Mild early life stress enhances prefrontal-dependent response inhibition in monkeys

Biological Psychiatry

Volumn 57, Issue 8, 2005, Pages 848-855

  Parker, Karen J ^a   Buckmaster, Christine L ^a   Justus, Katharine R ^a   Schatzberg, Alan F ^a   Lyons, David M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cognitive; HPA axis; Prefrontal cortex; Primate; Response inhibition; Stress inoculation; Stress resistance

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN FUNCTION; COGNITION; CONTROLLED STUDY; EXPERIENCE; FEMALE; HYPOPHYSIS ADRENAL SYSTEM; INHIBITION (PSYCHOLOGY); MALE; MONKEY; NEUROENDOCRINE SYSTEM; NONHUMAN; PERFORMANCE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PUERPERIUM; REACTIVE INHIBITION; REARING; STRESS;

EID: 16844362547     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2004.12.024     Document Type: Article

References (80)

1. A.F. Arnsten, P.S. Goldman-Rakic Noise stress impairs prefrontal cortical cognitive function in monkeys Evidence for a hyperdopaminergic mechanism Arch Gen Psychiatry 55 1998 362 368
2. A.R. Aron, T.W. Robbins, R.A. Poldrack Inhibition and the right inferior frontal cortex Trends Cogn Sci 8 2004 170 177
3. M.P. Austin, P. Mitchell, G.M. Goodwin Cognitive deficits in depression Possible implications for functional neuropathology Br J Psychiatry 178 2001 200 206
4. S. Bannon, C.J. Gonsalvez, R.J. Croft, P.M. Boyce Response inhibition deficits in obsessive-compulsive disorder Psychiatry Res 110 2002 165 174
5. J.K. Belanoff, K. Gross, A. Yager, A.F. Schatzberg Corticosteroids and cognition J Psychiatr Res 35 2001 127 145
6. S. Boinski, D.M. Fragaszy The ontogeny of foraging in squirrel monkeys, Saimiri oerstedi Anim Behav 37 1989 415 428
7. O. Bonne, A. Gilboa, Y. Louzoun, D. Brandes, I. Yona, H. Lester Resting regional cerebral perfusion in recent posttraumatic stress disorder Biol Psychiatry 54 2003 1077 1086
8. M.M. Botvinick, T.S. Braver, D.M. Barch, C.S. Carter, J.D. Cohen Conflict monitoring and cognitive control Psychol Rev 108 2001 624 652
9. W.T. Boyce, E. Chesterman Life events, social support, and cardiovascular reactivity in adolescence J Dev Behav Pediatr 11 1990 105 111
10. D.B. Bugental, G.A. Martorell, V. Barraza The hormonal costs of subtle forms of infant maltreatment Horm Behav 43 2003 237 244
11. G. Bush, P. Luu, M.I. Posner Cognitive and emotional influences in anterior cingulate cortex Trends Cogn Sci 4 2000 215 222
12. C.S. Carter, M.M. Botvinick, J.D. Cohen The contribution of the anterior cingulate cortex to executive processes in cognition Rev Neurosci 10 1999 49 57
13. J. Castle, C. Groothues, D. Bredenkamp, C. Beckett, T. O'Connor, M. Rutter Effects of qualities of early institutional care on cognitive attainment E.R.A. Study Team English and Romanian Adoptees Am J Orthopsychiatry 69 1999 424 437
14. D. Cicchetti, F.A. Rogosch Diverse patterns of neuroendocrine activity in maltreated children Dev Psychopathol 13 2001 677 693
15. C.L. Coe, S.P. Mendoza, W.P. Smotherman, S. Levine Mother-infant attachment in the squirrel monkey Adrenal response to separation Behav Neural Biol 22 1978 256 263
16. R.J. Davidson Anxiety and affective style Role of prefrontal cortex and amygdala Biol Psychiatry 51 2002 68 80
17. V. Delaney-Black, C. Covington, S.J. Ondersma, B. Nordstrom-Klee, T. Templin, J. Ager Violence exposure, trauma, and IQ and/or reading deficits among urban children Arch Pediatr Adolesc Med 156 2002 280 285
18. A. Diamond Developmental time course in human infants and infant monkeys, and the neural bases of, inhibitory control in reaching Ann N Y Acad Sci 608 1990 637 676
19. A. Diamond, S. Zola-Morgan, L.R. Squire Successful performance by monkeys with lesions of the hippocampal formation on AB and object retrieval, two tasks that mark developmental changes in human infants Behav Neurosci 103 1989 526 537
20. R. Dias, T.W. Robbins, A.C. Roberts Primate analogue of the Wisconsin Card Sorting Test Effects of excitotoxic lesions of the prefrontal cortex in the marmoset Behav Neurosci 110 1996 872 886
21. D. Diorio, V. Viau, M.J. Meaney The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress J Neurosci 13 1993 3839 3847
22. W.C. Drevets Neuroimaging and neuropathological studies of depression Implications for the cognitive-emotional features of mood disorders Curr Opin Neurobiol 11 2001 240 249
23. K. Erickson, W. Drevets, J. Schulkin Glucocorticoid regulation of diverse cognitive functions in normal and pathological emotional states Neurosci Biobehav Rev 27 2003 233 246
24. K.B. Forest The interplay of childhood stress and adult life events on women's symptoms of depression Diss Abstr Int 51 1991 3237
25. N. Garmezy, A.S. Masten, A. Tellegen The study of stress and competence in children A building block for developmental psychopathology Child Dev 55 1984 97 111
26. D. Glaser Child abuse and neglect and the brain-a review J Child Psychol Psychiatry 41 2000 97 116
27. W.J. Griffiths Jr, W.F. Stringer The effects of intense stimulation experienced during infancy on adult behavior in the rat J Comp Physiol Psychol 45 1952 301 306
28. M.R. Gunnar, L. Brodersen, M. Nachmias, K. Buss, J. Rigatuso Stress reactivity and attachment security Dev Psychobiol 29 1996 191 204
29. M.R. Gunnar, S.J. Morison, K. Chisholm, M. Schuder Salivary cortisol levels in children adopted from Romanian orphanages Dev Psychopathol 13 2001 611 628
30. S.L. Halligan, J. Herbert, I.M. Goodyer, L. Murray Exposure to postnatal depression predicts elevated cortisol in adolescent offspring Biol Psychiatry 55 2004 376 381
31. M.D. Hauser Perseveration, inhibition and the prefrontal cortex A new look Curr Opin Neurobiol 9 1999 214 222
32. C. Heim, C.B. Nemeroff Neurobiology of early life stress Clinical studies Semin Clin Neuropsychiatry 7 2002 147 159
33. D. Hoffman-Plotkin, C.T. Twentyman A multimodal assessment of behavioral and cognitive deficits in abused and neglected preschoolers Child Dev 55 1984 794 802
34. F.B. Holmes Experimental study of the fears of young children A.T. Jersild F.B. Holmes Children's Fears, Child Development Monographs, Number 20. 1935 Teacher's College, Columbia University New York 167 296
35. J.D. Jentsch, D.E. Redmond Jr, J.D. Elsworth, J.R. Taylor, K.D. Youngren, R.H. Roth Enduring cognitive deficits and cortical dopamine dysfunction in monkeys after long-term administration of phencyclidine Science 277 1997 953 955
36. S. Kaiser, J. Unger, M. Kiefer, J. Markela, C. Mundt, M. Weisbrod Executive control deficit in depression Event-related potentials in a Go/Nogo task Psychiatry Res 122 2003 169 184
37. S.R. Kaler, B.J. Freeman Analysis of environmental deprivation Cognitive and social development in Romanian orphans J Child Psychol Psychiatry 35 1994 769 781
38. J. Kaufman, P.M. Plotsky, C.B. Nemeroff, D.S. Charney Effects of early adverse experiences on brain structure and function Clinical implications Biol Psychiatry 48 2000 778 790
39. G. Keppel Design and Analysis, A Researcher's Handbook 1982 Prentice Hall. Englewood Cliffs, NJ
40. D.M. Khoshaba, S.R. Maddi Early experiences in hardiness development Consult Psychol J Pract Res 51 1999 106 116
41. G. Kochanska, A. Knaack Effortful control as a personality characteristic of young children Antecedents, correlates, and consequences J Pers 71 2003 1087 1112
42. G. Kochanska, K. Murray, T.Y. Jacques, A.L. Koenig, K.A. Vandegeest Inhibitory control in young children and its role in emerging internalization Child Dev 67 1996 490 507
43. G. Kochanska, K.T. Murray, E.T. Harlan Effortful control in early childhood Continuity and change, antecedents, and implications for social development Dev Psychol 36 2000 220 232
44. K.C. Koenen, T.E. Moffitt, A. Caspi, A. Taylor, S. Purcell Domestic violence is associated with environmental suppression of IQ in young children Dev Psychopathol 15 2003 297 311
45. A. Kuelz, F. Hohagen, U. Voderholzer Neuropsychological performance in obsessive-compulsive disorder A critical review Biol Psychol 65 2004 185 236
46. J. Lehmann, C.R. Pryce, D. Bettschen, J. Feldon The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats Pharmacol Biochem Behav 64 1999 705 715
47. J. Lehmann, T. Stohr, J. Schuller, A. Domeney, C. Heidbreder, J. Feldon Long-term effects of repeated maternal separation on three different latent inhibition paradigms Pharmacol Biochem Behav 59 1998 873 882
48. S. Levine A further study of infantile handling and adult avoidance learning J Pers 25 1956 70 80
49. S. Levine, C.L. Coe, W.P. Smotherman, J.N. Kaplan Prolonged cortisol elevation in the infant squirrel monkey after reunion with mother Physiol Behav 20 1978 7 10
50. S. Levine, T. Mody The long-term psychobiological consequences of intermittent postnatal separation in the squirrel monkey Neurosci Biobehav Rev 27 2003 83 89
51. D.M. Lyons, H. Afarian, A.F. Schatzberg, A. Sawyer-Glover, M.E. Moseley Experience-dependent asymmetric variation in primate prefrontal morphology Behav Brain Res 136 2002 51 59
52. D.M. Lyons, C.M. Ha, S. Levine Social effects and circadian rhythms in squirrel monkey pituitary-adrenal activity Horm Behav 29 1995 177 190
53. D.M. Lyons, J.M. Lopez, C. Yang, A.F. Schatzberg Stress-level cortisol treatment impairs inhibitory control of behavior in monkeys J Neurosci 20 2000 7816 7821
54. D.M. Lyons, F.L. Martel, S. Levine, N.J. Risch, A.F. Schatzberg Postnatal experiences and genetic effects on squirrel monkey social affinities and emotional distress Horm Behav 36 1999 266 275
55. D.M. Lyons, O.J. Wang, S.E. Lindley, S. Levine, N.H. Kalin, A.F. Schatzberg Separation induced changes in squirrel monkey hypothalamic-pituitary- adrenal physiology resemble aspects of hypercortisolism in humans Psychoneuroendocrinology 24 1999 131 142
56. P. Malloy, S. Rasmussen, W. Braden, R.J. Haier Topographic evoked potential mapping in obsessive-compulsive disorder Evidence of frontal lobe dysfunction Psychiatry Res 28 1989 63 71
57. M.J. Meaney Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations Annu Rev Neurosci 24 2001 1161 1192
58. M.J. Meaney, D.H. Aitken, C. van Berkel, S. Bhatnagar, R.M. Sapolsky Effect of neonatal handling on age-related impairments associated with the hippocampus Science 239 1988 766 768
59. M.J. Meaney, J. Diorio, D. Francis, J. Widdowson, P. LaPlante, C. Caldji Early environmental regulation of forebrain glucocorticoid receptor gene expression Implications for adrenocortical responses to stress Dev Neurosci 18 1996 49 72
60. M.J. Meaney, J.B. Mitchell, D.H. Aitken, S. Bhatnagar, S.R. Bodnoff, L.J. Iny The effects of neonatal handling on the development of the adrenocortical response to stress Implications for neuropathology and cognitive deficits in later life Psychoneuroendocrinology 16 1991 85 103
61. E.P. Merriam, M.E. Thase, G.L. Haas, M.S. Keshavan, J.A. Sweeney Prefrontal cortical dysfunction in depression determined by Wisconsin Card Sorting Test performance Am J Psychiatry 156 1999 780 782
62. R.K. Oates, A. Peacock, D. Forrest The development of abused children Dev Med Child Neurol 26 1984 649 656
63. K.N. Ochsner, S.A. Bunge, J.J. Gross, J.D. Gabrieli Rethinking feelings An FMRI study of the cognitive regulation of emotion J Cogn Neurosci 14 2002 1215 1229
64. V.E. O'Leary Strength in the face of adversity Individual and social thriving J Soc Issues 54 1998 425 446
65. K.J. Parker, C.L. Buckmaster, A.F. Schatzberg, D.M. Lyons Prospective investigation of stress inoculation in young monkeys Arch Gen Psychiatry 61 2004 933 941
66. K.J. Parker, A.F. Schatzberg, D.M. Lyons Neuroendocrine aspects of hypercortisolism in major depression Horm Behav 43 2003 60 66
67. M.I. Posner, M.K. Rothbart Developing mechanisms of self-regulation Dev Psychopathol 12 2000 427 441
68. A.C. Roberts, J.D. Wallis Inhibitory control and affective processing in the prefrontal cortex Neuropsychological studies in the common marmoset Cereb Cortex 10 2000 252 262
69. M. Rutter Psychosocial resilience and protective mechanisms Am J Orthopsychiatry 57 1987 316 331
70. M.M. Sanchez, E.F. Hearn, D. Do, J.K. Rilling, J.G. Herndon Differential rearing affects corpus callosum size and cognitive function of rhesus monkeys Brain Res 812 1998 38 49
71. A.F. Schatzberg, J.A. Posener, C. DeBattista, B.M. Kalehzan, A.J. Rothschild, P.K. Shear Neuropsychological deficits in psychotic versus nonpsychotic major depression and no mental illness Am J Psychiatry 157 2000 1095 1100
72. H. Selye Stress Without Distress 1974 Lippincott. Philadelphia
73. M. Stacey, R. Dearden, R. Pill, D. Robinson Hospitals, Children and Their Families The Report of a Pilot Study 1970 Routledge and Kegan Paul. London
74. R.M. Sullivan, A. Gratton Prefrontal cortical regulation of hypotha-lamic-pituitary-adrenal function in the rat and implications for psychopathology Side matters Psychoneuroendocrinology 27 2002 99 114
75. S.J. Suomi Early determinants of behaviour Evidence from primate studies Br Med Bull 53 1997 170 184
76. A.C. Tang, B.C. Reeb, R.D. Romeo, B.S. McEwen Modification of social memory, hypothalamic-pituitary-adrenal axis, and brain asymmetry by neonatal novelty exposure J Neurosci 23 2003 8254 8260
77. J.R. Taylor, R.H. Roth, J.R. Sladek Jr, D.E. Redmond Jr Cognitive and motor deficits in the performance of an object retrieval task with a barrier-detour in monkeys (Cercopithecus aethiops sabaeus) treated with MPTP Long-term performance and effect of transparency of the barrier Behav Neurosci 104 1990 564 576
78. C. Trichard, J.L. Martinot, M. Alagille, M.C. Masure, P. Hardy, D. Ginestet Time course of prefrontal lobe dysfunction in severely depressed in-patients A longitudinal neuropsychological study Psychol Med 25 1995 79 85
79. J.D. Wallis, R. Dias, T.W. Robbins, A.C. Roberts Dissociable contributions of the orbitofrontal and lateral prefrontal cortex of the marmoset to performance on a detour reaching task Eur J Neurosci 13 2001 1797 1808
80. J.M. Zeitzer, C.L. Buckmaster, K.J. Parker, C.M. Hauck, D.M. Lyons, E. Mignot Circadian and homeostatic regulation of hypocretin in a primate model Implications for the consolidation of wakefulness J Neurosci 23 2003 3555 3560