraumatic stress disorder: a meta-analysis. Hippocampus 2008, 18:729-736.
67. Yamasue H., Kasai K., Iwanami A., Ohtani T., Yamada H., Abe O., Kuroki N., Fukuda R., Tochigi M., Furukawa S., Sadamatsu M., Sasaki T., Aoki S., Ohtomo K., Asukai N., Kato N. 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.
68. Zhang T.Y., Bagot R., Parent C., Nesbitt C., Bredy T.W., Caldji C., Fish E., Anisman H., Szyf M., Meaney M.J. Maternal programming of defensive responses through sustained effects on gene expression. Biological Psychology 2006, 73:72-89.