Loss of sustained activity in the ventromedial prefrontal cortex in response to repeated stress in individuals with early-life emotional abuse: Implications for depression vulnerability

Frontiers in Psychology

Volumn 4, Issue JUN, 2013, Pages

  Wang, Lihong ^a,b   Paul, Natalie ^b   Stanton, Steve J ^c,d   Greeson, Jeffrey M ^b   Smoski, Moria J ^b  

^a TSINGHUA UNIVERSITY   (China)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c DUKE UNIVERSITY   (United States)

^d OAKLAND UNIVERSITY   (United States)

Author keywords

Depression resilience; Depression vulnerability; Early life stress; fMRI; Repeated stress; Ventromedial prefrontal cortex

Indexed keywords

EID: 84878887795     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2013.00320     Document Type: Article

References (58)

1. Astur, R. S., St Germain, S. A., Tolin, D., Ford, J., Russell, D., and Stevens, M. (2006). Hippocampus function predicts severity of post-traumatic stress disorder. Cyberpsychol. Behav. 9, 234-240. doi:10.1089/cpb.2006.9.234
2. Baer, R. A., Smith, G. T., Hopkins, J., Krietemeyer, J., and Toney, L. (2006). Using self-report assessment methods to explore facets of mindfulness. Assessment 13, 27-45. doi:10.1177/1073191105283504
3. Bernstein, D., and Fink, P. (1998). Manual for the Childhood Trauma Questionnaire: A Retrospective Self-Report. San Antonio: Harcourt Brace & Co.
4. Bernstein, D. P., Stein, J. A., Newcomb, M. D., Walker, E., Pogge, D., Ahluvalia, T., et al. (2003). Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abuse Negl. 27, 169-190. doi:10.1016/S0145-2134(02)00541-0
5. Binder, E., Malki, K., Paya-Cano, J. L., Fernandes, C., Aitchison, K. J., Mathe, A. A., et al. (2011). Antidepressants and the resilience to early-life stress in inbred mouse strains. Pharmacogenet. Genomics 21, 779-789. doi:10.1097/FPC.0b013e32834b3f35
6. Bird, C. M., Bisby, J. A., and Burgess, N. (2012). The hippocampus and spatial constraints on mental imagery. Front. Hum. Neurosci. 6:142. doi:10.3389/fnhum.2012.00142
7. Bishop, S. R., Lau, M., Shapiro, S., Carlson, L., Anderson, N. D., Carmody, J., et al. (2004). Mindfulness: a proposed operational definition. Clin. Psychol. Sci. Pract. 11, 230-241. doi:10.1093/clipsy/bph077
8. Byrne, P., Becker, S., and Burgess, N. (2007). Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol. Rev. 114, 340-375. doi:10.1037/0033-295X.114.2.340
9. Carli, V., Mandelli, L., Zaninotto, L., Roy, A., Recchia, L., Stoppia, L., et al. (2011). A protective genetic variant for adverse environments? The role of childhood traumas and serotonin transporter gene on resilience and depressive severity in a high-risk population. Eur. Psychiatry 26, 471-478. doi:10.1016/j.eurpsy.2011.04.008
10. Charney, D. S., and Manji, H. K. (2004). Life stress, genes, and depression: multiple pathways lead to increased risk and new opportunities for intervention. Sci. STKE 2004, re5.
11. Cohen, S., Kamarck, T., and Mermelstein, R. (1983). A global measure of perceived stress. J. Health Soc. Behav. 24, 385-396. doi:10.2307/2136404
12. Dickerson, S. S., and Kemeny, M. E. (2004). Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol. Bull. 130, 355-391. doi:10.1037/0033-2909.130.3.355
13. Dickie, E. W., Brunet, A., Akerib, V., and Armony, J. L. (2011). Neural correlates of recovery from post-traumatic stress disorder: a longitudinal fMRI investigation of memory encoding. Neuropsychologia 49, 1771-1778. doi:10.1016/j.neuropsychologia.2011.02.055
14. Fitzgerald, P. B., Laird, A. R., Maller, J., and Daskalakis, Z. J. (2008). A meta-analytic study of changes in brain activation in depression. Hum. Brain Mapp. 29, 683-695. doi:10.1002/hbm.20613
15. Hanh, T. N. T. M. H. (1976). The Miracle of Mindfulness: An Introduction to the Practice of Meditation. Boston: Beacon Press.
16. Harenski, C. L., and Hamann, S. (2006). Neural correlates of regulating negative emotions related to moral violations. Neuroimage 30, 313-324. doi:10.1016/j.neuroimage.2005.09.034
17. Hart, H., and Rubia, K. (2012). Neuroimaging of child abuse: a critical review. Front. Hum. Neurosci. 6:52. doi:10.3389/fnhum.2012.00052
18. Holland, P. C., and Gallagher, M. (2004). Amygdala-frontal interactions and reward expectancy. Curr. Opin. Neurobiol. 14, 148-155. doi:10.1016/j.conb.2004.03.007
19. Jansen, L. M., Gispen-De Wied, C. C., Gademan, P. J., De Jonge, R. C., Van Der Linden, J. A., and Kahn, R. S. (1998). Blunted cortisol response to a psychosocial stressor in schizophrenia. Schizophr. Res. 33, 87-94. doi:10.1016/S0920-9964(98)00066-8
20. Just, N., and Alloy, L. B. (1997). The response styles theory of depression: tests and an extension of the theory. J. Abnorm. Psychol. 106, 221-229. doi:10.1037/0021-843X.106.2.221
21. Keng, S. L., Smoski, M. J., and Robins, C. J. (2011). Effects of mindfulness on psychological health: a review of empirical studies. Clin. Psychol. Rev. 31, 1041-1056. doi:10.1016/j.cpr.2011.04.006
22. Kirschbaum, C., Pirke, K. M., and Hellhammer, D. H. (1993). The "Trier Social Stress Test" - a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28, 76-81. doi:10.1159/000119004
23. Kudielka, B. M., and Kirschbaum, C. (2005). Sex differences in HPA axis responses to stress: a review. Biol. Psychol. 69, 113-132. doi:10.1016/j.biopsycho.2004.11.009
24. Marks, A. D., Sobanski, D. J., and Hine, D. W. (2010). Do dispositional rumination and/or mindfulness moderate the relationship between life hassles and psychological dysfunction in adolescents? Aust. N. Z. J. Psychiatry 44, 831-838. doi:10.3109/00048674
25. Matsumoto, M., Yoshioka, M., and Togashi, H. (2009). Early postnatal stress and neural circuit underlying emotional regulation. Int. Rev. Neurobiol. 85, 95-107. doi:10.1016/S0074-7742(09)85007-1
26. McEwen, B. S. (1999). Stress and hippocampal plasticity. Annu. Rev. Neurosci. 22, 105-122. doi:10.1146/annurev.neuro.22.1.105
27. McEwen, B. S., and Stellar, E. (1993). Stress and the individual. Mechanisms leading to disease. Arch. Intern. Med. 153, 2093-2101. doi:10.1001/archinte.153.18.2093
28. Nolen-Hoeksema, S. (1991). Responses to depression and their effects on the duration of depressive episodes. J. Abnorm. Psychol. 100, 569-582. doi:10.1037/0021-843X.100.4.569
29. Nolen-Hoeksema, S., Morrow, J., and Fredrickson, B. L. (1993). Response styles and the duration of episodes of depressed mood. J. Abnorm. Psychol. 102, 20-28. doi:10.1037/0021-843X.102.1.20
30. Ohira, H., Nomura, M., Ichikawa, N., Isowa, T., Iidaka, T., Sato, A., et al. (2006). Association of neural and physiological responses during voluntary emotion suppression. Neuroimage 29, 721-733. doi:10.1016/j.neuroimage.2005.08.047
31. Ossewaarde, L., Hermans, E. J., Van Wingen, G. A., Kooijman, S. C., Johansson, I. M., Backstrom, T., et al. (2010). Neural mechanisms underlying changes in stress-sensitivity across the menstrual cycle. Psychoneuroendocrinology 35, 47-55. doi:10.1016/j.psyneuen.2009.08.011
32. Paul, N. A., Stanton, S. J., Greeson, J. M., Smoski, M. J., and Wang, L. (2013). Psychological and neural mechanisms of trait mindfulness in reducing depression vulnerability. Soc. Cogn. Affect. Neurosci. 8, 56-64. doi:10.1093/scan/nss070
33. Pechtel, P., and Pizzagalli, D. A. (2011). Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology (Berl.) 214, 55-70. doi:10.1007/s00213-010-2009-2
34. Phelps, E. A., Delgado, M. R., Nearing, K. I., and Ledoux, J. E. (2004). Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43, 897-905. doi:10.1016/j.neuron.2004.08.042
35. Powers, A., Ressler, K. J., and Bradley, R. G. (2009). The protective role of friendship on the effects of childhood abuse and depression. Depress. Anxiety 26, 46-53. doi:10.1002/da.20534
36. Price, J. L. (2005). Free will versus survival: brain systems that underlie intrinsic constraints on behavior. J. Comp. Neurol. 493, 132-139. doi:10.1002/cne.20750
37. Sah, P., Faber, E. S., Lopez De Armentia, M., and Power, J. (2003). The amygdaloid complex: anatomy and physiology. Physiol. Rev. 83, 803-834.
38. Schneider, G. M., Jacobs, D. W., Gevirtz, R. N., and O'Connor, D. T. (2003). Cardiovascular haemodynamic response to repeated mental stress in normotensive subjects at genetic risk of hypertension: evidence of enhanced reactivity, blunted adaptation, and delayed recovery. J. Hum. Hypertens. 17, 829-840. doi:10.1038/sj.jhh.1001624
39. Schultheiss, O. C., and Stanton, S. J. (2009). "Assessment of salivary hormones," in Methods in Social Neuroscience, eds E. Harmon-Jones and J. S. Beer (New York: NY: Guilford Press), 17-44.
40. Shin, L. M., Orr, S. P., Carson, M. A., Rauch, S. L., Macklin, M. L., Lasko, N. B., et al. (2004a). Regional cerebral blood flow in the amygdala and medial prefrontal cortex during traumatic imagery in male and female Vietnam veterans with PTSD. Arch. Gen. Psychiatry 61, 168-176. doi:10.1001/archpsyc.61.2.168
41. Shin, L. M., Shin, P. S., Heckers, S., Krangel, T. S., Macklin, M. L., Orr, S. P., et al. (2004b). Hippocampal function in posttraumatic stress disorder. Hippocampus 14, 292-300. doi:10.1002/hipo.10183
42. Siegle, G. J., Thompson, W., Carter, C. S., Steinhauer, S. R., and Thase, M. E. (2007). Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biol. Psychiatry 61, 198-209. doi:10.1016/j.biopsych.2006.05.048
43. Soufer, R., Bremner, J. D., Arrighi, J. A., Cohen, I., Zaret, B. L., Burg, M. M., et al. (1998). Cerebral cortical hyperactivation in response to mental stress in patients with coronary artery disease. Proc. Natl. Acad. Sci. U.S.A. 95, 6454-6459. doi:10.1073/pnas.95.11.6454
44. Spielberger, C. D., Gorsuch, R. L., Lushene, P. R., Vagg, P. R., and Jocobs, A. G. (1983). Manual for the Statie-Trait Anxiety Inventory (Form Y): Self-Evaluation Questionnaire. Palo Alto: Consulting Psychologists Press, Inc.
45. Stanton, S. J., Beehner, J. C., Saini, E. K., Kuhn, C. M., and Labar, K. S. (2009). Dominance, politics, and physiology: voters' testosterone changes on the night of the 2008 United States presidential election. PLoS ONE 4:e7543. doi:10.1371/journal.pone.0007543
46. Taylor, S. E., Eisenberger, N. I., Saxbe, D., Lehman, B. J., and Lieberman, M. D. (2006). Neural responses to emotional stimuli are associated with childhood family stress. Biol. Psychiatry 60, 296-301. doi:10.1016/j.biopsych.2005.09.027
47. Taylor, S. E., Lerner, J. S., Sage, R. M., Lehman, B. J., and Seeman, T. E. (2004). Early environment, emotions, responses to stress, and health. J. Pers. 72, 1365-1393. doi:10.1111/j.1467-6494.2004.00300.x
48. Taylor, S. E., Way, B. M., and Seeman, T. E. (2011). Early adversity and adult health outcomes. Dev. Psychopathol. 23, 939-954. doi:10.1017/S0954579411000411
49. Thomaes, K., Dorrepaal, E., Draijer, N., De Ruiter, M. B., Elzinga, B. M., Sjoerds, Z., et al. (2013). Increased anterior cingulate cortex and hippocampus activation in Complex PTSD during encoding of negative words. Soc. Cogn. Affect. Neurosci. 8, 190-200. doi:10.1093/scan/nsr084
50. Urry, H. L., Van Reekum, C. M., Johnstone, T., Kalin, N. H., Thurow, M. E., Schaefer, H. S., et al. (2006). Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. J. Neurosci. 26, 4415-4425. doi:10.1523/JNEUROSCI.3215-05.2006
51. Wals, M., and Verhulst, F. (2005). Child and adolescent antecedents of adult mood disorders. Curr. Opin. Psychiatry 18, 15-19.
52. Wang, J., Korczykowski, M., Rao, H., Fan, Y., Pluta, J., Gur, R. C., et al. (2007). Gender difference in neural response to psychological stress. Soc. Cogn. Affect. Neurosci. 2, 227-239. doi:10.1093/scan/nsm018
53. Wang, J., Rao, H., Wetmore, G. S., Furlan, P. M., Korczykowski, M., Dinges, D. F., et al. (2005). Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress. Proc. Natl. Acad. Sci. U.S.A. 102, 17804-17809. doi:10.1073/pnas.0503082102
54. Wang, L., Labar, K. S., Smoski, M., Rosenthal, M. Z., Dolcos, F., Lynch, T. R., et al. (2008). Prefrontal mechanisms for executive control over emotional distraction are altered in major depression. Psychiatry Res. 163, 143-155. doi:10.1016/j.pscychresns.2007.10.004
55. Ward, A., Lyubomirsky, S., Sousa, L., and Nolen-Hoeksema, S. (2003). Can't quite commit: rumination and uncertainty. Pers. Soc. Psychol. Bull. 29, 96-107. doi:10.1177/0146167202238375
56. Watson, D., Clark, L. A., and Tellegen, A. (1988). Development and validation of brief measures of positive and negative affect: the PANAS scales. J. Pers. Soc. Psychol. 54, 1063-1070. doi:10.1037/0022-3514.54.6.1063
57. Werner, N. S., Meindl, T., Engel, R. R., Rosner, R., Riedel, M., Reiser, M., et al. (2009). Hippocampal function during associative learning in patients with posttraumatic stress disorder. J. Psychiatr. Res. 43, 309-318. doi:10.1016/j.jpsychires.2008.03.011
58. Wong, E. C., Buxton, R. B., and Frank, L. R. (1998). Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSS II). Magn. Reson. Med. 39, 702-708. doi:10.1002/mrm.1910390506