Childhood poverty predicts adult amygdala and frontal activity and connectivity in response to emotional faces

Frontiers in Behavioral Neuroscience

Volumn 9, Issue June, 2015, Pages

  Javanbakht, Arash ^a   King, Anthony P ^a,b   Evans, Gary W ^c   Swain, James E ^a   Angstadt, Michael ^a   Luan Phan, K ^d,e   Liberzon, Israel ^a,b  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

^c Department of Obstetrics Gynecology   (United States)

^d UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^e JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

Amygdala; Emotion; Emotional faces; Neurocircuitry; Poverty

Indexed keywords

ADULT; ADULTHOOD; AMYGDALOID NUCLEUS; ARTICLE; ASSESSMENT OF HUMANS; BRAIN DEVELOPMENT; BRAIN FUNCTION; CHILDHOOD; CONTROLLED STUDY; EMOTION; EMOTIONAL BIAS; EMOTIONAL FACES ASSESSMENT TASK; ENVIRONMENTAL FACTOR; FACE; FEMALE; HAPPINESS; HEALTH STATUS; HUMAN; HUMAN EXPERIMENT; LONGITUDINAL STUDY; MALADJUSTMENT; MALE; MEDIAL PREFRONTAL CORTEX; NEUROIMAGING; NORMAL HUMAN; POVERTY; PREDICTION; PROSPECTIVE STUDY; SOCIAL ASPECT; STIMULUS RESPONSE; THREAT; VISUAL STIMULATION;

EID: 84935849510     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2015.00154     Document Type: Article

References (55)

1. Adler, N. E., and Rehkopf, D. H. (2008). U.S. disparities in health: descriptions, causes, and mechanisms. Annu. Rev. Public Health 29, 235–252. doi:10.1146/annurev.publhealth.29.020907.090852
2. Beard, C., Sawyer, A. T., and Hofmann, S. G. (2012). Efficacy of attention bias modification using threat and appetitive stimuli: a meta-analytic review. Behav. Ther. 43, 724–740. doi:10.1016/j.beth.2012.01.002
3. Birnie, K., Cooper, R., Martin, R. M., Kuh, D., Sayer, A. A., Alvarado, B. E., et al. (2011). Childhood socioeconomic position and objectively measured physical capability levels in adulthood: a systematic review and meta-analysis. PLoS ONE 6:e15564. doi:10.1371/journal.pone.0015564
4. Britton, J. C., Taylor, S. F., Sudheimer, K. D., and Liberzon, I. (2006). Facial expressions and complex IAPS pictures: common and differential networks. Neuroimage 31, 906–919. doi:10.1016/j.neuroimage.2005.12.050
5. Brown, J., Barbarin, O., and Scott, K. (2013). Socioemotional trajectories in black boys between kindergarten and the fifth grade: the role of cognitive skills and family in promoting resiliency. Am. J. Orthopsychiatry 83(2 Pt 3), 176–184. doi:10.1111/ajop.12027
6. Carsey Institute. (2013). 2012 National Child Poverty Rate Stagnates at 22.6 Percent. Durham, NH: Carsey Institute, University of New Hampshire. National Issue Brief #65.
7. Chen, E., Langer, D. A., Raphaelson, Y. E., and Matthews, K. A. (2004). Socioeconomic status and health in adolescents: the role of stress interpretations. Child Dev. 75, 1039–1052. doi:10.1111/j.1467-8624.2004.00724.x
8. Chen, E., and Matthews, K. A. (2001). Cognitive appraisal biases: an approach to understanding the relation between socioeconomic status and cardiovascular reactivity in children. Ann. Behav. Med. 23, 101–111. doi:10.1207/S15324796ABM2302_4
9. Cohen, R. A., Grieve, S., Hoth, K. F., Paul, R. H., Sweet, L., Tate, D., et al. (2006). Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biol. Psychiatry 59, 975–982. doi:10.1016/j.biopsych.2005.12.016
10. Cohen, S., Janicki-Deverts, D., Chen, E., and Matthews, K. A. (2010). Childhood socioeconomic status and adult health. Ann. N.Y. Acad. Sci. 1186, 37–55. doi:10.1111/j.1749-6632.2009.05334.x
11. Davis, M., and Whalen, P. J. (2001). The amygdala: vigilance and emotion. Mol. Psychiatry 6, 13–34. doi:10.1038/sj.mp.4000812
12. Etkin, A., Egner, T., Peraza, D. M., Kandel, E. R., and Hirsch, J. (2006). Resolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron 51, 871–882. doi:10.1016/j.neuron.2006.07.029
13. Etkin, A., Prater, K. E., Hoeft, F., Menon, V., and Schatzberg, A. F. (2010). Failure of anterior cingulate activation and connectivity with the amygdala during implicit regulation of emotional processing in generalized anxiety disorder. Am. J. Psychiatry 167, 545–554. doi:10.1176/appi.ajp.2009.09070931
14. Etkin, A., and Wager, T. D. (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am. J. Psychiatry 164, 1476–1488. doi:10.1176/appi.ajp.2007.07030504
15. Evans, G. W. (2003). A multimethodological analysis of cumulative risk and allostatic load among rural children. Dev. Psychol. 39, 924–933. doi:10.1037/0012-1649.39.5.924
16. Evans, G. W. (2004). The environment of childhood poverty. Am. Psychol. 59, 77–92. doi:10.1037/0003-066X.59.2.77
17. Evans, G. W., and Schamberg, M. (2009). Childhood poverty, chronic stress, and adult working memory. Proc. Natl. Acad. Sci. U.S.A.106, 6545–6549. doi:10.1073/pnas.0811910106
18. Fusar-Poli, P., Placentino, A., Carletti, F., Landi, P., Allen, P., Surguladze, S., et al. (2009). Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J. Psychiatry Neurosci. 34, 418–432.
19. Gianaros, P. J., Horenstein, J. A., Cohen, S., Matthews, K. A., Brown, S. M., Flory, J. D., et al. (2007). Perigenual anterior cingulate morphology covaries with perceived social standing. Soc. Cogn. Affect. Neurosci. 2, 161–173. doi:10.1093/scan/nsm013
20. Gianaros, P. J., Horenstein, J. A., Hariri, A. R., Sheu, L. K., Manuck, S. B., Matthews, K. A., et al. (2008). Potential neural embedding of parental social standing. Soc. Cogn. Affect. Neurosci. 3, 91–96. doi:10.1093/scan/nsn003
21. Gur, R. C., Sara, R., Hagendoorn, M., Marom, O., Hughett, P., Macy, L., et al. (2002). A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies. J. Neurosci. Methods 115, 137–143. doi:10.1016/S0165-0270(02)00006-7
22. Hanson, J. L., Nacewicz, B. M., Sutterer, M. J., Cayo, A. A., Schaefer, S. M., Rudolph, K. D., et al. (2015). Behavioral problems after early life stress: contributions of the hippocampus and amygdala. Biol. Psychiatry 77, 314–323. doi:10.1016/j.biopsych.2014.04.020
23. Hariri, A. R., Tessitore, A., Mattay, V. S., Fera, F., and Weinberger, D. R. (2002). The amygdala response to emotional stimuli: a comparison of faces and scenes. Neuroimage 17, 317–323. doi:10.1006/nimg.2002.1179
24. Herman, J. P., Prewitt, C. M. F., and Cullinan, W. E. (1996). Neuronal circuit regulation of the hypothalamo-pituitary-adrenocortical stress axis. Crit. Rev. Neurobiol. 10, 371–394. doi:10.1615/CritRevNeurobiol.v10.i3-4.50
25. Kalisch, R. (2009). The functional neuroanatomy of reappraisal: time matters. Neurosci. Biobehav. Rev. 33, 1215–1226. doi:10.1016/j.neubiorev.2009.06.003
26. Kelley, W. M., Macrae, C. N., Wyland, C. L., Caglar, S., Inati, S., and Heatherton, T. F. (2002). Finding the self? An event-related fMRI study. J. Cogn. Neurosci. 14, 785–794. doi:10.1162/08989290260138672
27. Kessler, R. C., Duncan, G. J., Gennetian, L. A., Katz, L. F., Kling, J. R., Sampson, N. A., et al. (2014). Associations of housing mobility interventions for children in high-poverty neighborhoods with subsequent mental disorders during adolescence. JAMA 311, 937–948. doi:10.1001/jama.2014.607
28. Kim, H., Somerville, L. H., Johnstone, T., Polis, S., Alexander, A. L., Shin, L. M., et al. (2004). Contextual modulation of amygdala responsivity to surprised faces. J. Cogn. Neurosci. 16, 1730–1745. doi:10.1162/0898929042947865
29. Kim, P., Evans, G. W., Angstadt, M., Ho, S. S., Sripada, C. S., Swain, J. E., et al. (2013). Effects of childhood poverty and chronic stress on emotion regulatory brain function in adulthood. Proc. Natl. Acad. Sci. U.S.A. 110, 18442–18447. doi:10.1073/pnas.1308240110
30. Knigge, K. (1961). Adrenocortical response to stress in rats with lesions in hippocampus and amygdala. Proc. Soc. Exp. Biol. Med. 180, 18–20. doi:10.3181/00379727-108-26832
31. Lee, K. H., and Siegle, G. J. (2014). Different brain activity in response to emotional faces alone and augmented by contextual information. Psychophysiology 51, 1147–1157. doi:10.1111/psyp.12254
32. Luby, J., Belden, A., Botteron, K., Marrus, N., Harms, M. P., Babb, C., et al. (2013). The effects of poverty on childhood brain development: the mediating effect of caregiving and stressful life events. JAMA Pediatr. 167, 1135–1142. doi:10.1001/jamapediatrics.2013.3139
33. Mayberg, H. S. (1997). Limbic-cortical dysregulation: a proposed model of depression. J. Neuropsychiatry Clin. Neurosci. 9, 471–481. doi:10.1176/jnp.9.3.471
34. McLaren, D. G., Ries, M. L., Xu, G., and Johnson, S. C. (2012). A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. Neuroimage 61, 1277–1286. doi:10.1016/j.neuroimage.2012.03.068
35. Milad, M. R., and Quirk, G. J. (2012). Fear extinction as a model for translational neuroscience: ten years of progress. Annu. Rev. Psychol. 63, 129–151. doi:10.1146/annurev.psych.121208.131631
36. Mobbs, D., Weiskopf, N., Lau, H. C., Featherstone, E., Dolan, R. J., and Frith, C. D. (2006). The Kuleshov effect: the influence of contextual framing on emotional attributions. Soc. Cogn. Affect. Neurosci. 1, 95–106. doi:10.1093/scan/nsl014
37. Moore, W. E. III, Merchant, J. S., Kahn, L. E., and Pfeifer, J. H. (2014). Like me?: ventromedial prefrontal cortex is sensitive to both personal relevance and self-similarity during social comparisons. Soc. Cogn. Affect. Neurosci. 9, 421–426. doi:10.1093/scan/nst007
38. Muscatell, K. A., Morelli, S. A., Falk, E. B., Way, B. M., Pfeifer, J. H., Galinsky, A. D., et al. (2012). Social status modulates neural activity in the mentalizing network. Neuroimage 60, 1771–1777. doi:10.1016/j.neuroimage.2012.01.080
39. Noble, K. G., Houston, S. M., Kan, E., and Sowell, E. R. (2012). Neural correlates of socioeconomic status in the developing human brain.Dev. Sci. 15, 516–527. doi:10.1111/j.1467-7687.2012.01147.x
40. Ochsner, K. N., Silvers, J. A., and Buhle, J. T. (2012). Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion. Ann. N. Y. Acad. Sci. 1251, E1–E24. doi:10.1111/j.1749-6632.2012.06751.x
41. Phan, K. L., Angstadt, M., Golden, J., Onyewuenyi, I., Popovska, A., and de Wit, H. (2008). Cannabinoid modulation of amygdala reactivity to social signals of threat in humans. J. Neurosi. 28, 2313–2319. doi:10.1523/JNEUROSCI.5603-07.2008
42. Phan, K. L., Coccaro, E. F., Angstadt, M., Kreger, K. J., Mayberg, H. S., Liberzon, I., et al. (2013). Corticolimbic brain reactivity to social signals of threat before and after sertraline treatment in generalized social phobia. Biol. Psychiatry 73, 329–336. doi:10.1016/j.biopsych.2012.10.003
43. Phan, K. L., Wager, T. D., Taylor, S. F., and Liberzon, I. (2004). Functional neuroimaging studies of human emotions. CNS Spectr. 9, 258–266.
44. Phelps, E. A., and LeDoux, J. E. (2005). Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48, 175–187. doi:10.1016/j.neuron.2005.09.025
45. Poulton, R., Caspi, A., Milne, B. J., Thomson, W. M., Taylor, A., Sears, M. R., et al. (2002). Association between children’s experience of socioeconomic disadvantage and adult health: a life-course study. Lancet 360, 1640–1645. doi:10.1016/S0140-6736(02)11602-3
46. Prater, K. E., Hosanagar, A., Klumpp, H., Angstadt, M., and Phan, K. L. (2013). Aberrant amygdala-frontal cortex connectivity during perception of fearful faces and at rest in generalized social anxiety disorder. Depress. Anxiety 30, 234–241. doi:10.1002/da.22014
47. Rodrigues, S. M., LeDoux, J. E., and Sapolsky, R. M. (2009). The influence of stress hormones on fear circuitry. Annu. Rev. Neurosci. 32, 289–313. doi:10.1146/annurev.neuro.051508.135620
48. Sauder, C. L., Hajcak, G., Angstadt, M., and Phan, K. L. (2013). Test-retest reliability of amygdala response to emotional faces. Psychophysiology 50, 1147–1156. doi:10.1111/psyp.12129
49. Shechner, T., Britton, J. C., Pérez-Edgar, K., Bar-Haim, Y., Ernst, M., Fox, N. A., et al. (2012). Attention biases, anxiety, and development: toward or away from threats or rewards. Depress. Anxiety 29, 282–294. doi:10.1002/da.20914
50. Shin, L. M., and Liberzon, I. (2010). The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35, 169–191. doi:10.1038/npp.2009.83
51. Shonkoff, J. P., Boyce, W. T., and McEwen, B. S. (2009). Neuroscience, molecular biology, and the childhood roots of health disparities: building a new framework for health promotion and disease prevention. JAMA 301, 2252–2259. doi:10.1001/jama.2009.754
52. Silverman, M. E., Muennig, P., Liu, X., Rosen, Z., and Goldstein, M. A. (2009). The impact of socioeconomic status on the neural substrates associated with pleasure. Open Neuroimag. J. 3, 58–63. doi:10.2174/1874440000903010058
53. Wadsworth, M. E., Evans, G. W., Grant, K., Carter, J. S., and Duffy, S. (Forthcoming). “Poverty and the development of psychopathology,” in Developmental Psychopathology, ed. D. Cicchetti (New York, NY: Wiley).
54. Wager, T. D., Davidson, M. L., Hughes, B. L., Lindquist, M. A., and Ochsner, K. N. (2008). Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron 59, 1037–1050. doi:10.1016/j.neuron.2008.09.006
55. Whalen, P. J., Shin, L. M., McInerney, S. C., Fischer, H., Wright, C. I., and Rauch, S. L. (2001). A functional MRI study of human amygdala responses to facial expressions of fear versus anger. Emotion 1, 70–83. doi:10.1037/1528-3542.1.1.70