Cited by 222

The DOI matches its Crossref record; 9 of the 9 references it cites were found in a registry or an index.

The impact of early adverse care on HPA axis development: Nonhuman primate models

Sanchez, Mar M.·2006·Hormones and Behavior

Abstract

This review presents supporting evidence that early disruptions in mother-infant relationship in primates, including infant maltreatment, are important risk factors for the development of psychopathology and pathophysiology during childhood and adolescence. Current research in this field is trying to identify important aspects of early adverse experiences such as the timing, frequency, duration, "perceived" intensity of the stressful or traumatic events, the role of social support (e.g., nurturing caregiver) in buffering the deleterious outcomes of early adversity, as well as the role of sex and genetic factors on individual variability in vulnerability. The use of nonhuman primate models of early adverse caregiving is helping to put the pieces of the puzzle together to fully understand the causes and consequences of similar experiences in humans. These models are essential to characterize the time course of biobehavioral alterations throughout development, using prospective, longitudinal studies performed under controlled experimental conditions and using invasive approaches that are unrealistic and unethical when studying human populations.

Overview

Integrity signals

Registry

Crossref · 10.1016/j.yhbeh.2006.06.012

Cites

9 of 9 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Show all 9 references

Research works printed but not linked: 76

  1. Andrews, 1991, Attachment in monkey infants raised in variable and low-demand environments, Child Dev., 62, 686, 10.2307/1131170 · DOI
  2. Bowlby, 1968, Effects on behaviour of disruption of an affectional bond, Eugen. Soc. Symp., 4, 94
  3. Bowman, 1965, Plasma 17-OHCS response of the infant rhesus monkey to a non-injurious, noxious stimulus, Proc. Soc. Exp. Biol. Med., 119, 133, 10.3181/00379727-119-30118 · DOI
  4. Boyce, 1995, Salivary cortisol in nursery-reared rhesus monkeys: reactivity to peer interactions and altered circadian activity, Dev. Psychobiol., 28, 257, 10.1002/dev.420280502 · DOI
  5. Bugental, 2003, The hormonal costs of subtle forms of infant maltreatment, Horm. Behav., 43, 237, 10.1016/S0018-506X(02)00008-9 · DOI · Paper page
  6. Capitanio, 1986, Long-term follow up of previously separated pigtail macaques: group and individual differences in response to novel situations, J. Child Psychol. Psychiatry, 27, 531, 10.1111/j.1469-7610.1986.tb00639.x · DOI
  7. Carrion, 2002, Diurnal salivary cortisol in pediatric posttraumatic stress disorder, Biol. Psychiatry, 51, 575, 10.1016/S0006-3223(01)01310-5 · DOI · Paper page
  8. Chrousos, 1998, A healthy body in a healthy mind – and vice versa – the damaging power of “uncontrollable” stress, J. Clin. Endocrinol. Metab., 86, 1842, 10.1210/jc.83.6.1842 · DOI
  9. Cicchetti, 1998, Child abuse and neglect-usefulness of the animal data: comment on Maestripieri and Carroll (1998), Psychol. Bull., 123, 224, 10.1037/0033-2909.123.3.224 · DOI
  10. Cicchetti, 2001, Diverse patterns of neuroendocrine activity in maltreated children, Dev. Psychopathol., 13, 677, 10.1017/S0954579401003145 · DOI
  11. Coe, 1983, Behavioral, not physiological, adaptation to repeated separation in mother and infant primates, Psychoneuroendocrinology, 8, 401, 10.1016/0306-4530(83)90019-7 · DOI
  12. Coe, 1992, Phylogenetic influences on hormone levels across the primate order, Am. J. Primatol., 28, 81, 10.1002/ajp.1350280202 · DOI
  13. Coplan, 1996, Persistent elevations of cerebrospinal fluid concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors: implications for the pathophysiology of mood and anxiety disorders, Proc. Natl. Acad. Sci. U. S. A., 93, 1619, 10.1073/pnas.93.4.1619 · DOI · Paper page
  14. Coplan, 1998, Cerebrospinal fluid concentrations of somatostatin and biogenic amines in grown primates reared by mothers exposed to manipulated foraging conditions, Arch. Gen. Psychiatry, 55, 473, 10.1001/archpsyc.55.5.473 · DOI
  15. Coplan, 2000, Growth hormone response to clonidine in adversely reared young adult primates: relationship to serial cerebrospinal fluid corticotropin-releasing factor concentrations, Psychiatry Res., 95, 93, 10.1016/S0165-1781(00)00173-6 · DOI
  16. De Bellis, 1994, Hypothalamic–pituitary–adrenal axis dysregulation in sexually abused girls, J. Clin. Endocrinol. Metab., 78, 249, 10.1210/jc.78.2.249 · DOI
  17. De Bellis, 1999, AE Bennett research award: developmental traumatology: Part II. Brain development, Biol. Psychiatry, 45, 1271, 10.1016/S0006-3223(99)00045-1 · DOI · Paper page
  18. De Kloet, 1991, Brain corticosteroid receptor balance and homeostatic control, Front. Neuroendocrinol., 12, 95
  19. De Kloet, 1998, Brain corticosteroid receptor balance in health and disease, Endocr. Rev., 19, 269, 10.1210/er.19.3.269 · DOI · Paper page
  20. Dettling, 2002, Repeated parental deprivation in the infant common marmoset (Callithrix jacchus, primates) and analysis of its effects on early development, Biol. Psychiatry, 52, 1037, 10.1016/S0006-3223(02)01460-9 · DOI
  21. Finlay, 1995, Linked regularities in the development and evolution of mammalian brains, Science, 268, 1578, 10.1126/science.7777856 · DOI · Paper page
  22. Glaser, 2000, Child abuse and neglect and the brain—A review, J. Child Psychol. Psychiatry Allied Discipl., 41, 97, 10.1017/S0021963099004990 · DOI · Paper page
  23. Glaser, 2002, Emotional abuse and neglect (psychological maltreatment): a conceptual framework, Child Abuse Negl., 26, 697, 10.1016/S0145-2134(02)00342-3 · DOI
  24. Gunnar, 2001, Low cortisol and a flattening of expected daytime rhythm: potential indices of risk in human development, Dev. Psychopathol., 13, 515, 10.1017/S0954579401003066 · DOI · Paper page
  25. Gunnar, 1996, Stress reactivity and attachment security, Dev. Psychobiol., 29, 10, 10.1002/(SICI)1098-2302(199604)29:3<191::AID-DEV1>3.0.CO;2-M · DOI · Paper page
  26. Hane, A.A., Fox, N.A., 2005. Natural variations in maternal caregiving in human infants. Psychological Science in press.
  27. Harlow, 1965, Total social isolation in monkeys, Proc. Natl. Acad. Sci. U. S. A., 54, 90, 10.1073/pnas.54.1.90 · DOI · Paper page
  28. Harlow, 1971, From thought to therapy: lessons from a primate laboratory, Am. Sci., 59, 538
  29. Hart, 1995, Salivary cortisol in maltreated children: evidence of relations between neuroendocrine activity and social competence, Dev. Psychopathol., 7, 11, 10.1017/S0954579400006313 · DOI
  30. Hart, 1996, Altered neuroendocrine activity in maltreated children related to symptoms of depression, Dev. Psychopathol., 8, 201, 10.1017/S0954579400007045 · DOI · Paper page
  31. Heim, 2001, The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies, Biol. Psychiatry, 49, 1023, 10.1016/S0006-3223(01)01157-X · DOI · Paper page
  32. Heim, 2000, The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders, Psychoneuroendocrinology, 25, 1, 10.1016/S0306-4530(99)00035-9 · DOI · Paper page
  33. Heim, 2001, Altered pituitary–adrenal axis responses to provocative challenge tests in adult survivors of childhood abuse, Am. J. Psychiatry, 158, 575, 10.1176/appi.ajp.158.4.575 · DOI · Paper page
  34. Hennessy, 1986, Multiple, brief maternal separations in the squirrel monkey: changes in hormonal and behavioral responsiveness, Physiol. Behav., 36, 245, 10.1016/0031-9384(86)90011-9 · DOI
  35. Herman, 2003, Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo–pituitary–adrenocortical responsiveness, Front. Neuroendocrinol., 24, 151, 10.1016/j.yfrne.2003.07.001 · DOI · Paper page
  36. Hinde, 1977, Some factors influencing the effects of temporary mother–infant separation: some experiments with rhesus monkeys, Psychol. Med., 7, 197, 10.1017/S0033291700029275 · DOI
  37. Hinde, 1967, The behaviour of socially living rhesus monkeys in their first two and a half years, Anim. Behav., 15, 169, 10.1016/S0003-3472(67)80029-0 · DOI
  38. Johnson, 1996, Effects of early parenting on growth and development in a small primate, Pediatr. Res., 39, 999, 10.1203/00006450-199606000-00012 · DOI
  39. Kaufman, 1991, Depressive disorders in maltreated children, J. Am. Acad. Child Adolesc. Psych., 30, 257, 10.1097/00004583-199103000-00014 · DOI
  40. Kaufman, 1997, The corticotropin-releasing hormone challenge in depressed abused, depressed nonabused, and normal control children, Biol. Psychiatry, 42, 669, 10.1016/S0006-3223(96)00470-2 · DOI · Paper page
  41. Levine, 2005, Developmental determinants of sensitivity and resistance to stress, Psychoneuroendocrinology, 30, 939, 10.1016/j.psyneuen.2005.03.013 · DOI · Paper page
  42. Levine, 2003, The long-term psychobiological consequences of intermittent postnatal separation in the squirrel monkey, Neurosci. Biobehav. Rev., 27, 83, 10.1016/S0149-7634(03)00011-3 · DOI · Paper page
  43. Levitt, 2003, Structural and functional maturation of the developing primate brain, J. Pediatr., 243, S35, 10.1067/S0022-3476(03)00400-1 · DOI
  44. Luecken, 2004, Early caregiving and physiological stress responses, Clin. Psychol. Rev., 24, 171, 10.1016/j.cpr.2004.01.003 · DOI
  45. Lyons, 2000, Early environment regulation of glucocorticoid feedback sensitivity in young adult monkeys, J. Neuroendocrinol., 12, 723, 10.1046/j.1365-2826.2000.00505.x · DOI
  46. Maestripieri, 1998, Parenting styles of abusive mothers in group-living rhesus macaques, Anim. Behav., 55, 1, 10.1006/anbe.1997.0578 · DOI
  47. Maestripieri, 1999, The biology of human parenting: insights from nonhuman primates, Neurosci. Biobehav. Rev., 23, 411, 10.1016/S0149-7634(98)00042-6 · DOI
  48. Maestripieri, 2005, Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys, Proc. Natl. Acad. Sci. U. S. A., 102, 9726, 10.1073/pnas.0504122102 · DOI
  49. Maestripieri, 1998, Behavioral and environmental correlates of infant abuse in group-living pigtail macaques, Infant Behav. Dev., 21, 603, 10.1016/S0163-6383(98)90032-7 · DOI
  50. Maestripieri, 1998, Risk factors for infant abuse and neglect in group-living rhesus monkeys, Psychol. Sci., 9, 143, 10.1111/1467-9280.00027 · DOI
  51. Maestripieri, 2000, Causes and consequences of infant abuse and neglect in monkeys, Aggress. Violent Behav., 5, 245, 10.1016/S1359-1789(98)00019-6 · DOI
  52. Maestripieri, 1997, Genealogical and demographic influences on infant abuse and neglect in group-living sooty mangabeys (Cercocebus atys), Dev. Psychobiol., 31, 175, 10.1002/(SICI)1098-2302(199711)31:3<175::AID-DEV2>3.0.CO;2-P · DOI
  53. Maestripieri, 1997, Infant abuse runs in families of group-living pigtail macaques, Child Abuse Negl., 21, 465, 10.1016/S0145-2134(97)00006-9 · DOI
  54. Maestripieri, 2000, Crying and infant abuse in rhesus monkeys, Child Dev., 71, 301, 10.1111/1467-8624.00145 · DOI
  55. McCormack, K.M., Sanchez, M.M., Bardi, M., Maestripieri, D., in press. Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6 months of life. Dev. Psychobiol. 48 (6). · DOI · Paper page
  56. Patel, 2000, Glucocorticoid and mineralocorticoid receptor mRNA expression in squirrel monkey brain, J. Psychiatr. Res., 34, 383, 10.1016/S0022-3956(00)00035-2 · DOI · Paper page
  57. Pruessner, 1997, Free cortisol levels after awakening: a reliable biological marker for the assessment of adrenocortical activity, Life Sci., 61, 2539, 10.1016/S0024-3205(97)01008-4 · DOI · Paper page
  58. Pryce, 2005, Postnatal ontogeny of hippocampal expression of the mineralocorticoid and glucocorticoid receptors in the common marmoset monkey, Eur. J. Neurosci., 21, 1521, 10.1111/j.1460-9568.2005.04003.x · DOI
  59. Pryce, 2005, Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research, Neurosci. Biobehav. Rev., 29, 649, 10.1016/j.neubiorev.2005.03.011 · DOI
  60. Rilling, 2001, Neural correlates of maternal separation in rhesus monkeys, Biol. Psychiatry, 49, 146, 10.1016/S0006-3223(00)00977-X · DOI
  61. Rosenblum, 1994, Influences of environmental demand on maternal behavior and infant development, Acta Paediatr., Suppl., 397, 57, 10.1111/j.1651-2227.1994.tb13266.x · DOI
  62. Rosenfeld, 1988, Ontogeny of type I and type II corticosteroid receptors in the rat hippocampus, Dev. Brain Res., 42, 113, 10.1016/0165-3806(88)90206-4 · DOI
  63. Rosenfeld, 1992, Multifactorial regulation of the hypothalamic–pituitary–adrenal axis during development, Neurosci. Biobehav. Rev., 16, 553, 10.1016/S0149-7634(05)80196-4 · DOI
  64. Roy, 2002, Urinary free cortisol and childhood trauma in cocaine dependent adults, J. Psychiatr. Res., 36, 173, 10.1016/S0022-3956(02)00002-X · DOI
  65. Sanchez, 1999, Autoradiographic and in situ hybridization localization of corticotropin-releasing factor 1 and 2 receptors in nonhuman primate brain, J. Comp. Neurol., 408, 365, 10.1002/(SICI)1096-9861(19990607)408:3<365::AID-CNE5>3.0.CO;2-N · DOI · Paper page
  66. Sanchez, 2000, Distribution of corticosteroid receptors in the rhesus brain: relative absence of glucocorticoid receptors in the hippocampal formation, J. Neurosci., 20, 4657, 10.1523/JNEUROSCI.20-12-04657.2000 · DOI · Paper page
  67. Sanchez, 2001, Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models, Dev. Psychopathol., 13, 419, 10.1017/S0954579401003029 · DOI · Paper page
  68. Sanchez, 2005, Alterations in diurnal cortisol rhythm and acoustic startle response in non-human primates with adverse rearing, Biol. Psychiatry, 57, 373, 10.1016/j.biopsych.2004.11.032 · DOI · Paper page
  69. Schmidt, 2003, The postnatal development of the hypothalamic–pituitary–adrenal axis in the mouse, Int. J. Dev. Neurosci., 21, 125, 10.1016/S0736-5748(03)00030-3 · DOI
  70. Sephton, 2000, Diurnal cortisol rhythm as a predictor of breast cancer survival, J. Natl. Cancer Inst., 92, 994, 10.1093/jnci/92.12.994 · DOI · Paper page
  71. Suchecki, 1993, Effects of maternal deprivation on the ACTH stress response in the infant rat, Neuroendocrinology, 57, 204, 10.1159/000126361 · DOI
  72. Suomi, 2005, Mother–infant attachment, peer relationships, and the development of social networks in rhesus monkeys, Hum. Dev., 48, 67, 10.1159/000083216 · DOI
  73. Troisi, 1984, Ambivalence in monkey mothering: infant abuse combined with maternal possessiveness, J. Nerv. Ment. Dis., 172, 105, 10.1097/00005053-198402000-00007 · DOI
  74. Van Eekelen, 1991, Postnatal ontogeny of mineralocorticoid and glucocorticoid receptor gene expression in regions of the rat and diencephalon, Dev. Brain Res., 61, 33, 10.1016/0165-3806(91)90111-U · DOI
  75. Whitnall, 2001, Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system, Prog. Neurobiol., 40, 573, 10.1016/0301-0082(93)90035-Q · DOI · Paper page
  76. Yehuda, 2001, Childhood trauma and risk for PTSD: relationship to intergenerational effects of trauma, parental PTSD, and cortisol excretion, Dev. Psychopathol., 13, 733, 10.1017/S0954579401003170 · DOI · Paper page

Cited by

Sorted by citations

Metadata

Authors
Sanchez, M. M.
Venue
Hormones and Behavior
Publisher
Elsevier BV
Published
2006-11
Volume
50
Issue
4
Pages
623-631
ISSN
0018-506X
Cited by
222
References
9
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review