Psychoneuroendocrinology
Volume 32, Issue 7 , Pages 785-792 , August 2007

Early life stress and novelty seeking behavior in adolescent monkeys

  • Karen J. Parker

      Affiliations

    • Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, 1201 Welch Road, MSLS Room P104, Mail Code 5485, Stanford, CA 94305-5485, USA
    • Corresponding Author InformationCorresponding author. Tel.: +16507369863; fax: +16504987761.
    • ,
  • Kimberly L. Rainwater

      Affiliations

    • Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, 1201 Welch Road, MSLS Room P104, Mail Code 5485, Stanford, CA 94305-5485, USA
    • ,
  • Christine L. Buckmaster

      Affiliations

    • Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, 1201 Welch Road, MSLS Room P104, Mail Code 5485, Stanford, CA 94305-5485, USA
    • ,
  • Alan F. Schatzberg

      Affiliations

    • Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, 1201 Welch Road, MSLS Room P104, Mail Code 5485, Stanford, CA 94305-5485, USA
    • ,
  • Steven E. Lindley

      Affiliations

    • Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, 1201 Welch Road, MSLS Room P104, Mail Code 5485, Stanford, CA 94305-5485, USA
    • Department of Veterans Affairs, Veterans Administration Palo Alto Health Care System, Palo Alto, CA 94301-1290, USA
    • ,
  • David M. Lyons

      Affiliations

    • Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, 1201 Welch Road, MSLS Room P104, Mail Code 5485, Stanford, CA 94305-5485, USA

Received 1 August 2006 ,Revised 11 May 2007 ,Accepted 16 May 2007.

References 

  1. Agid O, Shapira B, Zislin J, Ritsner M, Hanin B, Murad H, 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;4:163–172
  2. 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
  3. Arnett J. Reckless behavior in adolescence: a developmental perspective. Dev. Rev. 1992;12:339–373
  4. Bacopoulos NG, Redmond DE, Roth RH. Serotonin and dopamine metabolites in brain regions and cerebrospinal fluid of a primate species: effects of ketamine and fluphenazine. J. Neurochem. 1979;32:1215–1218
  5. Baldwin JD. The behavior of squirrel monkeys (Saimiri) in natural environments. In:  Rosenblum LA,  Coe CL editor. Handbook of Squirrel Monkey Research. New York: Plenum Press; 1985;p. 35–53
  6. Bardo MT, Donohew RL, Harrington NG. Psychobiology of novelty seeking and drug seeking behavior. Behav. Brain Res. 1996;77:23–43
  7. Becker JB, Breedlove SM, Crews D, McCarthy MM. Behavioral Endocrinology. second ed. Cambridge, MA: The MIT Press; 2002;
  8. Boinski S, Fragaszy DM. The ontogeny of foraging in squirrel monkeys, Saimiri oerstedi. Anim. Behav. 1989;37:415–428
  9. Brady AG. Research techniques for the squirrel monkey (Saimiri sp.). Ilar. J. 2000;41:10–18
  10. Capitanio JP, Mendoza SP, Lerche NW. Individual differences in peripheral blood immunological and hormonal measures in adult male rhesus macaques (Macaca mulatta): evidence for temporal and situational consistency. Am. J. Primatol. 1998;44:29–41
  11. Dettling AC, Feldon J, Pryce CR. Repeated parental deprivation in the infant common marmoset (Callithrix jacchus, primates) and analysis of its effects on early development. Biol. Psychiatry. 2002;52:1037–1046
  12. Fergus S, Zimmerman MA. Adolescent resilience: a framework for understanding healthy development in the face of risk. Annu. Rev. Public Health. 2005;26:399–419
  13. Forest KB. The interplay of childhood stress and adult life events on women's symptoms of depression. Diss. Abstr. Int. 1991;51:3237
  14. Gerra G, Avanzini P, Zaimovic A, Sartori R, Bocchi C, Timpano M, et al. Neurotransmitters, neuroendocrine correlates of sensation-seeking temperament in normal humans. Neuropsychobiology. 1999;39:207–213
  15. Heim C, Plotsky PM, Nemeroff CB. Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology. 2004;29:641–648
  16. 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
  17. Higley JD, Suomi SJ, Linnoila M. A longitudinal assessment of CSF monoamine metabolite and plasma cortisol concentrations in young rhesus monkeys. Biol. Psychiatry. 1992;32:127–145
  18. 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
  19. Hinde RA, Spencer-Booth Y. Effects of brief separation from mother on rhesus monkeys. Science. 1971;173:111–118
  20. Kabbaj M, Devine DP, Savage VR, Akil H. Neurobiological correlates of individual differences in novelty-seeking behavior in the rat: differential expression of stress-related molecules. J. Neurosci. 2000;20:6983–6988
  21. Kalin NH, Shelton SE, Barksdale CM, Brownfield MS. A diurnal rhythm in cerebrospinal fluid corticotrophin-releasing hormone different from the rhythm of pituitary-adrenal activity. Brain Res. 1987;426:385–391
  22. Kashdan TB, Rose P, Fincham FD. Curiosity and exploration: facilitating positive subjective experiences and personal growth opportunities. J. Pers. Assess. 2004;82:291–305
  23. Kelley AE, Schochet T, Landry CF. Risk taking and novelty seeking in adolescence: introduction to part I. Ann. N Y Acad. Sci. 2004;1021:27–32
  24. Khoshaba DM, Maddi SR. Early experiences in hardiness development. Consult. Psychol. J.: Practice Res. 1999;51:106–116
  25. Komori H, Matsuishi T, Yamada S, Ueda N, Yamashita Y, Kato H. Effect of age on cerebrospinal fluid levels of metabolites of biopterin and biogenic amines. Acta Paediatr. 1999;88:1344–1347
  26. Langlais PJ, Walsh FX, Bird ED, Levy HL. Cerebrospinal fluid neurotransmitter metabolites in neurologically normal infants and children. Pediatrics. 1985;75:580–586
  27. Levine S, Mody T. The long-term psychobiological consequences of intermittent postnatal separation in the squirrel monkey. Neurosci. Biobehav. Rev. 2003;27:83–89
  28. Lindley SE, Gunnet JW, Lookingland KJ, Moore KE. Effects of alterations in the activity of tuberohypophysial dopaminergic neurons on the secretion of alpha-melanocyte stimulating hormone. Proc. Soc. Exp. Biol. Med. 1988;188:282–286
  29. Lyons DM. Conflict as a constructive force in social life. In:  Mason WA,  Mendoza SP editor. Primate Social Conflict. Albany, NY: State University of New York Press; 1993;p. 387–408
  30. Lyons DM, Martel FL, Levine S, Risch NJ, Schatzberg AF. Postnatal experiences and genetic effects on squirrel monkey social affinities and emotional distress. Horm. Behav. 1999;36:266–275
  31. In:  Mason WA editors. Motivational Factors in Psychosocial Development. Lincoln: University of Nebraska Press; 1971;
  32. Mehlman PT, Westergaard GC, Hoos BJ, Sallee FR, Marsh S, Suomi SJ, et al. CSF 5-HIAA and nighttime activity in free-ranging primates. Neuropsychopharmacology. 2000;22:210–218
  33. Mortimer JT, Staff J. Early work as a source of developmental discontinuity during the transition to adulthood. Dev. Psychopathol. 2004;16:1047–1070
  34. Nicotra A, Pierucci F, Parvez H, Senatori O. Monoamine oxidase expression during development and aging. Neurotoxicology. 2004;25:155–165
  35. Parker KJ, Buckmaster CL, Schatzberg AF, Lyons DM. Prospective investigation of stress inoculation in young monkeys. Arch. Gen. Psychiatry. 2004;61:933–941
  36. Parker KJ, Buckmaster CL, Justus KR, Schatzberg AF, Lyons DM. Mild early life stress enhances prefrontal-dependent response inhibition in monkeys. Biol. Psychiatry. 2005;57:848–855
  37. Parker KJ, Buckmaster CL, Sundlass K, Schatzberg AF, Lyons DM. Maternal mediation, stress inoculation, and the development of neuroendocrine stress resistance in primates. Proc. Nat. Acad. Sci. USA. 2006;103:3000–3005
  38. Raleigh MJ, Brammer GL, McGuire MT, Pollack DB, Yuwiler A. Individual differences in basal cisternal cerebrospinal fluid 5-HIAA and HVA in monkeys. The effects of gender, age, physical characteristics, and matrilineal influences. Neuropsychopharmacology. 1992;7:295–304
  39. Reio TG, Petrosko JM, Wiswell AK, Thongsukmag J. The measurement and conceptualization of curiosity. J. Genet. Psychol. 2006;167:117–135
  40. Rind HB, Russo AF, Whittemore SR. Developmental regulation of tryptophan hydroxylase messenger RNA expression and enzyme activity in the raphe and its target fields. Neuroscience. 2000;101:665–677
  41. Roder EL, Timmermans PJ, Vossen JM. Effects of rearing and exposure condition upon the acquisition of phobic behaviour in cynomolgus monkeys. Behav. Res. Ther. 1989;27:221–231
  42. Rosenblum LA. Mother-infant relations and early behavioral development in the squirrel monkey. In:  Rosenblum LA,  Cooper RW editor. The Squirrel Monkey. New York: Academic Press; 1968;p. 207–233
  43. Rutter M. Resilience: some conceptual considerations. J. Adolesc. Health. 1993;14:626–631, 690–626
  44. Sackett G. Exploratory behavior of rhesus monkeys as a function of rearing experiences and sex. Dev. Psychol. 1972;6:260–270
  45. Sara SJ, Dyon-Laurent C, Herve A. Novelty seeking behavior in the rat is dependent upon the integrity of the noradrenergic system. Brain Res. Cogn. Brain Res. 1995;2:181–187
  46. Shelton SE, Kalin NH, Gluck JP, Keresztury MF, Schneider VA, Lewis MH. Effect of age on cisternal cerebrospinal fluid concentrations of monoamine metabolites in nonhuman primates. Neurochem. Int. 1988;13:353–357
  47. Thorsell A, Slawecki CJ, El Khoury A, Mathe AA, Ehlers CL. The effects of social isolation on neuropeptide Y levels, exploratory and anxiety-related behaviors in rats. Pharmacol. Biochem. Behav. 2006;83:28–34
  48. Wada Y, Egashira T, Takayama F, Yamanaka Y, Takada K, Takeda H, et al. Variation of monoamines and their metabolite contents in the cerebrospinal fluid of conscious rats. Jpn J. Pharmacol. 1998;78:237–240
  49. Wester P, Bergstrom U, Eriksson A, Gezelius C, Hardy J, Winblad B. Ventricular cerebrospinal fluid monoamine transmitter and metabolite concentrations reflect human brain neurochemistry in autopsy cases. J. Neurochem. 1990;54:1148–1156
  50. Zeitzer JM, Buckmaster CL, Parker KJ, Hauck CM, Lyons DM, Mignot E. Circadian and homeostatic regulation of hypocretin in a primate model: implications for the consolidation of wakefulness. J. Neurosci. 2003;23:3555–3560
  51. Zuckerman M. Sensation seeking, mania, and monoamines. Neuropsychobiology. 1985;13:121–128

PII: S0306-4530(07)00117-5

doi: 10.1016/j.psyneuen.2007.05.008

Psychoneuroendocrinology
Volume 32, Issue 7 , Pages 785-792 , August 2007

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