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Early-life adversity and adolescent depression: mechanisms involving the ventral striatum

Published online by Cambridge University Press:  16 December 2014

Bonnie Goff  and
Nim Tottenham
Bonnie Goff
Affiliation:
Department of Psychology, The University of California–Los Angeles, Los Angeles, California, USA
Nim Tottenham*
Affiliation:
Department of Psychology, Columbia University, New York, New York, USA
*
*Address for correspondence: Nim Tottenham, Columbia University, Psychology Dept., 406 Schermerhorn Hall, 1190 Amsterdam Avenue MC 5501, New York, NY 10027, USA. (Email: [email protected])
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Abstract

Early-life adversity is a well-established risk factor for the development of depression later in life. Here we discuss the relationship between early-life adversity and depression, focusing specifically on effects of early-life caregiver deprivation on alterations in the neural and behavioral substrates of reward-processing. We also examine vulnerability to depression within the context of sensitive periods of neural development and the timing of adverse exposure. We further review the development of the ventral striatum, a limbic structure implicated in reward processing, and its role in depressive outcomes following early-life adversity. Finally, we suggest a potential neurobiological mechanism linking early-life adversity and altered ventral striatal development. Together these findings may help provide further insight into the role of reward circuitry dysfunction in psychopathological outcomes in both clinical and developmental populations.

Keywords

adolescencecaregiver deprivationdepressionearly-life adversityventral striatum
Type
Review Articles
Information
CNS Spectrums , Volume 20 , Special Issue 4: Pediatric Neuroimaging , August 2015 , pp. 337 - 345
Copyright
© Cambridge University Press 2014 

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Footnotes

This work was supported by NIMH R01MH091864 (NT) and The Dana Foundation.

References

1. Gunnar, M, Quevedo, K. The neurobiology of stress and development. Annu Rev Psychol. 2007; 58: 145–173.CrossRefGoogle ScholarPubMed
2. Kendler, K. Toward a comprehensive developmental model for major depression in women. Am J Psychiatry. 2002; 159(7): 1133–1145.CrossRefGoogle Scholar
3. Maier, W. Genetic epidemiology of psychiatric disorders. Eur Arch Psychiatry Clin Neurosci. 1993; 243(3–4): 119–120.CrossRefGoogle ScholarPubMed
4. Nestler, EJ, Barrot, M, DiLeone, RJ, Eisch, AJ, Gold, SJ, Monteggia, LM. Neurobiology of depression. Neuron. 2002; 34(1): 13–25.CrossRefGoogle ScholarPubMed
5. Heim, C, Shugart, M, Craighead, WE, Nemeroff, CB. Neurobiological and psychiatric consequences of child abuse and neglect. Dev Psychobiol. 2010; 52(7): 671–690.CrossRefGoogle ScholarPubMed
6. Child Welfare Information Gateway. Determining the best interests of the child. Washington, DC: Child Welfare Information Gateway; 2012. Available at: https://www.childwelfare.gov/systemwide/laws_policies/statutes/best_interest.pdf.Google Scholar
7. Cornell University, College of Human Ecology. National Data Archive on Child Abuse and Neglect. http://www.ndacan.cornell.edu.Google Scholar
8. Maercker, A, Michael, T, Fehm, L, Becker, ES, Margraf, J. Age of traumatisation as a predictor of post-traumatic stress disorder or major depression in young women. Br J Psychiatry. 2004; 184(6): 482–487.Google ScholarPubMed
9. Chapman, DP, Whitfield, CL, Felitti, VJ, Dube, SR, Edwards, VJ, Anda, RF. Adverse childhood experiences and the risk of depressive disorders in adulthood. J Affect Disord. 2004; 82(2): 217–225.CrossRefGoogle ScholarPubMed
10. Brown, J, Cohen, P, Johnson, JG, Smailes, EM. Childhood abuse and neglect: specificity of effects on adolescent and young adult depression and suicidality. J Am Acad Child Adolesc Psychiatry. 1999; 38(12): 1490–1496.CrossRefGoogle Scholar
11. McCauley, J, Kern, DE, Kolodner, K, et al. Clinical characteristics of women with a history of childhood abuse: unhealed wounds. JAMA. 1997; 277(17): 1362–1368.Google ScholarPubMed
12. Mullen, PE, Martin, JL, Anderson, JC, Romans, SE, Herbison, GP. The long-term impact of the physical, emotional, and sexual abuse of children: a community study. Child Abuse Negl. 1996; 20(1): 7–21.Google ScholarPubMed
13. Heim, C, Nemeroff, CB. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry. 2001; 49(12): 1023–1039.Google ScholarPubMed
14. Agid, O, Shapira, B, Zislin, J, et al. Environment and vulnerability to major psychiatric illness: a case control study of early parental loss in major depression, bipolar disorder and schizophrenia. Mol Psychiatry. 1999; 4(2): 163–172.Google Scholar
15. Francis, DD, Caldji, C, Champagne, F, Plotsky, PM, Meaney, MJ. The role of corticotropin-releasing factor–norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress. Biol Psychiatry. 1999; 46(9): 1153–1166.CrossRefGoogle ScholarPubMed
16. Kendler, KS, Neale, MC, Kessler, RC, Heath a, C, Eaves, LJ. A population-based twin study of major depression in women: the impact of varying definitions of illness. Arch Gen Psychiatry. 1992; 49(4): 257–266.CrossRefGoogle ScholarPubMed
17. Romanov, K, Varjonen, J, Kaprio, J, Koskenvuo, M. Life events and depressiveness—the effect of adjustment for psychosocial factors, somatic health and genetic liability. Acta Psychiatr Scand. 2003; 107(1): 25–33.CrossRefGoogle ScholarPubMed
18. Edwards, VJ, Holden, GW, Felitti, VJ, Anda, RF. Relationship between multiple forms of childhood maltreatment and adult mental health in community respondents: results from the adverse childhood experiences study. Am J Psychiatry. 2003; 160(8): 1453–1460.CrossRefGoogle ScholarPubMed
19. Felitti, VJ, Anda, RF, Nordenberg, D, et al. Household dysfunction to many of the leading causes of death in adults: the Adverse Childhood Experiences (ACE) study. Am J Prev Med. 1998; 14(4): 245–258.CrossRefGoogle ScholarPubMed
20. Kendler, KS, Karkowski, LM, Prescott, CA. Causal relationship between stressful life events and the onset of major depression. Am J Psychiatry. 1999; 156(6): 837–841.CrossRefGoogle ScholarPubMed
21. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed., text rev. Washington, DC: American Psychiatric Association; 2000.Google Scholar
22. Insel, T, Cuthbert, B, Garvey, M, et al. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am J Psychiatry. 2010; 167(7): 748–751.CrossRefGoogle Scholar
23. Chiu, PH, Deldin, PJ. Neural evidence for enhanced error detection in major depressive disorder. Am J Psychiatry. 2007; 164(4): 608–616.Google ScholarPubMed
24. Loas, G, Boyer, P. Anhedonia in endogenomorphic depression. Psychiatry Res. 1996; 60(1): 57–65.CrossRefGoogle Scholar
25. Snaith, P. Anhedonia: a neglected symptom of psychopathology. Psychol Med. 1993; 23(4): 957–966.Google ScholarPubMed
26. Cicchetti, D, Toth, SL. Child maltreatment. Annu Rev Clin Psychol. 2005; 1: 409–438.CrossRefGoogle ScholarPubMed
27. Gunnar, MR. Integrating neuroscience and psychological approaches in the study of early experiences. Ann N Y Acad Sci. 2003; 1008: 238–247.CrossRefGoogle Scholar
28. Heim, C, Bradley, B, Mletzko, TC, et al. Effect of childhood trauma on adult depression and neuroendocrine function: sex-specific moderation by CRH receptor 1 gene. Front Behav Neurosci. 2009; 3: 41.Google ScholarPubMed
29. Stovall-McClough, KC, Cloitre, M. Unresolved attachment, PTSD, and dissociation in women with childhood abuse histories. J Consult Clin Psychol. 2006; 74(2): 219–228.CrossRefGoogle ScholarPubMed
30. Teicher, MH, Andersen, SL, Polcari, A, Anderson, CM, Navalta, CP, Kim, DM. The neurobiological consequences of early stress and childhood maltreatment. Neurosci Biobehav Rev. 2003; 27(1–2): 33–44.CrossRefGoogle ScholarPubMed
31. Letcher, P, Smart, D, Sanson, A, Toumbourou, JW. Psychosocial precursors and correlates of differing internalizing trajectories from 3 to 15 years. Social Development. 2009; 18(3): 618–646.Google Scholar
32. Mason, WA, Kosterman, R, Hawkins, JD, Herrenkohl, TI, Lengua, LJ, McCauley, E. Predicting depression, social phobia, and violence in early adulthood from childhood behavior problems. J Am Acad Child Adolesc Psychiatry. 2004; 43(3): 307–315.CrossRefGoogle ScholarPubMed
33. Mazza, JJ, Abbott, RD, Fleming, CB, et al. Early predictors of adolescent depression: a 7-year longitudinal study. Journal of Early Adolescence. 2009; 29(5): 664–692.CrossRefGoogle Scholar
34. Teicher, MH, Tomoda, A, Andersen, SE. Neurobiological consequences of early stress and childhood maltreatment: are results from human and animal studies comparable? Ann N Y Acad Sci. 2006; 1071: 313–323.CrossRefGoogle ScholarPubMed
35. Kaufman, J, Plotsky, PM, Nemeroff, CB, Charney, DS. Effects of early adverse experiences on brain structure and function: clinical implications. Biol Psychiatry. 2000; 48(8): 778–790.Google ScholarPubMed
36. Rice, D, Barone, S. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect. 2000; 108(Suppl 3): 511–533.Google ScholarPubMed
37. Andersen, SL, Tomada, A, Vincow, ES, Valente, E, Polcari, A, Teicher, MH. Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. J Neuropsychiatry Clin Neurosci. 2008; 20(3): 292–301.CrossRefGoogle ScholarPubMed
38. Weiss, MJS, Wagner, SH. What explains the negative consequences of adverse childhood experiences on adult health? Insights from cognitive and neuroscience research. Am J Prev Med. 1998; 14(4): 356–360.Google ScholarPubMed
39. Gunnar, MR, Fisher, PA. Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children. Dev Psychopathol. 2006; 18(3): 651–677.CrossRefGoogle ScholarPubMed
40. McEwen, BS. The neurobiology of stress: from serendipity to clinical relevance. Brain Res. 2000; 886(1–2): 172–189.CrossRefGoogle ScholarPubMed
41. Loman, MM, Gunnar, MR, Early Experience, Stress, and Neurobehavioral Development Center. Early experience and the development of stress reactivity and regulation in children. Neurosci Biobehav Rev. 2010; 34(6): 867–876.CrossRefGoogle ScholarPubMed
42. Heim, C, Newport, DJ, Mletzko, T, Miller, AH, Nemeroff, CB. The link between childhood trauma and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology. 2008; 33(6): 693–710.CrossRefGoogle ScholarPubMed
43. Gold, PW, Gabry, KE, Yasuda, MR, Chrousos, GP. Divergent endocrine abnormalities in melancholic and atypical depression: clinical and pathophysiologic implications. Endocrinol Metab Clin North Am. 2002; 31(1): 37–62.Google ScholarPubMed
44. Gold, PW, Chrousos, GP. The endocrinology of melancholic and atypical depression: relation to neurocircuitry and somatic consequences. Proc Assoc Am Physicians. 1999; 111(1): 22–34.CrossRefGoogle ScholarPubMed
45. Pintor, L, Torres, X, Navarro, V, Martinez de Osaba, MJ, Matrai, S, Gasto, C. Corticotropin-releasing factor test in melancholic patients in depressed state versus recovery: a comparative study. Prog Neuropsychopharmacology Biol Psychiatry. 2007; 31(5): 1027–1033.CrossRefGoogle ScholarPubMed
46. Coplan, JD, Smith, ELP, Altemus, M, et al. Maternal-infant response to variable foraging demand in nonhuman primates: effects of timing of stressor on cerebrospinal fluid corticotropin-releasing factor and circulating glucocorticoid concentrations. Ann N Y Acad Sci. 2006; 1071: 525–533.CrossRefGoogle ScholarPubMed
47. Van Oers, HJ, de Kloet, ER, Levine, S. Early vs. late maternal deprivation differentially alters the endocrine and hypothalamic responses to stress. Brain Res Dev Brain Res. 1998; 111(2): 245–252.CrossRefGoogle ScholarPubMed
48. Pesonen, AK, Räikkönen, K, Feldt, K, et al. Childhood separation experience predicts HPA axis hormonal responses in late adulthood: a natural experiment of World War II. Psychoneuroendocrinology. 2010; 35(5): 758–767.Google ScholarPubMed
49. Mullen, PE, Martin, JL, Anderson, JC, Romans, SE, Herbison, GP. Childhood sexual abuse and mental health in adult life. Br J Psychiatry. 1993; 163(6): 721–732.Google ScholarPubMed
50. MacLean, K. The impact of institutionalization on child development. Dev Psychopathol. 2003; 15(4): 853–884.CrossRefGoogle ScholarPubMed
51. Gunnar, MR, Bruce, J, Grotevant, HD. International adoption of institutionally reared children : research and policy. Dev Psychopathol. 2000; 12(4): 677–693.CrossRefGoogle ScholarPubMed
52. Pollak, SD, Nelson, CA, Schlaak, MF, Roeber, BJ, Wewerka, SS, Wiik, KL. Neurodevelopmental effects of early deprivation in post-institutionalized children. Child Dev. 2010; 81(1): 224–236.CrossRefGoogle Scholar
53. Gunnar, MR, van Dulmen, MHM, International Adoption Project Team. Behavior problems in postinstitutionalized internationally adopted children. Dev Psychopathol. 2007; 19(1): 129–148.CrossRefGoogle ScholarPubMed
54. Rutter, ML, Kreppner, JM, O’Connor, TG, English and Romanian Adoptees (ERA) Study Team. Specificity and heterogeneity in children’s responses to profound institutional privation. Br J Psychiatry. 2001; 179(2): 97–103.CrossRefGoogle ScholarPubMed
55. Zeanah, CH, Egger, HL, Smyke, AT, et al. Institutional rearing and psychiatric disorders in Romanian preschool children. Am J Psychiatry. 2009; 166(7): 777–785.CrossRefGoogle ScholarPubMed
56. Mehta, MA, Golembo, NI, Nosarti, C, et al. Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: the English and Romanian Adoptees study pilot. J Child Psychol Psychiatry. 2009; 50(8): 943–951.CrossRefGoogle ScholarPubMed
57. Tottenham, N, Hare, TA, Quinn, BT, et al. Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Dev Sci. 2010; 13(1): 46–61.CrossRefGoogle ScholarPubMed
58. Pechtel, P, Lyons-Ruth, K, Anderson, CM, Teicher, MH. Sensitive periods of amygdala development: the role of maltreatment in preadolescence. Neuroimage. 2014; 97: 236–244.CrossRefGoogle ScholarPubMed
59. Tottenham, N, Sheridan, MA. A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing. Front Hum Neurosci. 2009; 3: 68.Google ScholarPubMed
60. Andersen, SL, Teicher, MH. Stress, sensitive periods and maturational events in adolescent depression. Trends Neurosci. 2008; 31(4): 183–191.Google ScholarPubMed
61. Angold, A, Costello, EJ. Puberty and depression. Child Adolesc Psychiatr Clin N Am. 2006; 15(4): 919–937, ix.CrossRefGoogle ScholarPubMed
62. Paus, T, Keshavan, M, Giedd, JN. Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci. 2008; 9(12): 947–957.Google ScholarPubMed
63. Raineki, C, Cortés, MR, Belnoue, L, Sullivan, RM. Effects of early-life abuse differ across development: infant social behavior deficits are followed by adolescent depressive-like behaviors mediated by the amygdala. J Neurosci. 2012; 32(22): 7758–7765.CrossRefGoogle ScholarPubMed
64. Davidson, RJ, Pizzagalli, D, Nitschke, JB, Putnam, K. Depression: perspectives from affective neuroscience. Annu Rev Psychol. 2002; 53: 545–574.CrossRefGoogle ScholarPubMed
65. Stahl, S, Zhang, L, Damatarca, C, Grady, M. Brain Circuits Determine Destiny in Depression : A Novel Approach to the Psychopharmacology of wakefulness, fatigue, and executive dysfunction in major depressive disorder. J Clin Psychiatry. 2003; 64(Suppl 14): 6–17.Google Scholar
66. Mayberg, HS, Liotti, M, Brannan, SK, et al. Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry. 1999; 156(5): 675–682.CrossRefGoogle ScholarPubMed
67. Price, JL, Drevets, WC. Neurocircuitry of mood disorders. Neuropsychopharmacology. 2010; 35(1): 192–216.CrossRefGoogle ScholarPubMed
68. Drevets, WC. Neuroimaging studies of mood disorders. Biol Psychiatry. 2000; 48(8): 813–829.Google ScholarPubMed
69. Anand, A, Li, Y, Wang, Y, et al. Activity and connectivity of brain mood regulating circuit in depression: a functional magnetic resonance study. Biol Psychiatry. 2005; 57(10): 1079–1088.Google ScholarPubMed
70. Soares, JC, Mann, JJ. The anatomy of mood disorders—review of structural neuroimaging studies. Biol Psychiatry. 1997; 41(1): 86–106.CrossRefGoogle ScholarPubMed
71. Johnstone, T, van Reekum, CM, Urry, HL, Kalin, NH, Davidson, RJ. Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. J Neurosci. 2007; 27(33): 8877–8884.Google ScholarPubMed
72. Davidson, RJ, Jackson, DC, Kalin, NH. Emotion, plasticity, context, and regulation: perspectives from affective neuroscience. Psychol Bull. 2000; 126(6): 890–909.CrossRefGoogle ScholarPubMed
73. Roberts, JE, Kassel, JD. Mood-state dependence in cognitive vulnerability to depression: the roles of positive and negative affect. Cognitive Therapy and Research. 1996; 20(1): 1–12.Google Scholar
74. Elliott, R, Sahakian, BJ, Michael, A, Paykel, ES, Dolan, RJ. Abnormal neural response to feedback on planning and guessing tasks in patients with unipolar depression. Psychol Med. 1998; 28(3): 559–571.CrossRefGoogle ScholarPubMed
75. Elliott, R, Rubinsztein, JS, Sahakian, BJ, Dolan, RJ. The neural basis of mood-congruent processing biases in depression. Arch Gen Psychiatry. 2002; 59(7): 597–604.CrossRefGoogle ScholarPubMed
76. Forbes, EE, Dahl, RE. Neural systems of positive affect: relevance to understanding child and adolescent depression? Dev Psychopathol. 2005; 17(3): 827–850.CrossRefGoogle ScholarPubMed
77. Mitterschiffthaler, MT, Kumari, V, Malhi, GS, et al. Neural response to pleasant stimuli in anhedonia: an fMRI study. Neuroreport. 2003; 14(2): 177–182.CrossRefGoogle ScholarPubMed
78. Sheline, YI, Barch, DM, Donnelly, JM, Ollinger, JM, Snyder, AZ, Mintun, MA. Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biol Psychiatry. 2001; 50(9): 651–658.CrossRefGoogle ScholarPubMed
79. Siegle, GJ, Steinhauer, SR, Thase, ME, Stenger, VA, Carter, CS. Can’t shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals. Biol Psychiatry. 2002; 51(9): 693–707.Google ScholarPubMed
80. Dunlop, BW, Nemeroff, CB. The role of dopamine in the pathophysiology of depression. Arch Gen Psychiatry. 2007; 64(3): 327–337.CrossRefGoogle ScholarPubMed
81. Cabib, S, Puglisi-Allegra, S. Stress, depression and the mesolimbic dopamine system. Psychopharmacology (Berl). 1996; 128(4): 331–342.CrossRefGoogle ScholarPubMed
82. Pizzagalli, DA. Depression, stress, and anhedonia: toward a synthesis and integrated model. Annu Rev Clin Psychol. 2014; 10: 393–423.CrossRefGoogle Scholar
83. Hardin, MG, Schroth, E, Pine, DS, Ernst, M. Incentive-related modulation of cognitive control in healthy, anxious, and depressed adolescents: development and psychopathology related differences. J Child Psychol Psychiatry. 2007; 48(5): 446–454.CrossRefGoogle ScholarPubMed
84. Sesack, SR, Grace, AA. Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology. 2010; 35(1): 27–47.CrossRefGoogle ScholarPubMed
85. Haber, SN, Fudge, JL, McFarland, NR. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci. 2000; 20(6): 2369–2382.CrossRefGoogle ScholarPubMed
86. Haber, SN, Knutson, B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology. 2010; 35(1): 4–26.CrossRefGoogle ScholarPubMed
87. Robbins, TW, Everitt, BJ. Neurobehavioural mechanisms of reward and motivation. Curr Opin Neurobiol. 1996; 6(2): 228–236.CrossRefGoogle ScholarPubMed
88. Goff, B, Gee, DG, Telzer, EH, et al. Reduced nucleus accumbens reactivity and adolescent depression following early-life stress. Neuroscience. 2013; 249: 129–138.Google ScholarPubMed
89. Bos, K, Zeanah, CH, Fox, NA, Drury, SS, McLaughlin, KA, Nelson, CA. Psychiatric outcomes in young children with a history of institutionalization. Harv Rev Psychiatry. 2011; 19(1): 15–24.CrossRefGoogle ScholarPubMed
90. Mehta, MA, Gore-Langton, E, Golembo, N, Colvert, E, Williams, SCR, Sonuga-Barke, E. Hyporesponsive reward anticipation in the basal ganglia following severe institutional deprivation early in life. J Cogn Neurosci. 2010; 22(10): 2316–2325.CrossRefGoogle ScholarPubMed
91. Knutson, B, Adams, CM, Fong, GW, Hommer, D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci. 2001; 21(16): RC159.CrossRefGoogle ScholarPubMed
92. O’Doherty, J, Dayan, P, Schultz, J, Deichmann, R, Friston, K, Dolan, RJ. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science. 2004; 304(5669): 452–454.CrossRefGoogle ScholarPubMed
93. Pagnoni, G, Zink, CF, Montague, PR, Berns, GS. Activity in human ventral striatum locked to errors of reward prediction. Nat Neurosci . 2002; 5(2): 97–98.CrossRefGoogle ScholarPubMed
94. Tanaka, SC, Doya, K, Okada, G, Ueda, K, Okamoto, Y, Yamawaki, S. Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops. Nat Neurosci. 2004; 7(8): 887–893.CrossRefGoogle ScholarPubMed
95. Ikemoto, S, Panksepp, J. The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev. 1999; 31(1): 6–41.CrossRefGoogle ScholarPubMed
96. Epstein, J, Pan, H, Kocsis, JH, et al. Lack of ventral striatal response to positive stimuli in depressed versus normal subjects. Am J Psychiatry. 2006; 163(10): 1784–1790.CrossRefGoogle ScholarPubMed
97. Lawrence, NS, Williams, AM, Surguladze, S, et al. Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression. Biol Psychiatry. 2004; 55(6): 578–587.CrossRefGoogle ScholarPubMed
98. McCabe, C, Cowen, PJ, Harmer, CJ. Neural representation of reward in recovered depressed patients. Psychopharmacology (Berl). 2009; 205(4): 667–677.Google ScholarPubMed
99. Steele, JD, Kumar, P, Ebmeier, KP. Blunted response to feedback information in depressive illness. Brain. 2007; 130(Pt 9): 2367–2374.Google ScholarPubMed
100. Izuma, K, Saito, DN, Sadato, N. Processing of the incentive for social approval in the ventral striatum during charitable donation. J Cogn Neurosci. 2010; 22(4): 621–631.Google ScholarPubMed
101. Fareri, DS, Delgado, MR. The Importance of Social Rewards and Social Networks in the Human Brain. The Neuroscientist. 2014; 20(4): 387–402.CrossRefGoogle Scholar
102. Fliessbach, K, Weber, B, Trautner, P, et al. Social comparison affects reward-related brain activity in the human ventral striatum. Science. 2007; 318(5854): 1305–1308.CrossRefGoogle ScholarPubMed
103. Hirschfeld, RM, Montgomery, SA, Keller, MB, et al. Social functioning in depression: a review. J Clin Psychiatry. 2000; 61(4): 268–275.CrossRefGoogle ScholarPubMed
104. Giedd, JN, Snell, JW, Lange, N, et al. Quantitative magnetic resonance imaging of human brain development: ages 4–18. Cereb Cortex. 1996; 6(4): 551–560.CrossRefGoogle ScholarPubMed
105. Ernst, M, Nelson, EE, Jazbec, S, et al. Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents. Neuroimage. 2005; 25(4): 1279–1291.CrossRefGoogle ScholarPubMed
106. Galvan, A, Hare, TA, Parra, CE, et al. Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. J Neurosci. 2006; 26(25): 6885–6892.CrossRefGoogle ScholarPubMed
107. Geier, C, Luna, B. The maturation of incentive processing and cognitive control. Pharmacol Biochem Behav. 2009; 93(3): 212–221.Google ScholarPubMed
108. Urošević, S, Collins, P, Lim, K, Muetzel, R, Luciana, M. Longitudinal changes in behavioral approach system sensitivity and brain structures involved in reward processing during adolescence. Dev Psychol. 2012; 48(5): 1488–1500.CrossRefGoogle ScholarPubMed
109. Van Leijenhorst, L, Zanolie, K, Van Meel, CS, Westenberg, PM, Rombouts, SA, Crone, EA. What motivates the adolescent? Brain regions mediating reward sensitivity across adolescence. Cereb Cortex. 2010; 20(1): 61–69.CrossRefGoogle ScholarPubMed
110. Costello, EJ, Pine, DS, Hammen, C, et al. Development and natural history of mood disorders. Biol Psychiatry. 2002; 52(6): 529–542.CrossRefGoogle ScholarPubMed
111. Zahn-Waxler, C, Shirtcliff, EA, Marceau, K. Disorders of childhood and adolescence: gender and psychopathology. Annu Rev Clin Psychol. 2008; 4: 275–303.CrossRefGoogle ScholarPubMed
112. Bogdan, R, Nikolova, YS, Pizzagalli, DA. Neurogenetics of depression: a focus on reward processing and stress sensitivity. Neurobiol Dis. 2013; 52: 12–23.Google ScholarPubMed
113. Powell, SB, Geyer, MA, Preece, MA, Pitcher, LK, Reynolds, GP, Swerdlow, NR. Dopamine depletion of the nucleus accumbens reverses isolation-induced deficits in prepulse inhibition in rats. Neuroscience. 2003; 119(1): 233–240.Google ScholarPubMed
114. Hall, FS, Wilkinson, LS, Humby, T, et al. Isolation rearing in rats: Pre- and postsynaptic changes in striatal dopaminergic systems. Pharmacol Biochem Behav. 1998; 59(4): 859–872.CrossRefGoogle ScholarPubMed
115. Jones, GH, Hernandez, TD, Kendall, DA, Marsden, CA, Robbins, TW. Dopaminergic and serotonergic function following isolation rearing in rats: study of behavioural responses and postmortem and in vivo neurochemistry. Pharmacol Biochem Behav. 1992; 43(1): 17–35.CrossRefGoogle ScholarPubMed
116. Fulford, AJ, Marsden, CA. Effect of isolation-rearing on conditioned dopamine release in vivo in the nucleus accumbens of the rat. J Neurochem. 1998; 70(1): 384–390.CrossRefGoogle ScholarPubMed
117. Lapiz, MDS, Mateo, Y, Parker, T, Marsden, C. Effects of noradrenaline depletion in the brain on response to novelty in isolation-reared rats. Psychopharmacology (Berl). 2000; 152(3): 312–320. doi:10.1007/s002130000534.CrossRefGoogle ScholarPubMed
118. Dillon, DG, Holmes, AJ, Birk, JL, Brooks, N, Lyons-Ruth, K, Pizzagalli, DA. Childhood adversity is associated with left basal in adulthood. Biol Psychiatry. 2009; 66(3): 206–213.CrossRefGoogle ScholarPubMed
119. Wise, RA. Neuroleptics and operant behavior: the anhedonia hypothesis. Behav Brain Sci. 1982; 5(1): 39–53.CrossRefGoogle Scholar
120. Wise, RA. Addictive drugs and brain stimulation reward. Annu Rev Neurosci. 1996; 19: 319–340.CrossRefGoogle ScholarPubMed
121. Dackis, CA, Gold, MS. New concepts in cocaine addiction: the dopamine depletion hypothesis. Neurosci Biobehav Rev. 1985; 9(3): 469–477.CrossRefGoogle ScholarPubMed
122. Koob, GF, Le Moal, M. Drug abuse: hedonic homeostatic dysregulation. Science. 1997; 278(5335): 52–58.CrossRefGoogle ScholarPubMed
123. Markou, A, Koob, GF. Postcocaine anhedonia: an animal model of cocaine withdrawal. Neuropsychopharmacology. 1991; 4(1): 17–26.Google ScholarPubMed
124. Rossetti, ZL, Hmaidan, Y, Gessa, GL. Marked inhibition of mesolimbic dopamine release: a common feature of ethanol, morphine, cocaine and amphetamine abstinence in rats. Eur J Pharmacol. 1992; 221(2–3): 227–234.CrossRefGoogle ScholarPubMed
125. Volkow, ND, Wang, GJ, Fowler, JS, et al. Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects. Nature. 1997; 386(6627): 830–833.Google ScholarPubMed
126. Di Chiara, G, Tanda, G. Blunting of reactivity of dopamine transmission to palatable food: a biochemical marker of anhedonia in the CMS model? Psychopharmacology (Berl). 1997; 134(4): 351–353; discussion 371–377.CrossRefGoogle ScholarPubMed
127. Willner, P. Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology. 2005; 52(2): 90–110.CrossRefGoogle ScholarPubMed
128. Bechara, A, Harrington, F, Nader, K, van der Kooy, D. Neurobiology of motivation: double dissociation of two motivational mechanisms mediating opiate reward in drug-naive versus drug-dependent animals. Behav Neurosci. 1992; 106(5): 798–807.CrossRefGoogle ScholarPubMed
129. Nader, K, Bechara, A, van der Kooy, D. Neurobiological constraints on behavioral models of motivation. Annu Rev Psychol. 1997; 48: 85–114.CrossRefGoogle ScholarPubMed
130. Kehoe, P, Shoemaker, WJ, Triano, L, Hoffman, J, Arons, C. Repeated isolation in the neonatal rat produces alterations in behavior and ventral striatal dopamine release in the juvenile after amphetamine challenge. Behav Neurosci. 1996; 110(6): 1435–1444.CrossRefGoogle ScholarPubMed
131. Hall, FS, Wilkinson, LS, Humby, T, Robbins, TW. Maternal deprivation of neonatal rats produces enduring changes in dopamine function. Synapse. 1999; 32(1): 37–43.Google ScholarPubMed
132. Pruessner, JC, Champagne, F, Meaney, MJ, Dagher, A. Dopamine release in response to a psychological stress in humans and its relationship to early life maternal care: a positron emission tomography study using [11C]raclopride. J Neurosci . 2004; 24(11): 2825–2831.CrossRefGoogle Scholar
133. Jahn, AL, Fox, AS, Abercrombie, HC, et al. Subgenual prefrontal cortex activity predicts individual differences in hypothalamic-pituitary-adrenal activity across different contexts. Biol Psychiatry. 2010; 67(2): 175–181.CrossRefGoogle ScholarPubMed
134. McEwen, BS, Gianaros, PJ. Central role of the brain in stress and adaptation: Links to socioeconomic status, health, and disease. Ann N Y Acad Sci. 2010; 1186: 190–222.CrossRefGoogle ScholarPubMed
135. Pruessner, JC, Dedovic, K, Pruessner, M, et al. Stress regulation in the central nervous system: evidence from structural and functional neuroimaging studies in human populations—2008 Curt Richter Award Winner. Psychoneuroendocrinology. 2010; 35(1): 179–191.Google ScholarPubMed
136. Tarullo, AR, Gunnar, MR. Child maltreatment and the developing HPA axis. Horm Behav. 2006; 50(4): 632–639.CrossRefGoogle ScholarPubMed
137. Carroll, BJ, Curtis, GC, Mendels, J. Cerebrospinal fluid and plasma free cortisol concentrations in depression. Psychol Med. 1976; 6(2): 235–244.CrossRefGoogle ScholarPubMed
138. Holsboer, F. Stress, hypercortisolism and corticosteroid receptors in depression: Implicatons for therapy. J Affect Disord. 2001; 62(1–2): 77–91.Google Scholar
139. Martínez-Téllez, RI, Hernández-Torres, E, Gamboa, C, Flores, G. Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse. 2009; 63(9): 794–804.CrossRefGoogle ScholarPubMed
140. Leão, P, Sousa, JC, Oliveira, M, Silva, R, Almeida, OF, Sousa, N. Programming effects of antenatal dexamethasone in the developing mesolimbic pathways. Synapse. 2007; 61(1): 40–49.CrossRefGoogle ScholarPubMed
141. Biron, D, Dauphin, C, Di Paolo, T. Effects of adrenalectomy and glucocorticoids on rat brain dopamine receptors. Neuroendocrinology. 1992; 55(4): 468–476.CrossRefGoogle ScholarPubMed
142. Barrot, M, Marinelli, M, Abrous, DN, Rougé-Pont, F, Le Moal, M, Piazza, PV. The dopaminergic hyper-responsiveness of the shell of the nucleus accumbens is hormone-dependent. Eur J Neurosci. 2000; 12(3): 973–979.CrossRefGoogle ScholarPubMed
143. Andersen, SL, Lyss, PJ, Dumont, NL, Teicher, MH. Enduring neurochemical effects of early maternal separation on limbic structures. Ann N Y Acad Sci. 1999; 877: 756–759.CrossRefGoogle ScholarPubMed
144. Küppers, E, Beyer, C. Dopamine regulates brain-derived neurotrophic factor (BDNF) expression in cultured embryonic mouse striatal cells. Neuroreport. 2001; 12(6): 1175–1179.CrossRefGoogle ScholarPubMed
145. Berton, O, McClung, CA, Dileone, RJ, et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science. 2006; 311(5762): 864–868.CrossRefGoogle ScholarPubMed
146. Cordeira, JW, Frank, L, Sena-Esteves, M, Pothos, EN, Rios, M. Brain-derived neurotrophic factor regulates hedonic feeding by acting on the mesolimbic dopamine system. J Neurosci. 2010; 30(7): 2533–2541.CrossRefGoogle ScholarPubMed
147. Smith, MA. Hippocampal vulnerability to stress and aging: possible role of neurotrophic factors. Behav Brain Res. 1996; 78(1): 25–36.Google ScholarPubMed
148. Lippmann, M, Bress, A, Nemeroff, CB, Plotsky, PM, Monteggia, LM. Long-term behavioural and molecular alterations associated with maternal separation in rats. Eur J Neurosci. 2007; 25(10): 3091–3098.CrossRefGoogle ScholarPubMed
149. Lee, B-H, Kim, Y-K. The roles of BDNF in the pathophysiology of major depression and in antidepressant treatment. Psychiatry Investig. 2010; 7(4): 231–235.CrossRefGoogle ScholarPubMed
150. Karege, F, Bondolfi, G, Gervasoni, N, Schwald, M, Aubry, JM, Bertschy, G. Low Brain-Derived Neurotrophic Factor (BDNF) levels in serum of depressed patients probably results from lowered platelet BDNF release unrelated to platelet reactivity. Biol Psychiatry. 2005; 57(9): 1068–1072.CrossRefGoogle ScholarPubMed
151. Shimizu, E, Hashimoto, K, Okamura, N, et al. Alterations of serum levels of brain-derived neurotrophic factor (BDNF) in depressed patients with or without antidepressants. Biol Psychiatry. 2003; 54(1): 70–75.CrossRefGoogle ScholarPubMed
152. Dwivedi, Y. Brain-derived neurotrophic factor: role in depression and suicide. Neuropsychiatr Dis Treat. 2009; 5: 433–449.CrossRefGoogle ScholarPubMed
153. Nestler, EJ, Carlezon, WA Jr. The mesolimbic dopamine reward circuit in depression. Biol Psychiatry. 2006; 59(12): 1151–1159.CrossRefGoogle ScholarPubMed
154. Karege, F, Perret, G, Bondolfi, G, Schwald, M, Bertschy, G, Aubry, JM. Decreased serum brain-derived neurotrophic factor levels in major depressed patients. Psychiatry Res. 2002; 109(2): 143–148.CrossRefGoogle ScholarPubMed
155. Pechtel, P, Pizzagalli, DA. Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology (Berl). 2011; 214(1): 55–70.Google ScholarPubMed