Psychoneuroendocrinology
Volume 34, Issue 7 , Pages 1029-1040 , August 2009

Early adverse rearing experiences alter sleep–wake patterns and plasma cortisol levels in juvenile rhesus monkeys

  • Catherine E. Barrett

      Affiliations

    • Mood and Anxiety Disorders Program, National Institute of Mental Health, Bethesda, MD 20892, United States
    • ,
  • Pamela Noble

      Affiliations

    • Primate Core Facility, National Institute of Mental Health, Poolesville, MD 20842, United States
    • ,
  • Erin Hanson

      Affiliations

    • Primate Core Facility, National Institute of Mental Health, Poolesville, MD 20842, United States
    • ,
  • Daniel S. Pine

      Affiliations

    • Mood and Anxiety Disorders Program, National Institute of Mental Health, Bethesda, MD 20892, United States
    • ,
  • James T. Winslow

      Affiliations

    • Mood and Anxiety Disorders Program, National Institute of Mental Health, Bethesda, MD 20892, United States
    • Primate Core Facility, National Institute of Mental Health, Poolesville, MD 20842, United States
    • ,
  • Eric E. Nelson

      Affiliations

    • Mood and Anxiety Disorders Program, National Institute of Mental Health, Bethesda, MD 20892, United States
    • Corresponding Author InformationCorresponding author.

Received 28 March 2008 ,Revised 5 February 2009 ,Accepted 5 February 2009.

References 

  1. Ancoli-Israel S, Cole R, Alessi C, Chambers M, Moorcroft W, Pollak CP. The role of actigraphy in the study of sleep and circadian rhythms. Sleep. 2003;26:342–392
  2. American Psychiatric Association. Diagnostic and statistical manual of mental disorders. American Psychiatric Press; 1994;
  3. Barr CS, Newman TK, Lindell S, Shannon C, Champoux M, Lesch KP, 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
  4. Barr CS, Newman TK, Shannon C, Parker C, Dvoskin RL, Becker ML, et al. Rearing condition and rh5-HTTLPR interact to influence limbic-hypothalamic-pituitary-adrenal axis response to stress in infant macaques. Biol. Psychiatry. 2004;55:733–738
  5. Bastian ML, Sponberg AC, Sponberg AC, Suomi SJ, Higley JD. Long-term effects of infant rearing condition on the acquisition of dominance rank in juvenile and adult rhesus macaques (Macaca mulatta). Dev. Psychobiol. 2003;42:44–51
  6. Benca RM, Obermeyer WH, Shelton SE, Droster J, Kalin NH. Effects of amygdala lesions on sleep in rhesus monkeys. Brain Res. 2000;879:130–138
  7. Bennett AJ, Lesch KP, Heils A, Long JC, Lorenz JG, Shoaf SE, et al. Early experience and serotonin transporter gene variation interact to influence primate CNS function. Mol. Psychiatry. 2002;7:118–122
  8. Buckley TM, Schatzberg AF. Review: on the interactions of the hypothalamic–pituitary–adrenal (HPA) axis and sleep: normal HPA axis activity and circadian rhythm, exemplary sleep disorders. J. Clin. Endocrin. Metab.: Clin. Exp. 2005;90:3106–3114
  9. Caldji C, Diorio J, Meaney MJ. Variations in maternal care in infancy regulate the development of stress reactivity. Biol. Psychiatry. 2000;48:1164–1174
  10. Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H, et al. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science. 2003;301:386–389
  11. Champoux M, Coe CL, Schanberg SM, Kuhn CM, Suomi SJ. Hormonal effects of early rearing conditions in the infant rhesus monkey. Am. J. Primatol. 1989;19:111–117
  12. Dahl RE, Ryan ND, Puig-Antich J, Nguyen NA, al-Shabbout M, Meyer VA, et al. 24-hour cortisol measures in adolescents with major depression: a controlled study. Biol. Psychiatry. 1991;30:25–36
  13. Davis EP, Bruce J, Gunnar MR. The anterior attention network: associations with temperament and neuroendocrine activity in 6-year-old children. Dev. Psychobiol. 2002;40:43–56
  14. De Kloet ER, Oltzl MS, Joels M. Stress and cognition: are corticosteroids good or bad guys?. Trends Neurosci. 1999;22:422–426
  15. El-Sheikh M, Buckhalt JA, Keller PS, Granger DA. Children's objective and subjective sleep disruptions: links with afternoon cortisol levels. Health Psychol. 2008;27:26–33
  16. Goodyer IM, Herbert J, Altham PM, Pearson J, Secher SM, Shiers HM. Adrenal secretion during major depression in 8- to 16-year-olds. I. Altered diurnal rhythms in salivary cortisol and dehydroepiandrosterone (DHEA) at presentation. Psychol. Med. 1996;26:245–256
  17. Hatzinger M, Brand S, Perren S, Stadelmann S, von Wyl A, von Klitzing K, et al. Electroencephalographic sleep profles and hypothalamic–pituitary–adrenocortical (HPA)-activity in kindergarten children: early indication of poor sleep quality associated with increase cortisol secretion. J. Psychiat. Res. 2008;42:542–543
  18. 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
  19. Higley JD, Suomi SJ, Linnoila M. A nonhuman primate model of type II alcoholism? Part 2. Diminished social competence and excessive aggression correlates with low cerebrospinal fluid 5-hydroxyindoleacetic acid concentrations. Alcohol. Clin. Exp. Res. 1996;20:643–650
  20. Hsieh KC, Robinson EL, Fuller CA. Sleep architecture in unrestrained rhesus onkeys (Macaca mulatta) synchronized to 24-hour light-dark cycles. Sleep. 2008;31:1239–1250
  21. Ichise M, Vines DC, Gura T, Anderson GM, Suomi SJ, Higley JD, et al. Effects of early life stress on [11C]DASB positron emission tomography imaging of serotonin transporters in adolescent peer- and mother-reared rhesus monkeys. J. Neurosci. 2006;26:4638–4643
  22. Ivanenko A, Crabtree VM, Gozal D. Sleep and depression in children and adolescents. Sleep Med. Rev. 2005;9:115–129
  23. Jans LA, Riedel WJ, Markus CR, Blokland A. Serotonergic vulnerability and depression: assumptions, experimental evidence and implications. Mol. Psychiatry. 2007;12:522–543
  24. Kaemingk K, Reite M. Social environment and nocturnal sleep: studies in peer-reared monkeys. Sleep. 1987;10:542–550
  25. Knowles JB, MacLean AW. Age-related changes in sleep in depressed and healthy subjects: a meta-analysis. Neuropsychopharmacology. 1990;3:251–259
  26. Kushida CA, Chang A, Gadkary C, Guilleminault C, Carrillo O, Dement WC. Comparison of actigraphic, polysomnographic, and subjective assessment of sleep parameters in sleep-disordered patients. Sleep Med. 2001;2:389–396
  27. Levine S. Primary social relationships influence the development of the hypothalamic–pituitary–adrenal axis in the rat. Physiol. Behav. 2001;73:255–260
  28. Lupien SJ, McEwen BS. The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Res. Rev. 1997;24:1–27
  29. Markov D, Goldman M. Normal sleep and circadian rhythms: neurobiologic mechanisms underlying sleep and wakefulness. Psychiatr. Clin. North Am. 2006;29:841–853(abstract vii)
  30. 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
  31. Mellman TA. Sleep and anxiety disorders. Psychiatr. Clin. North Am. 2006;29:1047–1058(abstract x)
  32. Oakley, N.R., 1997. Validation with polysomnography of the sleep-watch sleep/wake scoring algorithm used by the actiwatch activity monitoring system. Technical report to Mini Mitter Co., Inc.
  33. Papailiu A, Sullivan E, Cameron JL. Behaviors in rhesus monkeys (Macaca mulatta) associated with activity counts measured with accelerometer. Am. J. Primatol. 2007;69:1–9
  34. Parr LA, Winslow JT, Davis M. Rearing experience differentially affects somatic and cardiac startle responses in rhesus monkeys (Macaca mulatta). Behav. Neurosci. 2002;51:859–866
  35. Peterson MJ, Benca RM. Sleep in mood disorders. Psychiatr. Clin. North Am. 2006;29:1009–1032abstract ix
  36. Pine DS, Helfenstein SM, Bar-Haim Y, Nelson EE, Fox NA. Challenges for developing novel treatments for childhood disorders: lessons form research in anxiety. Neuropsychopharmacology. 2009;34:213–228
  37. Prather MD, Lavenex P, Mauldin-Jourdain ML, Mason WA, Capitanio JP, Mendoza SP, et al. Increased social fear and decreased fear of objects in monkeys with neonatal amygdala lesions. Neuroscience. 2001;106:653–658
  38. Reite MD, Short MS. Nocturnal sleep in separated monkey infants. Arch. Gen. Psychiatry. 1978;1247–1253
  39. Rutter M, O’Connor TG. Are there biological programming effects for psychological development? Findings from a study of Romanian adoptees. Dev. Psychol. 2004;40:81–94
  40. Sabatini MJ, Ebert P, Lewis DA, Levitt P, Cameron JL, Mirnics K. Amygdala gene expression correlates of social behavior in monkeys experiencing maternal separation. J. Neurosci. 2007;27:3295–3304
  41. Sadeh A, Hauri PJ, Kripke DF, Lavie P. The role of actigraphy in the evaluation of sleep disorders. Sleep. 1995;18:288–302
  42. Sadeh A, Acebo C. The role of actigraphy in sleep medicine. Sleep Med. Rev. 2002;6:113–124
  43. Sanchez MM. The impact of early adverse care on HPA axis development: nonhuman primate models. Horm. Behav. 2006;50:623–631
  44. Sanchez MM, Ladd CO, Plotsky PM. Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev. Psychopathol. 2001;13:419–449
  45. Sanchez MM, Noble PM, Lyon CK, Plotsky PM, Davis M, Nemeroff CB, et al. Alterations in diurnal cortisol rhythm and acoustic startle response in nonhuman primates with adverse rearing. Biol. Psychiatry. 2005;57:373–381
  46. Shannon C, Champoux M, Suomi SJ. Rearing condition and plasma cortisol in rhesus monkey infants. Am. J. Primatol. 1998;46:311–321
  47. Shannon C, Schwandt ML, Champoux M, Shoaf SE, Suomi SJ, Linnoila 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
  48. Southwick SM, Vythilingam M, Charney DS. The psychobiology of depression and resilience to stress: implications for prevention and treatment. Annu. Rev. Clin. Psychol. 2005;1:255–291
  49. Sri Kantha S, Suzuki J. Sleep quantitation in common marmoset, cotton top tamarin and squirrel monkey by non-invasive actigraphy. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2006;144:203–210
  50. Steiger A. Sleep and the hypothalamo–pituitary–adrenocortical system. Sleep Med. Rev. 2002;6:125–138
  51. Steiger A. Neurochemical regulation of sleep. J Psychiatr Res. 2007;41:537–552
  52. Suomi SJ. Early stress and adult emotional reactivity in rhesus monkeys. Ciba Found Symp. 1991;156:171–183(discussion 183-8)
  53. Winslow JT. Neuropeptides and non-human primate social deficits associated with pathogenic rearing experience. Int. J. Dev. Neurosci. 2005;23:245–251
  54. Zajicek KB, Higley JD, Suomi SJ, Linnoila M. Rhesus macaques with high CSF 5-HIAA concentrations exhibit early sleep onset. Psychiatry Res. 1997;73:15–25
  55. Zalsman G, Oquendo MA, Greenhill L, Goldberg PH, Kamali M, Martin A, et al. Neurobiology of depression in children and adolescents. Child Adolesc. Psychiatr. Clin. N. Am. 2006;15:843–868(vii–viii)
  56. Zhdanova IV, Geiger DA, Schwagerl AL, Leclair OU, Killiany R, Taylor JA, et al. Melatonin promotes sleep in three species of diurnal nonhuman primates. Physiol. Behav. 2002;75:523–529

PII: S0306-4530(09)00054-7

doi: 10.1016/j.psyneuen.2009.02.002

Psychoneuroendocrinology
Volume 34, Issue 7 , Pages 1029-1040 , August 2009

Article Tools

* Image Usage & Resolution