Childhood Adversity Is Associated with Left Basal Ganglia Dysfunction During Reward Anticipation in Adulthood

Biological Psychiatry

Volumn 66, Issue 3, 2009, Pages 206-213

  Dillon, Daniel G ^a   Holmes, Avram J ^a   Birk, Jeffrey L ^a   Brooks, Nancy ^a   Lyons Ruth, Karlen ^b   Pizzagalli, Diego A ^a  

^a HARVARD UNIVERSITY   (United States)

^b CAMBRIDGE HOSPITAL   (United States)

Author keywords

Anhedonia; basal ganglia; fMRI; maltreatment; reward; stress

Indexed keywords

ADULT; ADULTHOOD; ANHEDONIA; ARTICLE; ASSOCIATION; BASAL GANGLION; BRAIN DYSFUNCTION; CHILD ABUSE; CHILDHOOD; CONTROLLED STUDY; DEPRESSION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLOBUS PALLIDUS; HEMISPHERE; HUMAN; LEARNING; MALE; MOTIVATION; PRIORITY JOURNAL; PUNISHMENT; REWARD;

ADULT; ADULT SURVIVORS OF CHILD ABUSE; ANALYSIS OF VARIANCE; BASAL GANGLIA; BRAIN MAPPING; CUES; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MENTAL DISORDERS; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PSYCHIATRIC STATUS RATING SCALES; REACTION TIME; REGRESSION ANALYSIS; REWARD; YOUNG ADULT;

EID: 67649403175     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2009.02.019     Document Type: Article

References (59)

1. Dube S.R., Anda R.F., Felitti V.J., Chapman D.P., Williamson D.F., and Giles W.H. Childhood abuse, household dysfunction, and the risk of attempted suicide throughout the life span: Findings from the adverse childhood experiences study. JAMA 286 (2001) 3089-3096
2. Dube S.R., Felitti V.J., Dong M., Chapman D.P., Giles W.H., and Anda R.F. Childhood abuse, neglect, and household dysfunction and the risk of illicit drug use: The adverse childhood experiences study. Pediatrics 111 (2003) 564-572
3. Anda R.F., Croft J.B., Felitti V.J., Nordenberg D., Giles W.H., Williamson D.F., et al. Adverse childhood experiences and smoking during adolescence and adulthood. JAMA 282 (1999) 1652-1658
4. Widom C.S. Posttraumatic stress disorder in abused and neglected children grown up. Am J Psychiatry 156 (1999) 1223-1229
5. Nelson E.C., Heath A.C., Madden P.A., Cooper M.L., Dinwiddie S.H., Bucholz K.K., et al. Association between self-reported childhood sexual abuse and adverse psychosocial outcomes: Results from a twin study. Arch Gen Psychiatry 59 (2002) 139-145
6. Gladstone G.L., Parker G.B., Mitchell P.B., Malhi G.S., Wilhelm K., and Austin M.P. Implications of childhood trauma for depressed women: An analysis of pathways from childhood sexual abuse to deliberate self-harm and revictimization. Am J Psychiatry 161 (2004) 1417-1425
7. Heim C., Newport D.J., Heit S., Graham Y.P., Wilcox M., Bonsall R., et al. Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. JAMA 284 (2000) 592-597
8. Navalta C.P., Polcari A., Webster D.M., Boghossian A., and Teicher M.H. Effects of childhood sexual abuse on neuropsychological and cognitive function in college women. J Neuropsychiatr Clin Neurosci 18 (2006) 45-53
9. Bremner J.D., Vythilingam M., Vermetten E., Southwick S.M., McGlashan T., Nazeer A., et al. MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. Am J Psychiatry 160 (2003) 924-932
10. Guyer A.E., Kaufman J., Hodgdon H.B., Masten C.L., Jazbec S., Pine D.S., et al. Behavioral alterations in reward system function: The role of childhood maltreatment and psychopathology. J Am Acad Child Adolesc Psychiatry 45 (2006) 1059-1067
11. Fawcett J., Clark D.C., Scheftner W.A., and Gibbons R.D. Assessing anhedonia in psychiatric patients. Arch Gen Psychiatry 40 (1983) 79-84
12. APA. Diagnostic and Statistical Manual of Mental Disorders. 4th ed. (2000), American Psychiatric Association, Washington, DC
13. Lumley M., and Harkness K. Specificity in the relations among childhood adversity, early maladaptive schemas, and symptom profiles in adolescent depression. Cogn Ther Res 31 (2007) 639-657
14. Harkness K., and Monroe S. Childhood adversity and the endogenous versus nonendogenous distinction in women with major depression. Am J Psychiatry 159 (2002) 387-393
15. Cabib S., and Puglisi-Allegra S. Stress, depression and the mesolimbic dopamine system. Psychopharmacology 128 (1996) 331-342
16. Matthews K., and Robbins T.W. Early experience as a determinant of adult behavioural response to reward: The effects of repeated maternal separation in the rat. Neurosci Biobehav Rev 27 (2003) 45-55
17. Pryce C.R., Dettling A.C., Spengler M., Schnell C.R., and Feldon J. Deprivation of parenting disrupts development of homeostatic and reward systems in marmoset monkey offspring. Biol Psychiatry 56 (2004) 72-79
18. Anisman H., and Matheson K. Stress, depression, and anhedonia: Caveats concerning animal models. Neurosci Biobehav Rev 29 (2005) 525-546
19. Willner P. Chronic mild stress (CMS) revisited: Consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 52 (2005) 90-110
20. Martin L.J., Spicer D.M., Lewis M.H., Gluck J.P., and Cork L.C. Social deprivation of infant rhesus monkeys alters the chemoarchitecture of the brain. I. Subcortical regions. J Neurol Sci 11 (1991) 3344-3358
21. Smith K.S., Tindell A.J., Aldridge J.W., and Berridge K.C. Ventral pallidum roles in reward and motivation. Behav Brain Res 196 (2009) 155-167
22. Knutson B., and Cooper J.C. Functional magnetic resonance imaging of reward prediction. Curr Opin Neurol 18 (2005) 411-417
23. Dillon D.G., Holmes A.J., Jahn A.L., Bogdan R., Wald L.L., and Pizzagalli D.A. Dissociation of neural regions associated with anticipatory versus consummatory phases of incentive processing. Psychophysiology 45 (2008) 36-49
24. Lyons-Ruth K., Connell D.B., Grunebaum H.U., and Botein S. Infants at social risk: Maternal depression and family support services as mediators of infant development and security of attachment. Child Dev 61 (1990) 85-98
25. Bjork J.M., Knutson B., Fong G.W., Caggiano D.M., Bennett S.M., and Hommer D.W. Incentive-elicited brain activation in adolescents: Similarities and differences from young adults. J Neurol Sci 24 (2004) 1793-1802
26. Samanez-Larkin G.R., Gibbs S.E., Khanna K., Nielsen L., Carstensen L.L., and Knutson B. Anticipation of monetary gain but not loss in healthy older adults. Nat Neurosci 10 (2007) 787-791
27. Schott B.H., Minuzzi L., Krebs R.M., Elmenhorst D., Lang M., Winz O.H., et al. Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release. J Neurol Sci 28 (2008) 14311-14319
28. George C., Kaplan N., and Main M. Adult Attachment Interview (1985), University Of California Berkeley, Berkeley, California
29. Lyons-Ruth K., and Block D. The disturbed caregiving system: Relations among childhood trauma, maternal caregiving, and infant affect and attachment. Infant Ment Health J 17 (1996) 257-275
30. Strauss M.A., Hamby S.L., Boney-McCoy S., and Sugarman D.B. The revised conflict tactics scale (CTS2). J Fam Issues 17 (1996) 283-316
31. Norris F.H. Screening for traumatic stress: A scale for use in the general population. J Appl Soc Psychol 20 (1990) 1704-1718
32. Chapman L.J., and Chapman J.P. The measurement of handedness. Brain Cogn 6 (1987) 175-183
33. Pizzagalli DA, Holmes AJ, Dillon DG, Goetz EL, Birk JL, Bogdan R, et al. (in press): Reduced caudate and nucleus accumbens response to rewards in unmedicated subjects with major depressive disorder. Am J Psychiatry.
34. First M.B., Spitzer R.L., Gibbon M., and Williams J.B.W. Structured clinical interviews for DSM-IV axis I disorders (SCID) (1995), American Psychiatric Press, Washington, DC
35. Watson D., Clark L.A., Weber K., Assenheimer J.S., Strauss M.E., and McCormick R.A. Testing a tripartite model. II. Exploring the symptom structure of anxiety and depression in student, adult, and patient samples. J Abnorm Psychol 104 (1995) 15-25
36. Radloff L.S. The CES-D scale: A self-report depression scale for research in the general population. Appl Psychol Measure 1 (1977) 385-401
37. Beck A.T., Steer R.A., and Brown G.K. Beck Depression Inventory Manual. 2nd ed. (1996), Psychological Corporation, San Antonio, Texas
38. Deichmann R., Gottfried J.A., Hutton C., and Turner R. Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage 19 (2003) 430-441
39. Fischl B., Salat D.H., Busa E., Albert M., Dieterich M., Haselgrove C., et al. Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron 33 (2002) 341-355
40. Tae W.S., Kim S.S., Lee K.U., Nam E.-C., and Kim K.W. Validation of hippocampal volumes measured using a manual method and two automated methods (FreeSurfer and IBASPM) in chronic major depressive disorder. Neuroradiology 50 (2008) 569-581
41. Miller G.A., and Chapman J.P. Misunderstanding analysis of covariance. J Abnorm Psychol 110 (2001) 40-48
42. Blumenthal J.A., Lett H.S., Babyak M.A., White W., Smith P.K., Mark D.B., et al., NORG Investigators. Depression as a risk factor for mortality after coronary artery bypass surgery. Lancet 362 (2003) 604-609
43. Pizzagalli D.A., Jahn A.L., and O'Shea J.P. Toward an objective characterization of an anhedonic phenotype: A signal-detection approach. Biol Psychiatry 15 (2005) 319-327
44. Frank M.J., and Claus E.D. Anatomy of a decision: Striato-orbitofrontal interactions in reinforcement learning, decision making, and reversal. Psychol Rev 113 (2006) 300-326
45. Kalinichev M., Easterling K.W., and Holtzman S.G. Early neonatal experience of Long-Evans rats results in long-lasting changes in morphine tolerance and dependence. Psychopharmacology 157 (2001) 305-312
46. Epstein J., Pan H., Kocsis J.H., Yang Y., Butler T., Chusid J., et al. Lack of ventral striatal response to positive stimuli in depressed versus normal subjects. Am J Psychiatry 163 (2006) 1784-1790
47. Gabbay V., Hess D.A., Liu S., Babb J.S., Klein R.G., and Gonen O. Lateralized caudate metabolic abnormalities in adolescent major depressive disorder: A proton MR spectroscopy study. Am J Psychiatry 164 (2007) 1881-1889
48. Drevets W.C., Videen T.O., Price J.L., Preskorn S.H., Carmichael S.T., and Raichle M.E. A functional anatomical study of unipolar depression. J Neurol Sci 12 (1992) 3628-3641
49. Meyer J.H., McNeely H.E., Sagrati S., Boovariwala A., Martin K., Verhoeff N.P., et al. Elevated putamen D(2) receptor binding potential in major depression with motor retardation: An [11C]raclopride positron emission tomography study. Am J Psychiatry 163 (2006) 1594-1602
50. Starkstein S.E., Robinson R.G., and Price T.R. Comparison of cortical and subcortical lesions in the production of poststroke mood disorders. Brain 110 (1987) 1045-1059
51. Vataja R., Leppavuori A., Pohjasvaara T., Mantyla R., Aronen H.J., Salonen O., et al. Poststroke depression and lesion location revisited. J Neuropsychiatr Clin Neurosci 16 (2004) 156-162
52. Tomer R., Goldstein R.Z., Wang G.J., Wong C., and Volkow N.D. Incentive motivation is associated with striatal dopamine asymmetry. Biol Psychol 77 (2008) 98-101
53. Teicher M.H., Ito Y., Glod C.A., Andersen S.L., Dumont N., and Ackerman E. Preliminary evidence for abnormal cortical development in physically and sexually abused children using EEG coherence and MRI. Ann N Y Acad Sci 821 (1997) 160-175
54. Carlson J.N., Fitzgerald L.W., Keller R.W., and Glick S.D. Lateralized changes in prefrontal cortical dopamine activity induced by controllable and uncontrollable stress in the rat. Brain Res 630 (1993) 178-187
55. Volkow N.D., Fowler J.S., Wang G.J., and Swanson J.M. Dopamine in drug abuse and addiction: Results from imaging studies and treatment implications. Mol Psychiatry 9 (2004) 557-569
56. Pollak S.D. Mechanisms linking early experience and the emergence of emotions. Curr Dir Psychol Sci 17 (2008) 370-375
57. Kaufman J., Yang B.Z., Douglas-Palumberi H., Houshyar S., Lipschitz D., Krystal J.H., et al. Social supports and serotonin transporter gene moderate depression in maltreated children. Proc Natl Acad Sci U S A 101 (2004) 17316-17321
58. Charney D. Psychobiological mechanisms for resilience and vulnerability: Implications for successful adaptation to extreme stress. Am J Psychiatry 161 (2004) 195-216
59. Dong M., Anda R.F., Felitti V.J., Dube S.R., Williamson D.F., Thompson T.J., et al. The interrelatedness of multiple forms of childhood abuse, neglect, and household dysfunction. Child Abus Negl 28 (2004) 771-784