Stress-induced reduction in hippocampal volume and connectivity with the ventromedial prefrontal cortex are related to maladaptive responses to stressful military service

Human Brain Mapping

Volumn 34, Issue 11, 2013, Pages 2808-2816

  Admon, Roee ^a,b   Leykin, Dmitry ^a,c   Lubin, Gad ^d   Engert, Veronika ^e   Andrews, Julie ^e   Pruessner, Jens ^e   Hendler, Talma ^a,b  

^a TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c TEL HAI COLLEGE   (Israel)

^d Medical Corps Israel Defense Forces   (Israel)

^e DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

Author keywords

DTI; FMRI; Functional connectivity; MRI; PTSD; Structural connectivity; Uncinate fasciculus; Volumetry

Indexed keywords

ADULT; ARTICLE; BRAIN CONNECTIVITY; BRAIN SIZE; DIFFUSION TENSOR IMAGING; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; MALE; MILITARY SERVICE; NEUROPHYSIOLOGY; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; SOLDIER; STRESS; VENTROMEDIAL PREFRONTAL CORTEX; ADAPTIVE BEHAVIOR; ADOLESCENT; IMAGE PROCESSING; ISRAEL; MENTAL STRESS; NERVE TRACT; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; PSYCHOLOGY; VETERAN; YOUNG ADULT;

BIOLOGICAL MARKER;

ADAPTATION, PSYCHOLOGICAL; ADOLESCENT; BIOLOGICAL MARKERS; DIFFUSION TENSOR IMAGING; FEMALE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; ISRAEL; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; PREFRONTAL CORTEX; PSYCHOLOGY, MILITARY; STRESS DISORDERS, POST-TRAUMATIC; STRESS, PSYCHOLOGICAL; VETERANS; YOUNG ADULT;

EID: 84886310407     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22100     Document Type: Article

References (48)

1. Admon R, Lubin G, Rosenblatt JD, Stern O, Kahn I, Assaf M, Hendler T (2012): Imbalanced neural responsivity to risk and reward indicates stress vulnerability in humans. Cereb Cortex. Epub ahead of print.
2. Admon R, Lubin G, Stern O, Rosenberg K, Sela L, Ben-Ami H, Hendler T (2009): Human vulnerability to stress depends on amygdala's predisposition and hippocampal plasticity. Proc Natl Acad Sci USA 106:14120-14125.
3. Blechert J, Michael T, Vriends N, Margraf J, Wilhelm FH (2007): Fear conditioning in posttraumatic stress disorder: Evidence for delayed extinction of autonomic, experiential, and behavioural responses. Behav Res Ther 45:2019-2033.
4. Brambilla P, Barale F, Caverzasi E, Soares JC (2002): Anatomical MRI findings in mood and anxiety disorders. Epidemiol Psichiatr Soc 11:88-99.
5. Bremner JD, Scott TM, Delaney RC, Southwick SM, Mason JW, Johnson DR, Innis RB, McCarthy G, Charney DS (1993): Deficits in short-term memory in posttraumatic stress disorder. Am J Psychiatry 150:1015-1019.
6. Carpenter M (1983): Human Neuroanatomy. Baltimore, MD:Williams & Wilkins.
7. Charney D, Bremner J (1999): The neurobiology of anxiety disorders. In: Charney D, Nestler E, Bunney B, editors.Neurobiology of Mental Illness. Oxford:Oxford University Press. pp494-517.
8. Collins DL, Neelin P, Peters TM, Evans AC (1994): Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr 18:192-205.
9. Diamond DM, Fleshner M, Rose GM (1994): Psychological stress repeatedly blocks hippocampal primed burst potentiation in behaving rats. Behav Brain Res 62:1-9.
10. DSM-IV-TR (2000): American Psychiatric Association: Diagnostic and Statistical Manual of Mental Disorders. Washington, DC:American Psychiatric Association.4 p.
11. Eluvathingal TJ, Chugani HT, Behen ME, Juhasz C, Muzik O, Maqbool M, Chugani DC, Makki M (2006): Abnormal brain connectivity in children after early severe socioemotional deprivation: A diffusion tensor imaging study. Pediatrics 117:2093-2100.
12. Farinelli M, Deschaux O, Hugues S, Thevenet A, Garcia R (2006): Hippocampal train stimulation modulates recall of fear extinction independently of prefrontal cortex synaptic plasticity and lesions. Learn Mem 13:329-334.
13. Foa E, Cashman L, Jaycox L, Perry K (1997): The validation of a self-report measure of posttraumatic stress disorder: The Posttraumatic Diagnostic Scale. Psychol Assess 9:445-451.
14. Giedd JN, Vaituzis AC, Hamburger SD, Lange N, Rajapakse JC, Kaysen D, Vauss YC, Rapoport JL (1996): Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4-18 years. J Comp Neurol 366:223-230.
15. Gilbertson MW, Shenton ME, Ciszewski A, Kasai K, Lasko NB, Orr SP, Pitman RK (2002): Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nat Neurosci 5:1242-1247.
16. Gogtay N, Nugent TF III, Herman DH, Ordonez A, Greenstein D, Hayashi KM, Clasen L, Toga AW, Giedd JN, Rapoport JL, Thompson PM (2006): Dynamic mapping of normal human hippocampal development. Hippocampus 16:664-672.
17. Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E (1997): Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17:2492-2498.
18. Joels M, Karst H, Alfarez D, Heine VM, Qin Y, van Riel E, Verkuyl M, Lucassen PJ, Krugers HJ (2004): Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 7:221-231.
19. Kier EL, Staib LH, Davis LM, Bronen RA (2004): Anatomic dissection tractography: A new method for precise MR localization of white matter tracts. AJNR Am J Neuroradiol 25:670-676.
20. Kim MJ, Whalen PJ (2009): The structural integrity of an amygdala-prefrontal pathway predicts trait anxiety. J Neurosci 29:11614-11618.
21. LaBar KS, Gatenby JC, Gore JC, LeDoux JE, Phelps EA (1998): Human amygdala activation during conditioned fear acquisition and extinction: A mixed-trial fMRI study. Neuron 20:937-945.
22. Lim KO, Helpern JA (2002): Neuropsychiatric applications of DTI-A review. NMR Biomed 15:587-593.
23. Lupien SJ, Evans A, Lord C, Miles J, Pruessner M, Pike B, Pruessner JC (2007): Hippocampal volume is as variable in young as in older adults: Implications for the notion of hippocampal atrophy in humans. Neuroimage 34:479-485.
24. Magarinos AM, McEwen BS, Flugge G, Fuchs E (1996): Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 16:3534-3540.
25. Magarinos AM, Deslandes A, McEwen BS (1999): Effects of antidepressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress. Eur J Pharmacol 371:113-122.
26. McEwen BS (1999): Stress and hippocampal plasticity. Annu Rev Neurosci 22:105-122.
27. Milad MR, Quinn BT, Pitman RK, Orr SP, Fischl B, Rauch SL (2005): Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory. Proc Natl Acad Sci USA 102:10706-10711.
28. Milad MR, Wright CI, Orr SP, Pitman RK, Quirk GJ, Rauch SL (2007): Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol Psychiatry 62:446-454.
29. Milad MR, Orr SP, Lasko NB, Chang Y, Rauch SL, Pitman RK (2008): Presence and acquired origin of reduced recall for fear extinction in PTSD: Results of a twin study. J Psychiatr Res 42:515-520.
30. Milad MR, Pitman RK, Ellis CB, Gold AL, Shin LM, Lasko NB, Zeidan MA, Handwerger K, Orr SP, Rauch SL (2009): Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry 66:1075-1082.
31. Pavlides C, Nivon LG, McEwen BS (2002): Effects of chronic stress on hippocampal long-term potentiation. Hippocampus 12:245-257.
32. Peri T, Ben-Shakhar G, Orr SP, Shalev AY (2000): Psychophysiologic assessment of aversive conditioning in posttraumatic stress disorder. Biol Psychiatry 47:512-519.
33. Phelps EA, Delgado MR, Nearing KI, LeDoux JE (2004): Extinction learning in humans: Role of the amygdala and vmPFC. Neuron 43:897-905.
34. Pruessner JC, Li LM, Serles W, Pruessner M, Collins DL, Kabani N, Lupien S, Evans AC (2000): Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: Minimizing the discrepancies between laboratories. Cereb Cortex 10:433-442.
35. Rothbaum BO, Davis M (2003): Applying learning principles to the treatment of post-trauma reactions. Ann N Y Acad Sci 1008:112-121.
36. Sapolsky R (1992): Stress, the Aging Brain and the Mechanisms of Neuron Death. Cambridge, MA:Massachusetts Institute of Technology.
37. Sapolsky RM, Uno H, Rebert CS, Finch CE (1990): Hippocampal damage associated with prolonged glucocorticoid exposure in primates. J Neurosci 10:2897-2902.
38. Shekhar A, McCann UD, Meaney MJ, Blanchard DC, Davis M, Frey KA, Liberzon I, Overall KL, Shear MK, Tecott LH, Winsky L (2001): Summary of a National Institute of Mental Health workshop: Developing animal models of anxiety disorders. Psychopharmacology (Berl) 157:327-339.
39. Shors TJ, Thompson RF (1992): Acute stress impairs (or induces) synaptic long-term potentiation (LTP) but does not affect paired-pulse facilitation in the stratum radiatum of rat hippocampus. Synapse 11:262-265.
40. Sled JG, Zijdenbos AP, Evans AC (1998): A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87-97.
41. Smith ME (2005): Bilateral hippocampal volume reduction in adults with post-traumatic stress disorder: A meta-analysis of structural MRI studies. Hippocampus 15:798-807.
42. Suzuki M, Hagino H, Nohara S, Zhou SY, Kawasaki Y, Takahashi T, Matsui M, Seto H, Ono T, Kurachi M (2005): Male-specific volume expansion of the human hippocampus during adolescence. Cereb Cortex 15:187-193.
43. Swaab DF, Bao AM, Lucassen PJ (2005): The stress system in the human brain in depression and neurodegeneration. Ageing Res Rev 4:141-194.
44. Talairach J, Tournoux P (1988): Co-planar Stereotaxic Atlas of the Human Brain; 3-Dimensional Proportional System: An Approach to Cerebral Imaging. New York:Thieme.
45. Uno H, Tarara R, Else JG, Suleman MA, Sapolsky RM (1989): Hippocampal damage associated with prolonged and fatal stress in primates. J Neurosci 9:1705-1711.
46. Vermetten E, Vythilingam M, Southwick SM, Charney DS, Bremner JD (2003): Long-term treatment with paroxetine increases verbal declarative memory and hippocampal volume in posttraumatic stress disorder. Biol Psychiatry 54:693-702.
47. Yehuda R, Keefe RS, Harvey PD, Levengood RA, Gerber DK, Geni J, Siever LJ (1995): Learning and memory in combat veterans with posttraumatic stress disorder. Am J Psychiatry 152:137-139.
48. Zola-Morgan SM, Squire LR (1990): The primate hippocampal formation: Evidence for a time-limited role in memory storage. Science 250:288-290.