Journal of the American Academy of Child & Adolescent Psychiatry
Volume 48, Issue 2 , Pages 114-127 , February 2009

Risk and Resilience: Early Manipulation of Macaque Social Experience and Persistent Behavioral and Neurophysiological Outcomes

,Accepted 27 August 2008.

References 

  1. Bowlby J . Attachment . New York: Basic Books; 1982;
  2. Rutter M . Some research considerations on intergenerational continuities and discontinuities: comment on the special section . Dev Psychol . 1998;34:1269–1273
  3. Ruppenthal GC , Arling GL , Harlow HF , Sackett GP , Suomi SJ . A 10-year perspective of motherless-mother monkey behavior . J Abnorm Psychol . 1976;85:341–349
  4. Moffitt TE , Caspi A , Rutter M . Strategy for investigating interactions between measured genes and measured environments . Arch Gen Psychiatry . 2005;62:473–481
  5. Newport DJ , Stowe ZN , Nemeroff CB . Parental depression: animal models of an adverse life event . Am J Psychiatry . 2002;159:1265–1283
  6. Suomi SJ . Aggression and social behaviour in rhesus monkeys . Novartis Found Symp . 2005;268:216–222
  7. Adler NE . Health disparities: what's optimism got to do with it? . J Adolesc Health . 2007;40:106–107
  8. Suomi SJ . Early determinants of behaviour: evidence from primate studies . Br Med Bull . 1997;53:170–184
  9. Seifer R , Sameroff AJ , Barrett LC , Krafchuk E . Infant temperament measured by multiple observations and mother report . Child Dev . 1994;65:1478–1490
  10. Suomi SJ . Gene-environment interactions and the neurobiology of social conflict . Ann N Y Acad Sci . 2003;1008:132–1329
  11. Clarke AS , Kraemer GW , Kupfer DJ . Effects of rearing condition on HPA axis response to fluoxetine and desipramine treatment over repeated social separations in young rhesus monkeys . Psychiatry Res . 1998;79:91–104
  12. Fox NA , Henderson HA , Marshall PJ , Nichols KE , Ghera MM . Behavioral inhibition: linking biology and behavior within a developmental framework . Annu Rev Psychol . 2005;56:235–262
  13. Hirshfeld DR , Rosenbaum JF , Biederman J , et al.   Stable behavioral inhibition and its association with anxiety disorder . J Am Acad Child Adolesc Psychiatry . 1992;31:103–111
  14. Higley JD , King ST , Hasert MF , Champoux M , Suomi SJ , Linnoila M . Stability of interindividual differences in serotonin function and its relationship to severe aggression and competent social behavior in rhesus macaque females . Neuropsychopharmacology . 1996;14:67–76
  15. Saudino KJ . Behavioral genetics and child temperament . J Dev Behav Pediatr . 2005;26:214–223
  16. Rasmussen KLR , Timme A , Suomi SJ . Comparison of physiological measures of Cayo Santiago rhesus monkey females with and between social groups . Primate Rep . 1997;47:49–55
  17. Higley JD , Mehlman PT , Poland RE , et al.   CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors . Biol Psychiatry . 1996;40:1067–1082
  18. Placidi GP , Oquendo MA , Malone KM , Huang YY , Ellis SP , Mann JJ . Aggressivity, suicide attempts, and depression: relationship to cerebro-spinal fluid monoamine metabolite levels . Biol Psychiatry . 2001;50:783–791
  19. Champoux M , Suomi SJ , Schneider ML . Temperament differences between captive Indian and Chinese-Indian hybrid rhesus macaque neonates . Lab Anim Sci . 1994;44:351–357
  20. Caspi A , Henry B , McGee RO , Moffitt TE , Silva PA . Temperamental origins of child and adolescent behavior problems: from age three to age fifteen . Child Dev . 1995;66:55–68
  21. Harlow HF . The nature of love . Am Psychol . 1958;13:673–685
  22. Harlow HF , Dodsworth RO , Harlow MK . Total social isolation in monkeys . Proc Natl Acad Sci U S A . 1965;54:90–97
  23. Clarke AS , Hedeker DR , Ebert MH , Schmidt DE , McKinney WT , Kraemer GW . Rearing experience and biogenic amine activity in infant rhesus monkeys . Biol Psychiatry . 1996;40:338–352
  24. Suomi SJ . Early stress and adult emotional reactivity in rhesus monkeys . Ciba Found Symp . 1991;156:171–183
  25. Meyer JS , Novak MA , Bowman RE , Harlow HF . Behavioral and hormonal effects of attachment object separation in surrogate-peer-reared and mother-reared infant rhesus monkeys . Dev Psychobiol . 1975;8:425–435
  26. Suomi SJ . Risk, resilience, and gene x environment interactions in rhesus monkeys . Ann N Y Acad Sci . 2006;1094:52–62
  27. Kraemer GW , McKinney WT . Interactions of pharmacological agents which alter biogenic amine metabolism and depression—an analysis of contributing factors within a primate model of depression . J Affect Disord . 1979;1:33–54
  28. Kraemer GW , Ebert MH , Schmidt DE , McKinney WT . Strangers in a strange land: a psychobiological study of infant monkeys before and after separation from real or inanimate mothers . Child Dev . 1991;62:548–566
  29. Higley JD , Suomi SJ , Linnoila M . CSF monoamine metabolite concentrations vary according to age, rearing, and sex, and are influenced by the stressor of social separation in rhesus monkeys . Psychopharmacology (Berl) . 1991;103:551–556
  30. Shannon C , Champoux M , Suomi SJ . Rearing condition and plasma cortisol in rhesus monkey infants . Am J Primatol . 1998;46:311–321
  31. Fahlke C , Lorenz JG , Long J , Champoux M , Suomi SJ , Higley JD . Rearing experiences and stress-induced plasma cortisol as early risk factors for excessive alcohol consumption in nonhuman primates . Alcohol Clin Exp Res . 2000;24:644–650
  32. Higley JD , Mehlman PT , Taub DM , et al.   Cerebrospinal fluid monoamine and adrenal correlates of aggression in free-ranging rhesus monkeys . Arch Gen Psychiatry . 1992;49:436–441
  33. Clarke AS , Ebert MH , Schmidt DE , McKinney WT , Kraemer GW . Biogenic amine activity in response to fluoxetine and desipramine in differentially reared rhesus monkeys . Biol Psychiatry . 1999;46:221–228
  34. Ginsberg SD , Hof PR , McKinney WT , Morrison JH . The noradrenergic innervation density of the monkey paraventricular nucleus is not altered by early social deprivation . Neurosci Lett . 1993;158:130–134
  35. Laudenslager ML , Clarke AS . Antidepressant treatment during social challenge prior to 1 year of age affects immune and endocrine responses in adult macaques . Psychiatry Res . 2000;95:25–34
  36. Laudenslager ML , Berger CL , Boccia ML , Reite ML . Natural cytotoxicity toward K562 cells by macaque lymphocytes from infancy through puberty: effects of early social challenge . Brain Behav Immun . 1996;10:275–287
  37. Lubach GR , Coe CL , Ershler WB . Effects of early rearing environment on immune responses of infant rhesus monkeys . Brain Behav Immun . 1995;9:31–46
  38. Lewis MH , Gluck JP , Petitto JM , Hensley LL , Ozer H . Early social deprivation in nonhuman primates: long-term effects on survival and cell-mediated immunity . Biol Psychiatry . 2000;47:119–126
  39. Coe CL , Lubach GR , Ershler WB , Klopp RG . Influence of early rearing on lymphocyte proliferation responses in juvenile rhesus monkeys . Brain Behav Immun . 1989;3:47–60
  40. Coe CL , Lubach GR , Schneider ML , Dierschke DJ , Ershler WB . Early rearing conditions alter immune responses in the developing infant primate . Pediatrics . 1992;90:505–509
  41. Shannon C , Schwandt ML , Champoux M , et al.   Maternal absence and stability of individual differences in CSF 5-HIAA concentrations in rhesus monkey infants . Am J Psychiatry . 2005;162:1658–1664
  42. Sanchez MM , Hearn EF , Do D , Rilling JK , Herndon JG . Differential rearing affects corpus callosum size and cognitive function of rhesus monkeys . Brain Res . 1998;812:38–49
  43. Huot RL , Plotsky PM , Lenox RH , McNamara RK . Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats . Brain Res . 2002;950:52–63
  44. Rosenblum LA , Paully GS . The effects of varying environmental demands on maternal and infant behavior . Child Dev . 1984;55:305–314
  45. Andrews MW , Rosenblum LA . Attachment in monkey infants raised in variable- and low-demand environments . Child Dev . 1991;62:686–693
  46. Andrews MW , Rosenblum LA . Assessment of attachment in differentially reared infant monkeys (Macaca radiata): response to separation and a novel environment . J Comp Psychol . 1993;107:84–90
  47. Andrews MW , Rosenblum LA . The development of affiliative and agonistic social patterns in differentially reared monkeys . Child Dev . 1994;65:1398–1404
  48. Rosenblum LA , Forger C , Noland S , Trost RC , Coplan JD . Response of adolescent bonnet macaques to an acute fear stimulus as a function of early rearing conditions . Dev Psychobiol . 2001;39:40–45
  49. Coplan JD , Andrews MW , Rosenblum LA , et al.   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 . 1996;93:1619–1623
  50. Coplan JD , Altemus M , Mathew SJ , et al.   Synchronized maternal-infant elevations of primate CSF CRF concentrations in response to variable foraging demand . CNS Spectr . 2005;10:530–536
  51. Rosenblum LA , Coplan JD , Friedman S , Bassoff T , Gorman JM , Andrews MW . Adverse early experiences affect noradrenergic and serotonergic functioning in adult primates . Biol Psychiatry . 1994;35:221–227
  52. Coplan JD , Smith EL , Trost RC , et al.   Growth hormone response to clonidine in adversely reared young adult primates: relationship to serial cerebrospinal fluid corticotropin-releasing factor concentrations . Psychiatry Res . 2000;95:93–102
  53. Coplan JD , Trost RC , Owens MJ , et al.   Cerebrospinal fluid concentrations of somatostatin and biogenic amines in grown primates reared by mothers exposed to manipulated foraging conditions . Arch Gen Psychiatry . 1998;55:473–477
  54. Smith EL , Batuman OA , Trost RC , Coplan JD , Rosenblum LA . Transforming growth factor-beta 1 and cortisol in differentially reared primates . Brain Behav Immun . 2002;16:140–149
  55. Kaufman D , Banerji MA , Shorman I , et al.   Early-life stress and the development of obesity and insulin resistance in juvenile bonnet macaques . Diabetes . 2007;56:1382–1386
  56. Mathew SJ , Shungu DC , Mao X , et al.   A magnetic resonance spectroscopic imaging study of adult nonhuman primates exposed to early-life stressors . Biol Psychiatry . 2003;54:727–735
  57. Czeh B , Michaelis T , Watanabe T , et al.   Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine . Proc Natl Acad Sci U S A . 2001;98:12796–12801
  58. Coplan JD , Smith EL , 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
  59. Kaufman J , Yang BZ , Douglas-Palumberi H , et al.   Brain-derived neurotrophic factor-5-HTTLPR gene interactions and environmental modifiers of depression in children . Biol Psychiatry . 2006;59:673–680
  60. Jaffee SR , Price TS . Gene-environment correlations: a review of the evidence and implications for prevention of mental illness . Mol Psychiatry . 2007;12:432–442
  61. Higley JD , Bennett A , Heils A , et al.   Early rearing and genotypic influences on CNS serotonin and behavior in nonhuman primates . Biol Psychiatry . 2000;47:S10–S11
  62. Bennett AJ , Lesch KP , Heils A , et al.   Early experience and serotonin transporter gene variation interact to influence primate CNS function . Mol Psychiatry . 2002;7:118–122
  63. Champoux M , Bennett A , Shannon C , Higley JD , Lesch KP , Suomi SJ . Serotonin transporter gene polymorphism, differential early rearing, and behavior in rhesus monkey neonates . Mol Psychiatry . 2002;7:1058–1063
  64. Barr CS , Newman TK , Becker ML , et al.   The utility of the non-human primate; model for studying gene by environment interactions in behavioral research . Genes Brain Behav . 2003;2:336–340
  65. Barr CS , Newman TK , Schwandt M , et al.   Sexual dichotomy of an interaction between early adversity and the serotonin transporter gene promoter variant in rhesus macaques . Proc Natl Acad Sci U S A . 2004;101:12358–12363
  66. Barr CS , Newman TK , Shannon C , et al.   Rearing condition and rh5-HTTLPR interact to influence limbic-hypothalamic-pituitary-adrenal axis response to stress in infant macaques . Biol Psychiatry . 2004;55(7):733–738
  67. Barr CS , Newman TK , Becker ML , et al.   Serotonin transporter gene variation is associated with alcohol sensitivity in rhesus macaques exposed to early-life stress . Alcohol Clin Exp Res . 2003;27:812–817
  68. Barr CS , Newman TK , Lindell S , et al.   Interaction between serotonin transporter gene variation and rearing condition in alcohol preference and consumption in female primates . Arch Gen Psychiatry . 2004;61:1146–1152
  69. Newman TK , Syagailo YV , Barr CS , et al.   Monoamine oxidase A gene promoter variation and rearing experience influences aggressive behavior in rhesus monkeys . Biol Psychiatry . 2005;57:167–172
  70. Nilsson KW , Sjoberg RL , Damberg M , et al.   Role of monoamine oxidase A genotype and psychosocial factors in male adolescent criminal activity . Biol Psychiatry . 2006;59:121–127
  71. Kaffman A , Meaney MJ . Neurodevelopmental sequelae of postnatal maternal care in rodents: clinical and research implications of molecular insights . J Child Psychol Psychiatry . 2007;48:224–244
  72. Suomi SJ . How gene-environment interactions shape biobehavioral development: lessons from studies with rhesus monkeys . Res Hum Dev . 2004;1:205–222
  73. Berman CM , Ionica CS , Li J . Dominance style among Macaca thibetana on Mt. Huangshan, China . Int J Primatol . 2004;25:1283–1312
  74. Wendland JR , Lesch KP , Newman TK , et al.   Differential functional variability of serotonin transporter and monoamine oxidase a genes in macaque species displaying contrasting levels of aggression-related behavior . Behav Genet . 2006;36:163–172
  75. Rutter M , O'Connor TG , English and Romanian Adoptees (ERA) Study Team  . Are there biological programming effects for psychological development? Findings from a study of Romanian adoptees . Dev Psychol . 2004;40:81–94
  76. Chugani HT , Behen ME , Muzik O , Juhász C , Nagy F , Chugani DC . Local brain functional activity following early deprivation: a study of post-institutionalized Romanian orphans . Neuroimage . 2001;14:1290–1301
  77. Kotch JB , Lewis T , Hussey JM , et al.   Importance of early neglect for childhood aggression . Pediatrics . 2008;121:725–731
  78. 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;18:651–677
  79. Harlow HF , Suomi SJ . Social recovery by isolation-reared monkeys . Proc Natl Acad Sci U S A . 1971;68:1534–1538
  80. Gershoff ET , Aber JL , Raver CC , Lennon MC . Income is not enough: incorporating material hardship into models of income associations with parenting and child development . Child Dev . 2007;78:70–95

 This article was reviewed under and accepted by Associate Editor James J. Hudziak, M.D.Financial support was provided by Yale Child Study Center Albert J. Solnit Integrated Training Program.The authors thank Jean Adnopoz, Joseph Woolston, and Linda Mayes for collaboration in organizing conferences on the topic covered in this review.

PII: S0890-8567(09)60005-8

doi: 10.1097/CHI.0b013e318193064c

Journal of the American Academy of Child & Adolescent Psychiatry
Volume 48, Issue 2 , Pages 114-127 , February 2009