Exposure to childhood trauma is associated with altered n-back activation and performance in healthy adults: implications for a commonly used working memory task

Brain Imaging and Behavior

Volumn 10, Issue 1, 2016, Pages 124-135

  Philip, Noah S ^a,b   Sweet, Lawrence H ^c   Tyrka, Audrey R ^b   Carpenter, S Louisa ^a   Albright, Sarah E ^a   Price, Lawrence H ^b   Carpenter, Linda L ^b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b BROWN UNIVERSITY   (United States)

^c University of Georgia   (United States)

Author keywords

Childhood adversity; Executive function; Functional magnetic resonance imaging; Life stress; Working memory

Indexed keywords

ACCURACY; ADULT; ARTICLE; CHILDHOOD INJURY; CHILDHOOD TRAUMA QUESTIONNAIRE; CLINICAL ARTICLE; ELECTROENCEPHALOGRAM; EMOTIONAL ABUSE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INFERIOR FRONTAL GYRUS; INFERIOR PARIETAL LOBULE; INSULA; MALE; N-BACK TEST; NEGLECT; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PARAHIPPOCAMPAL GYRUS; PHYSICAL ABUSE; PRECUNEUS; PRIORITY JOURNAL; RESPONSE TIME; SEXUAL ABUSE; SUPERIOR TEMPORAL GYRUS; TASK PERFORMANCE; WORKING MEMORY; BRAIN; BRAIN MAPPING; CHILD ABUSE SURVIVOR; GROWTH, DEVELOPMENT AND AGING; MENTAL STRESS; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; PSYCHOLOGY; SHORT TERM MEMORY;

ADULT; ADULT SURVIVORS OF CHILD ABUSE; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; NEUROPSYCHOLOGICAL TESTS; STRESS, PSYCHOLOGICAL;

EID: 84959876179     PISSN: 19317557     EISSN: 19317565     Source Type: Journal    
DOI: 10.1007/s11682-015-9373-9     Document Type: Article

References (69)

1. Abramovitch, A., Abramowitz, J. S., & Mittelman, A. (2013). The neuropsychology of adult obsessive-compulsive disorder: a meta-analysis. Clinical Psychology Review, 33, 1163–71.
2. Andrews-Hanna, J. R., Reidler, J. S., Sepulcre, J., Poulin, R., & Buckner, R. L. (2010). Functional-anatomic fractionation of the brain’s default network. Neuron, 65, 550–62.
3. Barber, A. D., Caffo, B. S., Pekar, J., Mostofsky, S. H. (2013). Developmental changes in within- and between-network connectivity between late childhood and adulthood. Neuropsychologia, 51, 156–167.
4. Baune, B. T., Czira, M. E., Smith, A. L., Mitchell, D., & Sinnamon, G. (2012). Neuropsychological performance in a sample of 13–25 year olds with a history of non-psychotic major depressive disorder. Journal of Affective Disorders, 14, 441–8.
5. Bernstein, D., & Fink, L. (1998a). Childhood trauma questionnaire: A retrospective self-report. San Antonio: Pearson Education, Inc.
6. Bernstein, D. P., & Fink, L. A. (1998b). Childhood trauma questionnaire: A retrospective self-report manual. San Antonio: The Psychological Corporation.
7. Bora, E., Yucel, M., Pantelis, C., & Berk, M. (2011). Meta-analytic review of neurocognition in bipolar II disorder. Acta Psychiatrica Scandinavica, 123, 165–74.
8. Braga, R. M., Sharp, D. J., Leeson, C., Wise, R. J., & Leech, R. (2013). Echoes of the brain within default mode, association, and heteromodal cortices. Journal of Neuroscience, 33, 14031–9.
9. Butters, M. A., Bhalla, R. K., Andreescu, C., et al. (2011). Changes in neuropsychological functioning following treatment for late-life generalised anxiety disorder. British Journal of Psychiatry, 199, 211–8.
10. Cao, H., Plichta, M. M., Schafer, A., et al. (2014). Test-retest reliability of fMRI-based graph theoretical properties during working memory, emotion processing, and resting state. NeuroImage, 84, 888–900.
11. Carrion, V. G., Haas, B. W., Garrett, A., Song, S., & Reiss, A. L. (2007). Reduced hippocampal activity in youth with posttraumatic stress symptoms: an FMRI study. Journal of Pediatric Psychology, 35, 559–69.
12. Castaneda, A. E., Suvisaari, J., Marttunen, M., et al. (2011). Cognitive functioning in a population-based sample of young adults with anxiety disorders. European Psychiatry, 26, 346–53.
13. Charlet, K., Beck, A., Jorde, A., et al. (2013). Increased neural activity during high working memory load predicts low relapse risk in alcohol dependence. Addiction Biology, 19, 402–14.
14. Cohen, S., Kamarck, T., & Mermelstein, R. (1983). A global measure of perceived stress. Journal of Health and Social Behavior, 24, 385–96.
15. Conrad, C. D., McLaughlin, K. J., Harman, J. S., et al. (2007). Chronic glucocorticoids increase hippocampal vulnerability to neurotoxicity under conditions that produce CA3 dendritic retraction but fail to impair spatial recognition memory. Journal of Neuroscience, 27, 8278–85.
16. Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–73.
17. Cromheeke, S., Herpoel, L. A., & Mueller, S. C. (2013). Childhood abuse is related to working memory impairment for positive emotion in female university students. Child Maltreatment, 19, 38–48.
18. Daniels, J. K., McFarlane, A. C., Bluhm, R. L., et al. (2010). Switching between executive and default mode networks in posttraumatic stress disorder: alterations in functional connectivity. Journal of Psychiatry and Neuroscience, 35, 258–66.
19. Eich, T. S., Nee, D. E., Insel, C., Malapani, C., & Smith, E. E. (2013). Neural correlates of impaired cognitive control over working memory in schizophrenia. Biological Psychiatry, 76, 146–53.
20. Evans, G. W., & Schamberg, M. A. (2009). Childhood poverty, chronic stress, and adult working memory. Proceedings of the National Academy of Sciences of the United States of America, 106, 6545–9.
21. Fernandez-Corcuera, P., Salvador, R., Monte, G. C., et al. (2013). Bipolar depressed patients show both failure to activate and failure to de-activate during performance of a working memory task. Journal of Affective Disorders, 148, 170–8.
22. First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (1994). Structural clinical interview for Axis I DSM-IV disorders: Biometrics research department. New York: New York State Psychiatric Institute.
23. Fuge, P., Aust, S., Fan, Y., Weigand, A., Gärtner, M., Feeser, M., Bajbouj, M., & Grimm, S. (2014). Interaction of early life stress and corticotropin-releasing hormone receptor gene: effects on working memory. Biological Psychiatry, 76(11), 888–94. doi:10.1016/j.biopsych.2014.04.016. Epub 2014 May 14.
24. Gould, F., Clarke, J., Heim, C., Harvey, P. D., Majer, M., & Nemeroff, C. B. (2012). The effects of child abuse and neglect on cognitive functioning in adulthood. Journal of Psychiatric Research, 46, 500–6.
25. Green, J. G., McLaughlin, K. A., Berglund, P. A., et al. (2010). Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: associations with first onset of DSM-IV disorders. Archives of General Psychiatry, 67, 113–23.
26. Hanson, J. L., Chung, M. K., Avants, B. B., et al. (2012). Structural variations in prefrontal cortex mediate the relationship between early childhood stress and spatial working memory. Journal of Neuroscience, 32, 7917–25.
27. Hart, H., & Rubia, K. (2012). Neuroimaging of child abuse: a critical review. Frontiers in Human Neuroscience, 6, 52.
28. Harvey, P. O., Le Bastard, G., Pochon, J. B., et al. (2004). Executive functions and updating of the contents of working memory in unipolar depression. Journal of Psychiatric Research, 38, 567–76.
29. Koso, M., & Hansen, S. (2006). Executive function and memory in posttraumatic stress disorder: a study of Bosnian war veterans. European Psychiatry, 21, 167–73.
30. Lagarde, G., Doyon, J., & Brunet, A. (2010). Memory and executive dysfunctions associated with acute posttraumatic stress disorder. Psychiatry Research, 177, 144–9.
31. Lansford, J. E., Dodge, K. A., Pettit, G. S., Bates, J. E., Crozier, J., & Kaplow, J. (2002). A 12-year prospective study of the long-term effects of early child physical maltreatment on psychological, behavioral, and academic problems in adolescence. Archives of Pediatrics and Adolescent Medicine, 156, 824–30.
32. Majer, M., Nater, U. M., Lin, J. M., Capuron, L., & Reeves, W. C. (2010). Association of childhood trauma with cognitive function in healthy adults: a pilot study. BMC Neurology, 10, 61.
33. Mayer, J. S., & Park, S. (2012). Working memory encoding and false memory in schizophrenia and bipolar disorder in a spatial delayed response task. Journal of Abnormal Psychology, 121, 784–94.
34. McCrory, E., De Brito, S. A., & Viding, E. (2011). The impact of childhood maltreatment: a review of neurobiological and genetic factors. Frontiers Psychiatry, 2, 48.
35. Moores, K. A., Clark, C. R., McFarlane, A. C., Brown, G. C., Puce, A., & Taylor, D. J. (2008). Abnormal recruitment of working memory updating networks during maintenance of trauma-neutral information in post-traumatic stress disorder. Psychiatry Research, 163, 156–70.
36. Nardo, D., Hogberg, G., Lanius, R. A., et al. (2013). Gray matter volume alterations related to trait dissociation in PTSD and traumatized controls. Acta Psychiatrica Scandinavica, 128, 222–33.
37. Owen, A. M., McMillan, K. M., Laird, A. R., & Bullmore, E. (2005). N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Human Brain Mapping, 25, 46–59.
38. Pardo, J. V., Fox, P. T., & Raichle, M. E. (1991). Localization of a human system for sustained attention by positron emission tomography. Nature, 349, 61–4.
39. Patel, N. V., & Finch, C. E. (2002). The glucocorticoid paradox of caloric restriction in slowing brain aging. Neurobiology of Aging, 23, 707–17.
40. Pechtel, P., & Pizzagalli, D. A. (2011). Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology, 214, 55–70.
41. Perna, R. B., & Kiefner, M. (2012). Long-term cognitive sequelae: abused children without PTSD. Applied Neuropsychology Child, 2, 1–5.
42. Petersen, S. E., Fox, P. T., Posner, M. I., Mintun, M., & Raichle, M. E. (1988). Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature, 331, 585–9.
43. Philip, N. S., Sweet, L. H., Tyrka, A. R., et al. (2013a). Early life stress is associated with greater default network deactivation during working memory in healthy controls: a preliminary report. Brain Imaging and Behavior, 7, 204–12.
44. Philip, N. S., Sweet, L. H., Tyrka, A. R., Price, L. H., Bloom, R. F., & Carpenter, L. L. (2013b). Decreased default network connectivity is associated with early life stress in medication-free healthy adults. European Neuropsychopharmacology, 23, 24–32.
45. Philip, N. S., Carpenter, S. L., & Sweet, L. H. (2014a). Developing neuroimaging phenotypes of the default mode network in PTSD: integrating the resting state, working memory, and structural connectivity. Journal of Visualized Experiments, 89, 51651. doi:10.3791/51651.
46. Philip, N. S., Valentine, T. R., Sweet, L. H., Tyrka, A. R., Price, L. H., & Carpenter, L. L. (2014b). Early life stress impacts dorsolateral prefrontal cortex functional connectivity in healthy adults: Informing future studies of antidepressant treatments. Journal of Psychiatric Research, 52, 63–9.
47. Plamondon, A., Akbari, E., Atkinson, L., Steiner, M., Meaney, M. J., & Fleming, A. S. (2015). MAVAN research team. Spatial working memory and attention skills are predicted by maternal stress during pregnancy. Early Human Development, 91(1), 23–9. doi:10.1016/j.earlhumdev.2014.11.004. Epub 2014 Nov 26.
48. Posner, M. I., Petersen, S. E., Fox, P. T., & Raichle, M. E. (1988). Localization of cognitive operations in the human brain. Science, 240, 1627–31.
49. Raine, A., Park, S., Lencz, T., et al. (2001). Reduced right hemisphere activation in severely abused violent offenders during a working memory task: an fMRI study. Aggressive Behavior, 27, 111–29.
50. Roopesh, B. N., Janardhan Reddy, Y. C., & Mukundan, C. R. (2013). Neuropsychological deficits in drug naive, non-depressed obsessive-compulsive disorder patients. Asian Journal Psychiatry, 6, 162–70.
51. Rush, A. J., et al. (2003). The 16-Item Quick Inventory of Depressive Symptomatology (QIDS), clinician rating (QIDS-C), and self-report (QIDS-SR): a psychometric evaluation in patients with chronic major depression. Biological Psychiatry, 54, 573–83.
52. Satterthwaite, T. D., Wolf, D. H., Erus, G., et al. (2013). Functional maturation of the executive system during adolescence. Journal of Neuroscience, 33, 16249–61.
53. Schuitevoerder, S., Rosen, J. W., Twamley, E. W., et al. (2013). A meta-analysis of cognitive functioning in older adults with PTSD. Journal of Anxiety Disorders, 27, 550–8.
54. Shonkoff, J. P., & Garner, A. S. (2012). The lifelong effects of early childhood adversity and toxic stress. Pediatrics, 129, e232–46.
55. Silver, H., Feldman, P., Bilker, W., & Gur, R. C. (2003). Working memory deficit as a core neuropsychological dysfunction in schizophrenia. The American Journal of Psychiatry, 160, 1809–16.
56. Spielberg, C. D., Gorsuch, R. L., & Lushene, R. E. (1983). Manual for the state-trait anxiety inventory consulting. Palo Alto: Consulting Psychologists Press.
57. Sutherland MT, Ross TJ, Shakleya DM, Huestis MA, Stein EA. (2011). Chronic smoking, but not acute nicotine administration, modulates neural correlates of working memory. Psychopharmacology (Berl), 213(1), 29–42.
58. Sweet, L. H., Rao, S. M., Primeau, M., Mayer, A. R., & Cohen, R. A. (2004). Functional magnetic resonance imaging of working memory among multiple sclerosis patients. Journal of Neuroimaging, 14, 150–7.
59. Sweet, L. H., Rao, S. M., Primeau, M., Durgerian, S., & Cohen, R. A. (2006). Functional magnetic resonance imaging response to increased verbal working memory demands among patients with multiple sclerosis. Human Brain Mapping, 27, 28–36.
60. Sweet, L. H., Paskavitz, J. F., Haley, A. P., et al. (2008). Imaging phonological similarity effects on verbal working memory. Neuropsychologia, 46, 1114–23.
61. Sweet, L. H., Mulligan, R. C., Finnerty, C. E., Jerskey, B. A., David, S. P., Cohen, R. A., & Niaura, R. S. (2010). Effects of nicotine withdrawal on verbal working memory and associated brain response. Psychiatry Research, 183, 69–74.
62. Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional system: An approach to cerebral imaging. Stuggart: Thieme Medical Publishers, Inc.
63. Teicher, M. H., & Samson, J. A. (2013). Childhood maltreatment and psychopathology: a case for ecophenotypic variants as clinically and neurobiologically distinct subtypes. The American Journal of Psychiatry, 170, 1114–33.
64. Teicher, M. H., Tomoda, A., & Andersen, S. L. (2006). Neurobiological consequences of early stress and childhood maltreatment: are results from human and animal studies comparable? Annals of the New York Academy of Sciences, 1071, 313–23.
65. Tek, C., Gold, J., Blaxton, T., Wilk, C., McMahon, R. P., & Buchanan, R. W. (2013). Visual perceptual and working memory impairments in schizophrenia. Archives of General Psychiatry, 59, 146–53.
66. Tyrka, A. R., Burgers, D. E., Philip, N. S., Price, L. H., & Carpenter, L. L. (2013). The neurobiological correlates of childhood adversity and implications for treatment. Acta Psychiatrica Scandinavica, 128, 434–47.
67. Vasterling, J. J., Duke, L. M., Brailey, K., Constans, J. I., Allain, A. N., Jr., & Sutker, P. B. (2002). Attention, learning, and memory performances and intellectual resources in Vietnam veterans: PTSD and no disorder comparisons. Neuropsychology, 16, 5–14.
68. Vythilingam, M., Heim, C., Newport, J., et al. (2002). Childhood trauma associated with smaller hippocampal volume in women with major depression. The American Journal of Psychiatry, 159, 2072–80.
69. Zhang, J. N., Xiong, K. L., Qiu, M. G., et al. (2013). Negative emotional distraction on neural circuits for working memory in patients with posttraumatic stress disorder. Brain Research, 1531, 94–101.