Magnetic resonance volumetry and spectroscopy of hippocampus and insula in relation to severe exposure of traumatic stress

Psychophysiology

Volumn 49, Issue 2, 2012, Pages 261-270

  Eckart, Cindy ^a,c   Kaufmann, Jörn ^b   Kanowski, Martin ^b   Tempelmann, Claus ^b   Hinrichs, Hermann ^b   Elbert, Thomas ^a   Heinze, Hans Jochen ^b   Kolassa, Iris Tatjana ^a,d  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b University Department of Neurology   (Germany)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d UNIVERSITY OF ULM   (Germany)

Author keywords

Hippocampus; Insula; MR spectroscopy; Posttraumatic stress disorder; Volumetry

Indexed keywords

EID: 84856084664     PISSN: 00485772     EISSN: 14698986     Source Type: Journal    
DOI: 10.1111/j.1469-8986.2011.01303.x     Document Type: Article

References (75)

1. Agartz, I., Momenan, R., Rawlings, R. R., Kerich, M. J., & Hommer, D. W. (1999). Hippocampal volume in patients with alcohol dependence. Archives of General Psychiatry, 56, 356-363. doi: 10.1001/archpsyc.56.4.356
2. Alvarez, R. P., Biggs, A., Chen, G., Pine, D. S., & Grillon, C. (2008). Contextual fear conditioning in humans: Cortical-hippocampal and amygdala contributions. Journal of Neuroscience, 28, 6211-6219. doi: 10.1523/JNEUROSCI.1246-08.2008
3. American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: American Psychiatric Association.
4. Andersen, S. L., Tomada, A., Vincow, E. S., Valente, E., Polcari, A., & Teicher, M. H. (2008). Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. Journal of Neuropsychiatry and Clinical Neurosciences, 20, 292-301. doi: 10.1176/appi.neuropsych.20.3.292
5. Augustine, J. R. (1996). Circuitry and functional aspects of the insular lobe in primates including humans. Brain Research. Brain Research Reviews, 22, 229-244. doi: 10.1016/S0165-0173(96)00011-2
6. Bernstein, D. P., Fink, L., Handelsman, L., Foote, J., Lovejoy, M., & Wenzel, K., ... Ruggiero, J. (1994). Initial reliability and validity of a new retrospective measure of child abuse and neglect. American Journal of Psychiatry, 151, 1132-1136.
7. Blake, D. D., Weathers, F. W., Nagy, L. M., Kaloupek, D. G., Gusman, F. D., & Charney, D. S., & Keane, T. M. (1995). The development of a clinician-administered PTSD scale. Journal of Traumatic Stress, 8, 75-90. doi: 10.1002/jts.2490080106
8. Bonne, O., Brandes, D., Gilboa, A., Gomori, J. M., Shenton, M. E., & Pitman, R. K., & Shalev, A. Y. (2001). Longitudinal MRI study of hippocampal volume in trauma survivors with PTSD. American Journal of Psychiatry, 158, 1248-1251. doi: 10.1176/appi.ajp.158.8.1248
9. Bonne, O., Vythilingam, M., Inagaki, M., Wood, S., Neumeister, A., Nugent, A. C., ... Charney, D. S. (2008). Reduced posterior hippocampal volume in posttraumatic stress disorder. Journal of Clinical Psychiatry, 69, 1087-1091. doi: 10.4088/JCP.v69n0707
10. Bremner, J. D., Vythilingam, M., Vermetten, E., Southwick, S. M., McGlashan, T., Nazeer, A., & Charney, D. S. (2003). MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. American Journal of Psychiatry, 160, 924-932. doi: 10.1176/appi.ajp.160.5.924
11. Choi, J., Jeong, B., Rohan, M. L., Polcari, A. M., & Teicher, M. H. (2009). Preliminary evidence for white matter tract abnormalities in young adults exposed to parental verbal abuse. Biological Psychiatry, 65, 227-234. doi: 10.1016/j.biopsych.2008.06.022
12. Craig, A. D. (2002). How do you feel? Interoception: The sense of the physiological condition of the body. Nature Reviews Neuroscience, 3, 655-666. doi: 10.1038/nrn894
13. Craig, A. D. (2009). How do you feel-now? The anterior insula and human awareness. Nature Reviews Neuroscience, 10, 59-70. doi: 10.1038/nrn2555
14. Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage, 9, 179-194. doi: 10.1006/nimg.1998.0395
15. Dale, A. M., & Sereno, M. I. (1993). Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: A linear approach. Journal of Cognitive Neuroscience, 5, 162-176. doi: 10.1162/jocn.1993.5.2.162
16. De Bellis, M. D., Hall, J., Boring, A. M., Frustaci, K., & Moritz, G. (2001). A pilot longitudinal study of hippocampal volumes in pediatric maltreatment-related posttraumatic stress disorder. Biological Psychiatry, 504, 305-309. doi: 10.1016/S0006-3223(01)01105-2
17. de Quervain, D. J., Kolassa, I. T., Ertl, V., Onyut, P. L., Neuner, F., Elbert, T., & Papassotiropoulos, A. (2007). A deletion variant of the alpha2b-adrenoceptor is related to emotional memory in Europeans and Africans. Nature Neuroscience, 10, 1137-1139. doi: 10.1038/nn1945
18. Driessen, M., Herrmann, J., Stahl, K., Zwaan, M., Meier, S., Hill, A., & Petersen, D. (2000). Magnetic resonance imaging volumes of the hippocampus and the amygdala in women with borderline personality disorder and early traumatization. Archives of General Psychiatry, 57, 1115-1122. doi: 10.1001/archpsyc.57.12.1115
19. Eckart, C., Stoppel, C., Kaufmann, J., Tempelmann, C., Hinrichs, H., Elbert, T., & Kolassa, I.-T. (2011). Structural alterations in lateral prefrontal, parietal and posterior midline regions of men with chronic posttraumatic stress disorder. Journal of Psychiatry and Neuroscience, 36, 176-186. doi: 10.1503/jpn.100010
20. Elbert, T., & Schauer, M. (2002). Burnt into memory. Nature, 419, 883. doi: 10.1038/419883a
21. Elbert, T., Schauer, M., Schauer, E., Huschka, B., Hirth, M., & Neuner, F. (2009). Trauma-related impairment in children-A survey in Sri Lankan provinces affected by armed conflict. Child Abuse & Neglect, 33, 238-246. doi: 10.1016/j.chiabu.2008.02.008
22. Ernst, T., Kreis, R., & Ross, B. D. (1993). Absolute quantitation of water and metabolites in the human brain. Part I: Compartments and water. Journal of Magnetic Resonance, 102, 1-8.
23. Etkin, A., & Wager, T. D. (2007). Functional neuroimaging of anxiety: A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry, 164, 1476-1488. doi: 10.1176/appi.ajp.2007.07030504
24. Fischl, B., Sereno, M. I., & Dale, A. M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. NeuroImage, 9, 195-207. doi: 10.1006/nimg.1998.0396
25. Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Segonne, F., Salat, D. H., ... Dale, A. M. (2004). Automatically parcellating the human cerebral cortex. Cerebral Cortex, 14, 11-22. doi: 10.1093/cercor/bhg087
26. Freeman, T., Kimbrell, T., Booe, L., Myers, M., Cardwell, D., Lindquist, D. M., & Komorowski, R. A. (2006). Evidence of resilience: Neuroimaging in former prisoners of war. Psychiatry Research: Neuroimaging, 146, 59-64. doi: 10.1016/j.pscychresns.2005.07.007
27. Freeman, T. W., Cardwell, D., Karson, C. N., & Komoroski, R. A. (1998). In vivo proton magnetic resonance spectroscopy of the medial temporal lobes of subjects with combat-related posttraumatic stress disorder. Magnetic Resonance in Medicine, 40, 66-71. doi: 10.1002/mrm.1910400110
28. Gahm, G. A., Lucenko, B. A., Retzlaff, P., & Fukuda, S. (2007). Relative impact of adverse events and screened symptoms of posttraumatic stress disorder and depression among active duty soldiers seeking mental health care. Journal of Clinical Psychology, 63, 199-211. doi: 10.1002/jclp.20330
29. Geuze, E., Vermetten, E., & Bremner, J. D. (2005a). MR-based in vivo hippocampal volumetrics: 1. Review of methodologies currently employed. Molecular Psychiatry, 10, 147-159. doi: 10.1038/sj.mp.4001580
30. Geuze, E., Vermetten, E., & Bremner, J. D. (2005b). MR-based in vivo hippocampal volumetrics: 2. Findings in neuropsychiatric disorders. Molecular Psychiatry, 10, 160-184. doi: 10.1038/sj.mp.4001579
31. Gilbertson, M. W., Shenton, M. E., Ciszewski, A., Kasai, K., Lasko, N. B., Orr, S. P., & Pitman, R. K. (2002). Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nature Neuroscience, 5, 1242-1247. doi: 10.1038/nn958
32. Giménez, M., Junqué, C., Narberhaus, A., Caldú, X., Segarra, D., Vendrell, P., ... Mercader, J. M. (2004). Medial temporal MR spectroscopy is related to memory performance in normal adolescent subjects. NeuroReport, 15, 703-707. doi: 10.1097/00001756-200403220-00026
33. Golier, J. A., Yehuda, R., De Santi, S., Segal, S., Dolan, S., & de Leon, M. J. (2005). Absence of hippocampal volume differences in survivors of the Nazi Holocaust with and without posttraumatic stress disorder. Psychiatry Research: Neuroimaging, 139, 53-64. doi: 10.1016/j.pscychresns.2005.02.007
34. Gurvits, T. V., Shenton, M. E., Hokama, H., Ohta, H., Lasko, N. B., Gilbertson, M. W., ... Pitman, R. K. (1996). Magnetic resonance imaging study of hippocampal volume in chronic, combat-related posttraumatic stress disorder. Biological Psychiatry, 40, 1091-1099. doi: 10.1016/S0006-3223(96)00229-6
35. Ham, B. J., Chey, J., Yoon, S. J., Sung, Y., Jeong, D. U., Ju Kim, S., ... Lyoo, K. (2007). Decreased N-acetyl-aspartate levels in anterior cingulate and hippocampus in subjects with post-traumatic stress disorder: A proton magnetic resonance spectroscopy study. European Journal of Neuroscience, 25, 324-329. doi: 10.1111/j.1460-9568.2006.05253.x
36. Hommel, G. (1989). A comparison of two modified Bonferroni procedures. Biometrika, 76, 624-625. doi: 10.1093/biomet/76.3.624
37. Jatzko, A., Rothenhofer, S., Schmitt, A., Gaser, C., Demirakca, T., Weber-Fahr, W., ... Braus, D. F. (2006). Hippocampal volume in chronic posttraumatic stress disorder (PTSD): MRI study using two different evaluation methods. Journal of Affective Disorders, 94, 121-126. doi: 10.1016/j.jad.2006.03.010
38. Johnsen, G. E., & Asbjornsen, A. E. (2008). Consistent impaired verbal memory in PTSD: A meta-analysis. Journal of Affective Disorders, 111, 74-82. doi: 10.1016/j.jad.2008.02.007
39. Kanowski, M., Kaufmann, J., Braun, J., Bernarding, J., & Tempelmann, C. (2004). Quantitation of simulated short echo time 1H human brain spectra by LCModel and AMARES. Magnetic Resonance in Medicine, 51, 904-912. doi: 10.1002/mrm.20063
40. Karl, A., Schaefer, M., Malta, L. S., Dorfel, D., Rohleder, N., & Werner, A. (2006). A meta-analysis of structural brain abnormalities in PTSD. Neuroscience & Biobehavioral Reviews, 30, 1004-1031. doi: 10.1016/j.neubiorev.2006.03.004
41. Karl, A., & Werner, A. (2009). The use of proton magnetic resonance spectroscopy in PTSD research-Meta-analyses of findings and methodological review. Neuroscience & Biobehavioral Reviews, 34, 7-22. doi: 10.1016/j.neubiorev.2009.06.008
42. Kasai, K., Yamasue, H., Gilbertson, M. W., Shenton, M. E., Rauch, S. L., & Pitman, R. K. (2008). Evidence for acquired pregenual anterior cingulate gray matter loss from a twin study of combat-related posttraumatic stress disorder. Biological Psychiatry, 63, 550-556. doi: 10.1016/j.biopsych.2007.06.022
43. Kolassa, I.-T., & Elbert, T. (2007). Structural and functional neuroplasticity in relation to traumatic stress. Current Directions in Psychological Science, 16, 321-325. doi: 10.1111/j.1467-8721.2007.00529.x
44. Kolassa, I. T., Wienbruch, C., Neuner, F., Schauer, M., Ruf, M., Odenwald, M., & Elbert, T. (2007). Altered oscillatory brain dynamics after repeated traumatic stress. BMC Psychiatry, 7, 56. doi: 10.1186/1471-244X-7-56
45. Liberzon, I., & Martis, B. (2006). Neuroimaging studies of emotional responses in PTSD. Annals of the New York Academy of Sciences, 1071, 87-109. doi: 10.1196/annals.1364.009
46. Lindauer, R. J., Vlieger, E. J., Jalink, M., Olff, M., Carlier, I. V., Majoie, C. B., ... Gersons, B. P. (2004). Smaller hippocampal volume in Dutch police officers with posttraumatic stress disorder. Biological Psychiatry, 56, 356-363. doi: 10.1016/j.biopsych.2004.05.021
47. McNally, R. J. (2006). Cognitive abnormalities in post-traumatic stress disorder. Trends in Cognitive Sciences, 10, 271-277. doi: 10.1016/j.tics.2006.04.007
48. Miller, G. A., & Chapman, J. P. (2001). Misunderstanding analysis of covariance. Journal of Abnormal Psychology, 110, 40-48. doi: 10.1037/0021-843X.110.1.40
49. Mohanakrishnan Menon, P., Nasrallah, H. A., Lyons, J. A., Scott, M. F., & Liberto, V. (2003). Single-voxel proton MR spectroscopy of right versus left hippocampi in PTSD. Psychiatry Research: Neuroimaging, 123, 101-108. doi: 10.1016/S0925-4927(03)00044-1
50. O'Donnell, M. L., Creamer, M., & Pattison, P. (2004). Posttraumatic stress disorder and depression following trauma: Understanding comorbidity. American Journal of Psychiatry, 161, 1390-1396. doi: 10.1176/appi.ajp.161.8.1390
51. Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97-113. doi: 10.1016/0028-3932(71)90067-4
52. Osuch, E. A., Benson, B., Geraci, M., Podell, D., Herscovitch, P., McCann, U. D., & Post, R. M. (2001). Regional cerebral blood flow correlated with flashback intensity in patients with posttraumatic stress disorder. Biological Psychiatry, 50, 246-253. doi: 10.1016/S0006-3223(01)01107-6
53. Phan, K. L., Wager, T., Taylor, S. F., & Liberzon, I. (2002). Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI. NeuroImage, 16, 331-348. doi: 10.1006/nimg.2002.1087
54. Pinheiro, J., & Bates, D. (2000). Mixed-effects models in S and S-PLUS. New York, NY: Springer-Verlag. doi: 10.1007/978-1-4419-0318-1
55. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R Core Team. (2008). NLME: Linear and nonlinear mixed effects models. (Version R package version 3.1-90).
56. Pruessner, J. C., Li, L. M., Serles, W., Pruessner, M., Collins, D. L., Kabani, N., ... Evans, A. C. (2000). Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: Minimizing the discrepancies between laboratories. Cerebral Cortex, 10, 433-442. doi: 10.1093/cercor/10.4.433
57. R Development Core Team. (2007). R: A language and environment for statistical computing. Vienna, Austria.
58. Rasch, B., Spalek, K., Buholzer, S., Luechinger, R., Boesiger, P., Papassotiropoulos, A., & deQuervain, D. J. (2009). A genetic variation of the noradrenergic system is related to differential amygdala activation during encoding of emotional memories. Proceedings of the National Academy of Sciences of the U S A, 106, 19191-19196. doi: 10.1073/pnas.0907425106
59. Rolls, E. T., Xiang, J., & Franco, L. (2005). Object, space, and object-space representations in the primate hippocampus. Journal of Neurophysiology, 94, 833-844. doi: 10.1152/jn.01063.2004
60. Rooney, W. D., Johnson, G., Li, X., Cohen, E. R., Kim, S. G., Ugurbil, K., & Springer, C. S., Jr. (2007). Magnetic field and tissue dependencies of human brain longitudinal 1H2O relaxation in vivo. Magnetic Resonance in Medicine, 57, 308-318. doi: 10.1002/mrm.21122
61. Sapolsky, R. M., Uno, H., Rebert, C. S., & Finch, C. E. (1990). Hippocampal damage associated with prolonged glucocorticoid exposure in primates. Journal of Neuroscience, 10, 2897-2902.
62. Sar, V., Tutkun, H., Alyanak, B., Bakim, B., & Baral, I. (2000). Frequency of dissociative disorders among psychiatric outpatients in Turkey. Comprehensive Psychiatry, 41, 216-222. doi: 10.1016/S0010-440X(00)90050-6
63. Schauer, M., Neuner, F., & Elbert, T. (2011). Narrative exposure therapy (2nd ed.). Göttingen, Germany: Hogrefe & Huber.
64. Schmahl, C., Berne, K., Krause, A., Kleindienst, N., Valerius, G., Vermetten, E., & Bohus, M. (2009). Hippocampus and amygdala volumes in patients with borderline personality disorder with or without posttraumatic stress disorder. Journal of Psychiatry & Neuroscience, 34, 289-295.
65. Schuff, N., Neylan, T. C., Fox-Bosetti, S., Lenoci, M., Samuelson, K. W., Studholme, C., ... Weiner, M. H. (2008). Abnormal N-acetylaspartate in hippocampus and anterior cingulate in posttraumatic stress disorder. Psychiatry Research: Neuroimaging, 162, 147-157. doi: 10.1016/j.pscychresns.2007.04.011
66. Schuff, N., Neylan, T. C., Lenoci, M. A., Du, A. T., Weiss, D. S., Marmar, C. R., & Weiner, M. W. (2001). Decreased hippocampal N-acetylaspartate in the absence of atrophy in posttraumatic stress disorder. Biological Psychiatry, 50, 952-959. doi: 10.1016/S0006-3223(01)01245-8
67. Segonne, F., Dale, A. M., Busa, E., Glessner, M., Salat, D., Hahn, H. K., & Fischl, B. (2004). A hybrid approach to the skull stripping problem in MRI. NeuroImage, 22, 1060-1075. doi: 10.1016/j.neuroimage.2004.03.032
68. Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P., Janavs, J., & Weiller, E. (1998). 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, 59 (Suppl 20) 22-33; quiz 34-57.
69. Shin, L. M., Shin, P. S., Heckers, S., Krangel, T. S., Macklin, M. L., Orr, S. P., ... & Rauch, S. L. (2004). Hippocampal function in posttraumatic stress disorder. Hippocampus, 14, 292-300. doi: 10.1002/hipo.10183
70. Stanisz, G. J., Odrobina, E. E., Pun, J., Escaravage, M., Graham, S. J., Bronskill, M. J., & Henkelman, R. M. (2005). T1, T2 relaxation and magnetization transfer in tissue at 3T. Magnetic Resonance in Medicine, 54, 507-512. doi: 10.1002/mrm.20605
71. Teicher, M. H., Andersen, S. L., Polcari, A., Anderson, C. M., Navalta, C. P., & Kim, D. M. (2003). The neurobiological consequences of early stress and childhood maltreatment. Neuroscience & Biobehavioral Reviews, 27, 33-44. doi: 10.1016/S0149-7634(03)00007-1
72. Vythilingam, M., Luckenbaugh, D. A., Lam, T., Morgan, C. A., 3rd, Lipschitz, D., Charney, D. S., ... Southwick, S. M. (2005). Smaller head of the hippocampus in Gulf War-related posttraumatic stress disorder. Psychiatry Research: Neuroimaging, 139, 89-99. doi: 10.1016/j.pscychresns.2005.04.003
73. Woodward, S. H., Kaloupek, D. G., Grande, L. J., Stegman, W. K., Kutter, C. J., Leskin, L., ... Eliez, S. (2009). Hippocampal volume and declarative memory function in combat-related PTSD. Journal of the International Neuropsychological Society: JINS, 15, 830-839. doi: 10.1017/S1355617709990476
74. Woodward, S. H., Kaloupek, D. G., Streeter, C. C., Kimble, M. O., Reiss, A. L., Eliez, S., ... Arsenault, N. J. (2006). Hippocampal volume, PTSD, and alcoholism in combat veterans. American Journal of Psychiatry, 163, 674-681. doi: 10.1176/appi.ajp.163.4.674
75. Zaidi, L. Y., & Foy, D. W. (1994). Childhood abuse experiences and combat-related PTSD. Journal of Traumatic Stress, 7, 33-42. doi: 10.1002/jts.2490070105