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Effects of sex and early maternal abuse on adrenocorticotropin hormone and cortisol responses to the corticotropin-releasing hormone challenge during the first 3 years of life in group-living rhesus monkeys

Published online by Cambridge University Press:  26 January 2010

Mar M. Sanchez ,
Kai Mccormack ,
Alison P. Grand ,
Richelle Fulks ,
Anne Graff  and
Dario Maestripieri
Mar M. Sanchez
Affiliation:
Emory University
Kai Mccormack
Affiliation:
Emory University Spelman College
Alison P. Grand
Affiliation:
Emory University
Richelle Fulks
Affiliation:
Emory University
Anne Graff
Affiliation:
Emory University
Dario Maestripieri*
Affiliation:
Emory University University of Chicago
*
Address correspondence and reprint requests to: Dario Maestripieri, University of Chicago, 5730 South Woodlawn Avenue, Chicago, IL 60637; E-mail: [email protected].
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Abstract

In this study we investigated the development of the hypothalamic–pituitary–adrenal (HPA) axis in 21 group-living rhesus monkeys infants that were physically abused by their mothers in the first few months of life and in 21 nonabused controls. Cortisol and adrenocorticotropin hormone (ACTH) responses to a corticotropin-releasing hormone (CRH) challenge were assessed at 6-month intervals during the subjects' first 3 years of life. Abused infants exhibited greater cortisol responses to CRH than controls across the 3 years. Abused infants also exhibited blunted ACTH secretion in response to CRH, especially at 6 months of age. Although there were no significant sex differences in abuse experienced early in life, females showed a greater cortisol response to CRH than males at all ages. There were no significant sex differences in the ACTH response to CRH, or significant interactions between sex and abuse in the ACTH or cortisol response. Our findings suggest that early parental maltreatment results in greater adrenocortical, and possibly also pituitary, responsiveness to challenges later in life. These long-term alterations in neuroendocrine function may be one the mechanisms through which infant abuse results in later psychopathologies. Our study also suggests that there are developmental sex differences in adrenal function that occur irrespective of early stressful experience. The results of this study can enhance our understanding of the long-term effects of child maltreatment as well as our knowledge of the development of the HPA axis in human and nonhuman primates.

Type
Regular Articles
Information
Development and Psychopathology , Volume 22 , Issue 1 , February 2010 , pp. 45 - 53
Copyright
Copyright © Cambridge University Press 2010

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References

Blank, M. S., Gordon, T. P., & Wilson, M. E. (1983). Effects of venipuncture on serum levels of prolactin, growth hormone, and cortisol in outdoor compound-housed female rhesus monkeys. Acta Endocrinologica, 102, 190–195.Google ScholarPubMed
Born, J., Ditschumeit, X., Schreiber, M., Dodt, C., & Fehm, H. L. (1995). Effects of age and gender on pituitary–adrenocortical responsiveness in humans. European Journal of Endocrinology, 132, 705–711.CrossRefGoogle ScholarPubMed
Bowman, R. E., & Wolf, R. C. (1969). Plasma 17-hydroxycorticosteroid response to ACTH in M. mulatta: Dose, age, weight, and sex. Proceedings of the Society for Experimental Biology and Medicine, 130, 61–64.CrossRefGoogle Scholar
Boyce, W. T., Champoux, M., Suomi, S. J., & Gunnar, M. R. (1995). Salivary cortisol in nursery-reared rhesus monkeys: Reactivity to peer interactions and altered circadian activity. Developmental Psychobiology, 28, 257–267.Google ScholarPubMed
Bugental, D. B., Martorell, G. A., & Barraza, V. (2003). The hormonal costs of subtle forms of infant maltreatment. Hormones & Behavior, 43, 237–244.CrossRefGoogle ScholarPubMed
Carrion, V., Weems, C., Ray, R., Glaser, B., Hessl, D., & Reiss, A. (2002). Diurnal salivary cortisol in pediatric posttraumatic stress disorder. Biological Psychiatry, 51, 575–582.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Cohen, D. J. (Eds.). (2006). Developmental psychopathology. New York: Wiley.Google ScholarPubMed
Clarke, A. S. (1993). Social rearing effects on HPA activity over early development and in response to stress in rhesus monkeys. Developmental Psychobiology, 26, 433–446.CrossRefGoogle ScholarPubMed
De Bellis, M. D., Chrousos, G. P., Dorn, L. D., Burke, L., Helmers, K., Kling, M. A., et al. (1994). Hypothalamic–pituitary–adrenal axis dysregulation in sexually abused girls. Journal of Clinical Endocrinology & Metabolism, 78, 249–255.Google ScholarPubMed
Glaser, D. (2000). Child abuse and neglect and the brain: A review. Journal of Child Psychology and Psychiatry, 41, 97–116.CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Donzella, B. (2002). Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology, 27, 199–220.CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Fisher, P. A. (2006). The early experience, stress, and prevention network: Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children. Development and Psychopathology, 18, 651–677.CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145–173.CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Vazquez, D. M. (2006). Stress neurobiology and developmental psychopathology. In: Cicchetti, D. & Cohen, D. (Eds.), Developmental psychopathology: Developmental neuroscience (pp. 533–577. New York: Wiley.Google Scholar
Gust, D. A., Gordon, T. P., & Hambright, K. (1993). Response to removal from and return to a social group in adult male rhesus monkeys. Physiology and Behavior, 53, 599–602.CrossRefGoogle ScholarPubMed
Hart, J., Gunnar, M., & Cicchetti, D. (1995). Salivary cortisol in maltreated children: Evidence of relations between neuroendocrine activity and social competence. Development and Psychopathology, 7, 11–26.CrossRefGoogle Scholar
Hart, J., Gunnar, M., & Cicchetti, D. (1996). Altered neuroendocrine activity in maltreated children related to symptoms of depression. Development and Psychopathology, 8, 201–214.CrossRefGoogle Scholar
Heim, C., Newport, D. J., Bonsall, R., Miller, A. H., & Nemeroff, C. B. (2001). Altered pituitary–adrenal axis responses to provocative challenge tests in adult survivors of childhood abuse. American Journal of Psychiatry, 158, 575–180.CrossRefGoogle ScholarPubMed
Heim, C., Newport, D. J., Heit, S., Graham, Y. P., Wilcox, M., Bonsall, R., Miller, A. H., & Nemeroff, C. B. (2000). Pituitary–adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. Journal of the American Medical Association, 284, 292–297.Google ScholarPubMed
Holsboer, F., Gerkin, A., Stalla, G., & Muller, A. (1987). Blunted aldosterone and ACTH release after human RH administration in depressed patients. American Journal of Psychiatry, 144, 229–231.Google Scholar
Kaufman, J. (1991). Depressive disorders in maltreated children. Journal of the American Academy of Child & Adolescent Psychiatry, 30, 257–265.CrossRefGoogle ScholarPubMed
Kaufman, J., Birmaher, B., Perel, J., Dahl, R. E., Moreci, P., Nelson, B., Wells, W., & Ryan, N.D. (1997). The corticotropin-releasing hormone challenge in depressed abused, depressed nonabused, and normal control children. Biological Psychiatry, 42, 669–679.CrossRefGoogle ScholarPubMed
Kaufman, J., Brent, D., Birmaher, B., Perel, J., Dahl, R. E., Nelson, B., et al. (1993). Measures of family adversity, clinical symptomatology, and cortisol secretion in a sample of preadolescent depressed children. Paper presented at the Annual Meeting of the Society for Research in Child and Adolescent Psychopathology, Santa Fe, NM.Google Scholar
Maestripieri, D. (1993). Maternal anxiety in rhesus macaques (Macaca mulatta). I. Measurement of anxiety and identification of anxiety-eliciting situations. Ethology, 95, 19–31.CrossRefGoogle Scholar
Maestripieri, D. (1994). Infant abuse associated with psychosocial stress in a group-living pigtail macaque (Macaca nemestrina) mother. American Journal of Primatology, 32, 41–49.CrossRefGoogle Scholar
Maestripieri, D. (1995). Assessment of danger to themselves and their infants by rhesus macaque (Macaca mulatta) mothers. Journal of Comparative Psychology, 109, 416–420.CrossRefGoogle ScholarPubMed
Maestripieri, D. (1998). Parenting styles of abusive mothers in group-living rhesus macaques. Animal Behaviour, 55, 1–11.CrossRefGoogle ScholarPubMed
Maestripieri, D. (2005). Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proceedings of the National Academy of Science of the United States of America, 102, 9726–9729.CrossRefGoogle ScholarPubMed
Maestripieri, D., & Carroll, K. A. (1998). Risk factors for infant abuse and neglect in rhesus monkeys. Psychological Science, 9, 143–145.CrossRefGoogle Scholar
Maestripieri, D., Wallen, K., & Carroll, K. A. (1997). Infant abuse runs in families of group-living pigtail macaques. Child Abuse and Neglect, 21, 465–471.CrossRefGoogle ScholarPubMed
Maestripieri, D., Higley, J. D., Lindell, S. G., Newman, T. K., McCormack, K., & Sanchez, M. M. (2006). Early maternal rejection affects the development of monoaminergic systems and adult abusive parenting in rhesus macaques. Behavioral Neuroscience, 120, 1017–1024.CrossRefGoogle ScholarPubMed
Maestripieri, D., Lindell, S. G., & Higley, J. D. (2007). Intergenerational transmission of maternal behavior in rhesus monkeys and its underlying mechanisms. Developmental Psychobiology, 49, 165–171.CrossRefGoogle ScholarPubMed
Maestripieri, D., McCormack, K., Lindell, S. G., Higley, J. D., & Sanchez, M. M. (2006). Influence of parenting style on the offspring's behavior and CSF monoamine metabolite levels in crossfostered and noncrossfostered female rhesus macaques. Behavioural and Brain Research, 175, 90–95.CrossRefGoogle ScholarPubMed
Maestripieri, D., Tomaszycki, M., & Carroll, K. A. (1999). Consistency and change in the behavior of rhesus macaque abusive mothers with successive infants. Developmental Psychobiology, 34, 29–35.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
McCormack, K. M., Sanchez, M. M., Bardi, M., & Maestripieri, D. (2006). Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6 months of life. Developmental Psychobiology, 48, 537–550.CrossRefGoogle ScholarPubMed
Meyer, J. S., & Bowman, R. E. (1972). Rearing experience, stress, and adrenocorticosteroids in the rhesus monkey. Physiology and Behavior, 8, 339–343.CrossRefGoogle ScholarPubMed
Nemeroff, C. B. (2004). Neurobiological consequences of childhood trauma. Journal of Clinical Psychiatry, 65, 18–28.Google ScholarPubMed
Roelfsema, F., van den Berg, G., Frolich, M., Veldhus, J. D., van Eijk, A., Buurman, M. M., & Etman, B. H. B. (1993). Sex-dependent alteration in cortisol response to endogenous adrenocorticotropin. Journal of Clinical Endocrinology and Metabolism, 77, 234–240.Google ScholarPubMed
Roy, A. (2002). Urinary free cortisol and childhood trauma in cocaine dependent adults. Journal of Psychiatry Research, 36, 173–177.CrossRefGoogle ScholarPubMed
Sanchez, M. M. (2006). The impact of early adverse care on HPA axis development: Nonhuman primate models. Hormones and Behavior, 50, 623–631.CrossRefGoogle ScholarPubMed
Sanchez, M. M., Noble, P. M., Lyon, C. K., Plotsky, P. M., Davis, M., Nemeroff, C. B., et al. (2005). Alterations in diurnal cortisol rhythm and acoustic startle response in non-human primates with adverse rearing. Biological Psychiatry, 57, 373–381.CrossRefGoogle Scholar
Scallet, A. C., Suomi, S. J., & Bowman, R. E. (1981). Sex differences in adrenocortical response to controlled agonistic encounters in rhesus monkeys. Physiology and Behavior, 26, 385–390.CrossRefGoogle ScholarPubMed
Scheer, F. A. J. L., & Buijs, R. M. (1999). Light affects morning salivary cortisol in humans. Journal of Clinical Endocrinology and Metabolism, 84, 3395–3398.CrossRefGoogle ScholarPubMed
Tarullo, A. R., & Gunnar, M. R. (2006). Child maltreatment and the developing HPA axis. Hormones and Behavior, 50, 632–639.CrossRefGoogle ScholarPubMed
Teicher, M. H., Andersen, S. L., Polcari, A., Anderson, C. M., Navalta, C. P., & Kim, D. M. (2003). The neurobiological consequences of early stress and childhood maltreatment. Neuroscience and Biobehavioral Reviews, 27, 33–44.CrossRefGoogle ScholarPubMed
Troisi, A., & D'Amato, F. R. (1991). Anxiety in the pathogenesis of primate infant abuse: A pharmacological study. Psychopharmacology, 103, 571–572.CrossRefGoogle ScholarPubMed
Wilson, M. E., Gordon, T. P., & Collins, D. C. (1986). Ontogeny of luteinizing hormone secretion and first ovulation in seasonal breeding rhesus monkeys. Endocrinology, 118, 293–301.CrossRefGoogle ScholarPubMed
Yehuda, R., Halligan, S. L., & Grossman, R. (2001). Childhood trauma and risk for PTSD: Relationship to intergenerational effects of trauma, parental PTSD, and cortisol excretion. Development and Psychopathology, 13, 733–753.CrossRefGoogle ScholarPubMed
Zahn-Waxler, C., Shirtcliff, E. A., & Marceau, K. (2008). Disorders of childhood and adolescence: Gender and psychopathology. Annual Review of Clinical Psychology, 4, 275–303.CrossRefGoogle ScholarPubMed