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Understanding behavioral effects of early life stress using the reactive scope and allostatic load models

Published online by Cambridge University Press:  21 October 2011

Brittany R. Howell  and
Mar M. Sanchez
Brittany R. Howell
Affiliation:
Emory University
Mar M. Sanchez*
Affiliation:
Emory University
*
Address correspondence and reprint requests to: Mar M. Sanchez, Department of Psychiatry and Behavioral Sciences, School of Medicine, and Yerkes National Primate Research Center, Emory University, 954 Gatewood Rd NE, Atlanta, GA 30329; E-mail: mmsanch@emory.edu.
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Abstract

The mechanisms through which early life stress leads to psychopathology are thought to involve allostatic load, the “wear and tear” an organism is subjected to as a consequence of sustained elevated levels of glucocorticoids caused by repeated/prolonged stress activations. The allostatic load model described this phenomenon, but has been criticized as inadequate to explain alterations associated with early adverse experience in some systems, including behavior, which cannot be entirely explained from an energy balance perspective. The reactive scope model has been more recently proposed and focuses less on energy balance and more on dynamic ranges of physiological and behavioral mediators. In this review we examine the mechanisms underlying the behavioral consequences of early life stress in the context of both these models. We focus on adverse experiences that involve mother–infant relationship disruption, and dissect those mechanisms involving maternal care as a regulator of development of neural circuits that control emotional and social behaviors in the offspring. We also discuss the evolutionary purpose of the plasticity in behavioral development, which has a clear adaptive value in a changing environment.

Type
Articles
Information
Development and Psychopathology , Volume 23 , Issue 4: Allostatic Load: Part 2 , November 2011 , pp. 1001 - 1016
Copyright
Copyright © Cambridge University Press 2011

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References

Albanese, A., Hamill, G., Jones, J., Skuse, D., Matthews, D. R., & Stanhope, R. (1994). Reversibility of physiological growth hormone secretion in children with psychosocial dwarfism. Clinical Endocrinology, 40, 687–692.CrossRefGoogle ScholarPubMed
Andersen, S. L. (2003). Trajectories of brain development: Point of vulnerability or window of opportunity? Neuroscience and Biobehavioral Reviews, 27, 3–18.CrossRefGoogle ScholarPubMed
Barr, C. S., Newman, T. K., Becker, M. L., Parker, C. C., Champoux, M., Lesch, K. P., et al. (2003). The utility of the non-human primate model for studying gene by environment interactions in behavioral research. Genes, Brain and Behavior, 2, 336–340.CrossRefGoogle ScholarPubMed
Bauman, M. D., & Amaral, D. G. (2005). The distribution of serotonergic fibers in the macaque monkey amygdala: An immunohistochemical study using antisera to 5-hydroxytryptamine. Neuroscience, 136, 193–203.CrossRefGoogle ScholarPubMed
Bernard, C. (1957). An introduction to the study of experimental medicine. New York: Dover Publications.Google Scholar
Bijou, S. W., & Baer, D. M. (1961). Child development. New York: Appleton–Century–Crofts.Google Scholar
Boinski, S., & Fragaszy, D. M. (1989). The ontogeny of foraging in squirrel monkeys, Saimiri oerstedi. Animal Behaviour, 37, 415–428.CrossRefGoogle Scholar
Bowlby, J. (1965). Attachment. New York: Basic Books.Google Scholar
Bredy, T. W., Grant, R. J., Champagne, D. L., & Meaney, M. J. (2003). Maternal care influences neuronal survival in the hippocampus of the rat. European Journal of Neuroscience, 18, 2903–2909.CrossRefGoogle ScholarPubMed
Brent, L., Koban, T., & Ramirez, S. (2002). Abnormal, abusive and stress-related behaviors in baboon mothers. Biological Psychiatry, 52, 1047–1056.CrossRefGoogle ScholarPubMed
Caldji, C., Diorio, J., & Meaney, M. J. (2000). Variations in maternal care in infancy regulate the development of stress reactivity. Biological Psychiatry, 48, 1164–1174.CrossRefGoogle ScholarPubMed
Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., & Meaney, M. J. (1998). Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proceedings of the National Academy of Sciences of the United States of America, 95, 5335–5340.CrossRefGoogle ScholarPubMed
Cameron, N. M., Champagne, F. A., Parent, C., Fish, E. W., Ozaki-Kuroda, K., & Meaney, M. J. (2005). The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neuroscience and Biobehavioral Reviews, 29, 843–865.CrossRefGoogle ScholarPubMed
Cannon, W. B. (1932). The wisdom of the body. New York: W.W. Norton & Company.CrossRefGoogle Scholar
Castren, E. (2004). Neurotrophic effects of antidepressant drugs. Current Opinion in Pharmacology, 4, 58–64.CrossRefGoogle ScholarPubMed
Cenci, M. A., & Kalen, P. (2000). Serotonin release from mesencephalic raphe neurons grafted to the 5,7-dihydroxytryptamine-lesioned rat hippocampus: Effects of behavioral activation and stress. Experimental Neurology, 164, 351–361.CrossRefGoogle Scholar
Champagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., de Kloet, E. R., et al. (2008). Maternal care and hippocampal plasticity: Evidence for experience dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. Journal of Neuroscience, 28, 6037–6045.CrossRefGoogle ScholarPubMed
Champagne, F. A., Chretien, P., Stevenson, C. W., Zhang, T. Y., Gratton, A., & Meaney, M. J. (2004). Variations in nucleus accumbens dopamine associated with individual differences in maternal behavior in the rat. Journal of Neuroscience, 24, 4113–4123.CrossRefGoogle ScholarPubMed
Champagne, F. A., Weaver, I. C., Diorio, J., Dymov, S., Szyf, M., & Meaney, M. J. (2006). Maternal care associated with methylation of the estrogen receptor-1b promoter and estrogen receptor-expression in the medial preoptic area of female offspring. Endocrinology, 147, 2909–2915.CrossRefGoogle Scholar
Chatterjee, D., Chatterjee-Chakraborty, M., Rees, S., Cauchi, J., de Medeiros, C. B., & Fleming, A. S. (2007). Maternal isolation alters the expression of neural proteins during development: “stroking” stimulation reverses these effects. Brain Research 1158, 11–27.CrossRefGoogle ScholarPubMed
Chubakov, A. R., Gromova, E. A., Konovalov, G. V., Sarkisova, E. F., & Chumasov, E. I. (1986). The effects of serotonin on the morpho-functional development of rat cerebral neocortex in tissue culture. Brain Research, 369, 285–297.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Dawson, G. (2002). Multiple levels of analysis. Development and Psychopathology, 14, 417–420.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Gunnar, M. R. (2008). Integrating biological processes into the design and evaluation of preventive interventions. Development and Psychopathology, 20, 737–743.CrossRefGoogle Scholar
Cicchetti, D., & Rogosch, F. (2001). The impact of child maltreatment and psychopathology on neuroendocrine functioning. Development and Psychopathology, 13, 783–780.CrossRefGoogle ScholarPubMed
Cicchetti, D., Rogosch, F. A., Gunnar, M. R., & Toth, S. L. (2010). The differential impacts of early abuse on internalizing problems and diurnal cortisol activity in school-aged children. Child Development, 25, 252–269.CrossRefGoogle Scholar
Cicchetti, D., & Toth, S. L. (2009). The past achievements and future promises of developmental psychopathology: The coming of age of a discipline. Journal of Child Psychology and Psychiatry, 50, 16–25.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Valentino, K. (2006). An ecological transactional perspective on child maltreatment: Failure of the average expectable environment and its influence upon child development. In Cicchetti, D., & Cohen, D. J. (Eds.), Developmental psychopathology (Vol. 3, 2nd ed., pp. 129–201). New York: Wiley.Google Scholar
Clarke-Stewart, K. A. (1973). Interactions between mothers and their young children: Characteristics and consequences. Monographs of the Society for Research in Child Development, 38, 1–109.CrossRefGoogle ScholarPubMed
Coe, C. L., Glass, J. C., Wiener, S. G., & Levine, S. (1983). Behavioral, but not physiological, adaptation to repeated separation in mother and infant primates. Psychoneuroendocrinology, 8, 401–409.CrossRefGoogle Scholar
Connell, C. M., & Prinz, R. J. (2002). The impact of childcare and parent–child interactions on school readiness and social skills development for low-income African American children. Journal of School Psychology, 40, 177–193.CrossRefGoogle Scholar
Coplan, J. D., Rosenblum, L. A., & Gorman, J. M. (1995). Primate models of anxiety. Longitudinal perspectives. Psychiatric Clinics of North America, 18, 727–743.CrossRefGoogle ScholarPubMed
Creel, S. (2001). Social dominance and stress hormones. Trends in Ecology and Evolution, 16, 491e–497e.CrossRefGoogle Scholar
Creel, S., Creel, N. M., & Monfort, S. L. (1996). Social stress and dominance. Nature 379, 212.CrossRefGoogle Scholar
Dallman, M. F. (2003). Stress by any other name . . . ? Hormones and Behavior, 43, 18–20; discussion 28–30.CrossRefGoogle ScholarPubMed
Eghbal-Ahmadi, M., Avishai-Eliner, S., Hatalski, C. G., & Baram, T. Z. (1999). Differential regulation of the expression of corticotropin-releasing factor receptor type 2 (CRF2) in hypothalamus and amygdala of the immature rat by sensory input and food intake. Journal of Neuroscience, 19, 3982–3991.CrossRefGoogle ScholarPubMed
Fairbanks, L. A. (1996). Individual differences in maternal style: causes and consequences of mothers and offspring. Advances in the Study of Behavior 25, 579–611.CrossRefGoogle Scholar
Feldman, R., Eidelman, A. I., Sirota, L., & Weller, A. (2002). Comparison of skin-to-skin (kangaroo) and traditional care: Parenting outcomes and preterm infant development. Pediatrics, 110(1, Pt. 1), 16–26.CrossRefGoogle ScholarPubMed
Fisher, A. E. (1955). The effects of differential early treatment on the social and exploratory behavior of puppies. Doctoral dissertation, Pennsylvania State University.Google Scholar
Flugge, G. (1995). Dynamics of central nervous 5-HT1A-receptors under psychosocial stress. Journal of Neuroscience, 15, 7132–7140.CrossRefGoogle ScholarPubMed
Forster, G. L., Feng, N., Watt, M. J., Korzan, W. J., Mouw, M. J., Summers, H., et al. (2006). Corticotropin-releasing factor in the dorsal raphe elicits temporally distinct serotonergic responses in the limbic system in relation to fear behavior. Neuroscience, 141, 1047–1055.CrossRefGoogle ScholarPubMed
Fox, K. (1995). The critical period for long-term potentiation in primary sensory cortex. Neuron, 15, 485–488.CrossRefGoogle ScholarPubMed
Freedman, L. J., & Shi, C. (2001). Monoaminergic innervations of the macaque extended amygdala. Neuroscience, 104, 1067–1084.CrossRefGoogle ScholarPubMed
Garlow, S. J., & Ciaranello, R. D. (1995). Transcriptional control of the rat serotonin-2 receptor gene. Brain Research Molecular Brain Research, 31, 201–209.CrossRefGoogle ScholarPubMed
Goldman-Rakic, P. S., & Brown, R. M. (1982). Postnatal development of monoamine content and synthesis in the cerebral cortex of rhesus monkeys. Brain Research, 256, 339–349.CrossRefGoogle ScholarPubMed
Goymann, W., & Wingfeld, J. C. (2004). Allostatic load, social status and stress hormones: The costs of social status matter. Animal Behavior, 67, 591–602.CrossRefGoogle Scholar
Grassi-Oliveira, R., Ashy, M., & Stein, L. M. (2008). Psychobiology of childhood maltreatment: effects of allostatic load? Revista Brasileira de Psiquiatria, 30, 60–68.CrossRefGoogle ScholarPubMed
Grewen, K. M., Girdler, S. S., Amico, J., & Light, K. C. (2005). Effects of partner support on resting oxytocin, cortisol, norepinephrine, and blood pressure before and after warm partner contact. Psychosomatic Medicine, 67, 531–538.CrossRefGoogle ScholarPubMed
Gunnar, M. R., Brodersen, L., Nachmias, M., Buss, M., & Rigatuso, R. (1996). Stress reactivity and attachment security. Developmental Psychobiology, 29, 10–36.3.0.CO;2-M>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., & 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
Hane, A. A., & Fox, N. A. (2006). Ordinary variations in maternal caregiving in human infants influences stress reactivity. Psychological Science, 17, 550–556.CrossRefGoogle ScholarPubMed
Hane, A. A., Henderson, H. A., Reeb-Sutherland, B. C., & Fox, N. A. (2010). Ordinary variations in human maternal caregiving in infancy and biobehavioral development in early childhood: A follow-up study. Developmental Psychobiology, 52, 558–567.CrossRefGoogle ScholarPubMed
Harlow, H. F., & Harlow, M. K. (1965). The affectional systems. In Shrier, A. M., Harlow, H. F., & Stollnitz, F. (Eds.), Behavior of nonhuman primates (Vol. 2). New York: Academic Press.Google Scholar
Harlow, H. F., & Zimmermann, R. R. (1959). Affectional responses in the infant monkey; Orphaned baby monkeys develop a strong and persistent attachment to inanimate surrogate mothers. Science, 130, 421–432.CrossRefGoogle Scholar
Heim, C., & Nemeroff, C. B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biological Psychiatry, 49, 1023–1039.CrossRefGoogle ScholarPubMed
Heim, C., Newport, D. J., Heit, S., Graham, Y. P., Wilcox, M., Bonsall, R., et al. (2000). Pituitary–adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. Journal of the American Medical Association, 284, 592–597.CrossRefGoogle ScholarPubMed
Heim, C., Newport, D. J., Mletzko, T., Miller, A. H., Young, L. J., & Nemeroff, C. B. (2006). Decreased cerebrospinal fluid oxytocin concentrations associated with childhood maltreatment in adult women. Developmental Psychobiology Abstracts, 48, 603–630.Google Scholar
Helfer, M. E., Kempe, R. S., & Krugman, R. D. (1997). The battered child. Chicago: University of Chicago Press.Google Scholar
Hennessy, M. B. (1986). Multiple, brief maternal separations in the squirrel monkey: Changes in hormonal and behavioral responsiveness. Physiology & Behavior, 36, 245–250.CrossRefGoogle ScholarPubMed
Higley, J. D., Suomi, S .J., & Linnoila, M. (1996). 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. Alcoholism: Clinical and Experimental Research, 20, 643–650.CrossRefGoogle ScholarPubMed
Hildyard, K. L., & Wolfe, D. A. (2002). Child neglect: Developmental issues and outcomes. Child Abuse & Neglect, 26, 679–695.CrossRefGoogle ScholarPubMed
Hofer, M. A. (1984). Relationships as regulators: A psychobiologic perspective on bereavement. Psychosomatic Medicine 46, 183–197.CrossRefGoogle ScholarPubMed
Johnson, E. O., Kamilaris, T. C., Calogero, A. E., Gold, P. W., & Chrousos, G. P. (1996). Effects of early parenting on growth and development in a small primate. Pediatric Research, 39, 999–1005.CrossRefGoogle ScholarPubMed
Junghans, D., Haas, I. G., & Kemler, R. (2005). Mammalian cadherins and protocadherins: About cell death, synapses and processing. Current Opinion in Cell Biology, 17, 446–452.CrossRefGoogle ScholarPubMed
Kaffman, A., & Meaney, M. J. (2007). Neurodevelopmental sequelae of postnatal maternal care in rodents: Clinical and research implications of molecular insights. Journal of Child Psychology and Psychiatry, 48, 224–244.CrossRefGoogle ScholarPubMed
Katori, S., Hamada, S., Noguchi, Y., Fukuda, E., Yamamoto, T., Yamamoto, H., et al. (2009). Protocadherin-alpha family is required for serotonergic projections to appropriately innervate target brain areas. Journal of Neuroscience, 29, 9137–9147.CrossRefGoogle ScholarPubMed
Kaufman, J., Birmaher, B., Perel, J., Dahl, R. E., Stull, S., Brent, D., et al. (1998). Serotonergic functioning in depressed abused children: Clinical and familial correlates. Biological Psychiatry, 44, 973–981.CrossRefGoogle ScholarPubMed
Kertes, D. A., Gunnar, M. R., Madsen, N. J., & Long, J. (2008). Early deprivation and home basal cortisol levels: A study of internationally-adopted children. Development and Psychopathology, 20, 473–491.CrossRefGoogle Scholar
Kimonis, E. R., Frick, P. J., Munoz, L. C., & Aucoin, K. J. (2008). Callous–unemotional traits and the emotional processing of distress cues in detained boys: Testing the moderating role of aggression, exposure to community violence, and histories of abuse. Development and Psychopathology, 20, 569–589.CrossRefGoogle ScholarPubMed
Kolber, B. J., Roberts, M. S., Howell, M. P., Wozniak, D. F., Sands, M. S., & Muglia, L. J. (2008). Central amygdala glucocorticoid receptor action promotes fear-associated CRH activation and conditioning. Proceedings of the National Academy of Sciences of the United States of America, 105, 12004–12009.CrossRefGoogle ScholarPubMed
Korosi, A., & Baram, T. Z. (2009). The pathways from mother's love to baby's future. Frontiers in Behavioral Neuroscience, 3, 1–8.CrossRefGoogle ScholarPubMed
Kuhn, C. M., Butler, S. R., & Schanberg, S. M. (1978). Selective depression of serum growth hormone during maternal deprivation in rat pups. Science, 20, 1034–1036.CrossRefGoogle Scholar
Kuhn, C. M., & Schanberg, S. M. (1998). Responses to maternal separation: Mechanisms and mediators. International Journal of Developmental Neuroscience, 16, 261–270.CrossRefGoogle ScholarPubMed
Lauder, J. M., & Krebs, H. (1976). Effects of p-chlorophenylalanine on time of neuronal origin during embryogenesis in the rat. Brain Research, 107, 638–644.CrossRefGoogle ScholarPubMed
Lauder, J. M., & Krebs, H. (1978). Serotonin as a differentiation signal in early neurogenesis. Developmental Neuroscience, 1, 15–30.CrossRefGoogle ScholarPubMed
Leonard, B. E. (2005). The HPA and immune axes in stress: The involvement of the serotonergic system. European Psychiatry, 20(Suppl 3), S302–S306.CrossRefGoogle ScholarPubMed
Levine, S., & Mody, T. (2003). The long-term psychobiological consequences of intermittent postnatal separation in the squirrel monkey. Neuroscience and Biobehavioral Reviews, 27, 83–89.CrossRefGoogle ScholarPubMed
Levine, S., & Ursin, H. (1991). What is stress? In Brown, M. R., Koob, G. F., & Rivier, C. (Eds.), Stress: Neurobiology and neuroendocrinology (pp. 3–21). New York: Marcel Dekker.Google Scholar
Liu, D., Diorio, J., Day, J. C., Francis, D. D., & Meaney, M. J. (2000). Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nature Neuroscience, 3, 799–806.CrossRefGoogle ScholarPubMed
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., et al. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic–pituitary–adrenal responses to stress. Science, 277, 1659–1662.CrossRefGoogle ScholarPubMed
Lyons, D. M., Kim, S., Schatzberg, A. F., & Levine, S. (1998). Postnatal foraging demands alter adrenocortical activity and psychosocial development. Developmental Psychobiology, 32, 285–291.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Lyons, D. M., Lopez, J. M., Yang, C., & Schatzberg, A. F. (2000). Stress-level cortisol treatment impairs inhibitory control of behavior in monkeys. Journal of Neuroscience, 20, 7816–7821.CrossRefGoogle ScholarPubMed
Lyons, D. M., Martel, F. L., Levine, S., Risch, N. J., & Schatzberg, A. F. (1999). Postnatal experiences and genetic effects on squirrel monkey social affinities and emotional distress. Hormones and Behavior, 36, 266–275.CrossRefGoogle ScholarPubMed
Lyons, D. M., & Parker, K. J. (2007). Stress inoculation-induced indications of resilience in monkeys. Journal of Traumatic Stress, 20, 423–433.CrossRefGoogle ScholarPubMed
Lyons, D. M., Parker, K. J., Katz, M., & Schatzberg, A. F. (2009). Developmental cascades linking stress inoculation, arousal regulation, and resilience. Frontiers in Behavioral Neuroscience, 3, 1–6.CrossRefGoogle ScholarPubMed
Mackowiak, M., Czyrak, A., & Wedzony, K. (2000). The involvement of 5-HT1a serotonin receptors in the pathophysiology and pharmacotherapy of schizophrenia [in Polish]. Psychiatria Polska, 34, 607–621.Google ScholarPubMed
Maestripieri, D. (1999). The biology of human parenting: Insights from nonhuman primates. Neuroscience and Biobehavioral Reviews, 23, 411–422.CrossRefGoogle ScholarPubMed
Maestripieri, D. (2005a). Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proceedings of the National Academy of Sciences of the United States of America, 102, 9726–9729.CrossRefGoogle ScholarPubMed
Maestripieri, D. (2005b). Effects of early experience on female behavioural and reproductive development in rhesus macaques. Proceedings of the Royal Society Part B: Biological Sciences, 272, 1243–1248.CrossRefGoogle ScholarPubMed
Maestripieri, D., Lindell, S. G., Higley, J. D., Newman, T. K., McCormack, K. M., & Sanchez, M. M. (2006a). Early maternal rejection affects the development of monoaminergic systems and adult parenting in rhesus macaques. Behavioral Neuroscience, 120, 1017–1024.CrossRefGoogle ScholarPubMed
Maestripieri, D., McCormack, K. M., Higley, J. D., Lindell, S. G., & Sanchez, M. M. (2006b). Influence of parenting style on the offspring's behavior and CSF monoamine metabolites in cross-fostered and noncrossfostered rhesus macaques. Behavioural Brain Research, 175, 90–95.CrossRefGoogle Scholar
Manji, H. K., Drevets, W. C., & Charney, D. S. (2001). The cellular neurobiology of depression. Nature Medicine, 7, 541–547.CrossRefGoogle ScholarPubMed
McCormack, K., Newman, T. K., Higley, J. D., Maestripieri, D., & Sanchez, M. M. (2009). Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants. Hormones and Behavior, 55, 538–547.CrossRefGoogle ScholarPubMed
McEwen, B. S. (1998). Protective and damaging effects of stress mediators. New England Journal of Medicine, 338, 171–179.CrossRefGoogle ScholarPubMed
McEwen, B. S., & Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Hormones and Behavior, 43, 2–15.CrossRefGoogle ScholarPubMed
McEwen, B. S., & Wingfield, J. C. (2010). What is in a name? Integrating homeostasis, allostasis and stress. Hormones and Behavior, 57, 105–111.CrossRefGoogle Scholar
McGowan, P. O., Sasaki, A., D'Alessio, A. C., Dymov, S., Labonte, B., Szyf, M., et al. (2009). Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuroscience, 12, 342–348.CrossRefGoogle ScholarPubMed
McGowan, P. O., Suderman, M., Sasaki, A., Huang, T. C. T., Hallett, M., Meaney, M. J., et al. (2011). Broad epigenetic signature of maternal care in the brain of adult rats. PLoS ONE, 6, e14739.CrossRefGoogle ScholarPubMed
Meaney, M. J., Diorio, J., Francis, D., Weaver, S., Yau, J., Chapman, K., et al. (2000). Postnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: The effects of thyroid hormones and serotonin. Journal of Neuroscience, 20, 3926–3935.CrossRefGoogle ScholarPubMed
Meaney, M. J., Mitchell, J. B., Aitken, D. H., Bhatnagar, S., Bodnoff, S. R., Iny, L. J., et al. (1991). The effects of neonatal handling on the development of the adrenocortical response to stress: Implications for neuropathology and cognitive deficits in later life. Psychoneuroendocrinology, 16, 85–103.CrossRefGoogle ScholarPubMed
Mears, C. E., & Harlow, H. F. (1975). Play: Early and eternal. Proceedings of the National Academy of Sciences of the United States of America, 72, 1878–1882.CrossRefGoogle ScholarPubMed
Meloni, E. G., Reedy, C. L., Cohen, B. M., & Carlezon, W. A. Jr. (2008). Activation of raphe efferents to the medial prefrontal cortex by corticotropin-releasing factor: correlation with anxiety-like behavior. Biological Psychiatry, 63, 832–839.CrossRefGoogle Scholar
Miller, L., Kramer, R., Warner, V., Wickramaratne, P., & Weissman, M. (1997). Intergenerational transmission of parental bonding among women. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 1134–1135.CrossRefGoogle ScholarPubMed
Mitchell, J. B., Betito, K., Rowe, W., Boksa, P., & Meaney, M. J. (1992). Serotonergic regulation of type II corticosteroid receptor binding in hippocampal cell cultures: Evidence for the importance of serotonininduced changes in cAMP levels. Neuroscience, 48, 631–639.CrossRefGoogle ScholarPubMed
Mitchell, J. B., Iny, L. J., & Meaney, M. J. (1990). The role of serotonin in the development and environmental regulation of type II corticosteroid receptor binding in rat hippocampus. Brain Research. Developmental Brain Research, 55, 231–235.CrossRefGoogle ScholarPubMed
Moriceau, S, & Sullivan, R. (2005). Neurobiology of infant attachment. Developmental Psychobiology, 47, 230–242.CrossRefGoogle ScholarPubMed
Nestler, E. J., & Carlezon, W. A. (2006). The mesolimbic dopamine reward circuit in depression. Biological Psychiatry, 59, 1151–1159.CrossRefGoogle ScholarPubMed
Numan, M., & Sheehan, T. P. (1997). Neuroanatomical circuitry for mammalian maternal behavior. Annals of the New York Academy of Sciences, 807, 101–125.CrossRefGoogle ScholarPubMed
Pedersen, C. A., Caldwell, J. D., Walker, C., Ayers, G., & Mason, G. A. (1994). Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behavioral Neuroscience, 108, 1163–1171.CrossRefGoogle ScholarPubMed
Pihoker, C., Owens, M. J., Kuhn, C. M., Schanberg, S. M., & Nemeroff, C. B. (1993). Maternal separation in neonatal rats elicits activation of the hypothalamic–pituitary–adrenocortical axis: A putative role for corticotropin-releasing factor. Psychoneuroendocrinology, 18, 485–493.CrossRefGoogle Scholar
Pollak, S. D., Cicchetti, D., Hornung, K., & Reed, A. (2000). Recognizing emotion in faces: Developmental effects of child abuse and neglect. Developmental Psychology, 36, 679–688.CrossRefGoogle ScholarPubMed
Rohwer, S., & Wingfield, J. C. (1981). A field study of social dominance, plasma levels of luteinizing hormone and steroid hormones in wintering Harris' sparrows. Zeitschrift für Tierpsychologie, 57, 173e183.CrossRefGoogle Scholar
Romero, L. M., Dickens, M. J., & Cyr, N. E. (2009). The reactive scope model—A new model integrating homeostasis, allostasis, and stress. Hormones and Behavior, 55, 375–389.CrossRefGoogle ScholarPubMed
Rosenblatt, J. S. (1975). Prepartum and postpartum regulation of maternal behaviour in the rat. Ciba Foundation Symposium, 33, 17–37.Google Scholar
Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D. (2009). Lasting epigenetic influence of early-life adversity on the BDNF gene. Biological Psychiatry, 57, 823–831.CrossRefGoogle Scholar
Rutter, M. (1981). Stress, coping and development: Some issues and some questions. Journal of Child Psychology and Psychiatry, 22, 323–356.CrossRefGoogle ScholarPubMed
Rutter, M. (1998). Developmental catch-up, and deficit, following adoption after severe global early privation. English and Romanian Adoptees (ERA) Study Team. Journal of Child Psychology and Psychiatry, 39, 465–476.Google ScholarPubMed
Saltzman, W., Schultz-Darken, N. J., Scheffler, G., Wegner, F. H., & Abbott, D. H. (1994). Social and reproductive influences on plasma cortisol in female marmoset monkeys. Physiology & Behavior, 56, 801–810.CrossRefGoogle ScholarPubMed
Saltzman, W., Schultz-Darken, N. J., Wegner, F. H., Wittwer, D. J., & Abbott, D. H. (1998). Suppression of cortisol levels in subordinate female marmosets: reproductive and social contributions. Hormones and Behavior, 33, 58–74.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., Alagbe, O., Felger, J., Zhang, J., Graff, A. E., Grand, A. P., et al. (2007). Activated p38 MAPK is associated with decreased CSF 5-HIAA and increased maternal rejection during infancy in rhesus monkeys. Molecular Psychiatry, 12, 895–897.CrossRefGoogle ScholarPubMed
Sanchez, M. M., Ladd, C. O., & Plotsky, P. M. (2001). Early adverse experience as a developmental risk factor for later psychopathology: Evidence from rodent and primate models. Development and Psychopathology, 13, 419–449.CrossRefGoogle ScholarPubMed
Sanchez, M. M., McCormack, K. M., & Maestripieri, D. (2010). Ethological case study: Infant abuse in rhesus macaques. In Plotsky, P. M., Schechter, D. S., & Cummings, C. (Eds.), Formative experiences: The interaction of caregiving, culture, and developmental psychobiology (pp. 224–237). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Sanchez, M. M., & Pollak, S. (2009). Socio-emotional development following early abuse and neglect. Challenges and insights from translational research. In Haan, M. de, & Gunnar, M. R. (Eds.), Handbook of developmental social neuroscience (pp. 497–520). New York: Guilford Press.Google Scholar
Sanchez, M. M., Young, L. J., Plotsky, P. M., & Insel, T. R. (2000). Distribution of corticosteroid receptors in the rhesus brain: Relative absence of glucocorticoid receptors in the hippocampal formation. Journal of Neuroscience, 20, 4657–4668.CrossRefGoogle ScholarPubMed
Sapolsky, R. M. (2002). Endocrinology of the stress response. In Becker, J. B., Breedlove, S. M., Crews, D., & McCarthy, M. (Eds.), Behavioral endocrinology (2nd ed., pp. 409–450). Cambridge, MA: MIT Press.Google Scholar
Savitz, J., Lucki, I., & Drevets, W. C. (2009). 5-HT(1A) receptor function in major depressive disorder. Progress in Neurobiology, 88, 17–31.CrossRefGoogle ScholarPubMed
Schulkin, J., Gold, P. W., & McEwen, B. S. (1998). Induction of corticotropin-releasing hormone gene expression by glucocorticoids: Implication for understanding the states of fear and anxiety and allostatic load. Psychoneuroendocrinology, 23, 219–243.CrossRefGoogle ScholarPubMed
Seltzer, L. J., Ziegler, T. E., & Pollak, S. D. (2010). Social vocalizations can realease oxytocin in humans. Proceedings of the Royal Society, Part B: Biological Sciences, 277, 2661–2666.CrossRefGoogle Scholar
Shackman, J. E., Shackman, A. J., & Pollak, S. D. (2007). Physical abuse amplifies attention to threat and increases anxiety in children. Emotion, 7, 838–852.CrossRefGoogle ScholarPubMed
Shepard, J. D., Barron, K. W., & Myers, D. A. (2000). Corticosterone delivery to the amygdala increases corticotropin-releasing factor mRNA in the central amygdaloid nucleus and anxiety-like behavior. Brain Research, 861, 288–295.CrossRefGoogle Scholar
Smythe, J. W., Rowe, W. B., & Meaney, M. J. (1994). Neonatal handling alters serotonin (5-HT) turnover and 5-HT2 receptor binding in selected brain regions: Relationship to the handling effect on glucocorticoid receptor expression. Brain Research Developmental Brain Research, 80, 183–189.CrossRefGoogle Scholar
Southwick, S. M., Vythilingam, M., & Charney, D. S. (2005). The psychobiology of depression and resilience to stress: Implications for prevention and treatment. Annual Review of Clinical Psychology, 1, 255–291.CrossRefGoogle ScholarPubMed
Sroufe, L. A. (1977). Wariness of strangers and the study of infant development. Child Development, 48, 731–746.CrossRefGoogle Scholar
Stein, M. B., Koverola, C., Hanna, C., Torchia, M. G., & McClarty, B. (1997). Hippocampal volume in women victimized by childhood sexual abuse. Psychological Medicine, 27, 951–959.CrossRefGoogle ScholarPubMed
Sterling, P., & Eyer, J. (1988). Allostasis: A new paradigm to explain arousal pathology. In Fisher, S., & Reason, J. (Eds.), Handbook of life stress, cognition and health (pp. 629–649). New York: Wiley.Google Scholar
Sullivan, R., & Lasley, E. N. (2010). Fear in love: Attachment, abuse, and the developing brain. Cerebrum, September. Retrieved from http://www.dana.org/news/cerebrum/detail.aspx?id=28926Google ScholarPubMed
Suomi, S. J. (1984). The development of affect in rhesus monkeys. In Fox, N. A., & Davidson, R. J. (Eds.), The psychobiology of affective development (pp. 119–159). Hillsdale, NJ: Erlbaum.Google Scholar
Szyf, M., Weaver, I. C. G., Champagne, F. A., Diorio, J., & Meaney, M. J. (2005). Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Frontiers in Neuroendocrinology, 26, 139–162.CrossRefGoogle ScholarPubMed
Teicher, M. H., Andersen, S. L., Polcari, A., Anderson, C. M., & Navalta, C. P. (2002). Developmental neurobiology of childhood stress and trauma. Psychiatric Clinics of North America, 25, 397–426, vii–viii.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
Teisl, M., & Cicchetti, D. (2007). Physical abuse, cognitive and emotional processes, and aggressive/disruptive behavior problems. Social Development, 17, 1467–9507.Google Scholar
Uvnas-Moberg, K. (1996). Neuroendocrinology of the mother–child interaction. Trends in Endocrinology and Metabolism, 7, 126–131.CrossRefGoogle ScholarPubMed
van IJzendoorn, H. W., & Juffer, F. (2006). The Emanuel Miller Memorial Lecture 2006: Adoption as intervention. Meta-analytic evidence for massive catch-up and plasticity in physical, socio-emotional, and cognitive development. Journal of Child Psychology and Psychiatry, 27, 1228–1245.CrossRefGoogle Scholar
Van Oers, H. J. J., de Kloet, E. R., Whelan, T., & Levine, S. (1998). Maternal deprivation effect on the infant's neural stress markers is reversed by tactile stimulation and feeding but not by suppressing corticosterone. Journal of Neuroscience, 18, 10171–10179.CrossRefGoogle Scholar
von Holst, D. (1998). The concept of stress and its relevance for animal behavior. Advances in the Study of Behavior, 27, 1–131.CrossRefGoogle Scholar
Weaver, I. C., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., et al. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847–854.CrossRefGoogle ScholarPubMed
Weaver, I. C., Meaney, M. J., & Szyf, M. (2006). Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proceedings of the National Academy of Sciences of the United States of America, 103, 3480–3485.CrossRefGoogle ScholarPubMed
Whitaker-Azmitia, P. M. (2001). Serotonin and brain development: Role in human developmental diseases. Brain Research Bulletin, 56, 479–485.CrossRefGoogle ScholarPubMed
Whitaker-Azmitia, P. M., & Azmitia, E. C. (1994). Astroglial 5-HT1a receptors and S-100 beta in development and plasticity. Perspectives on Developmental Neurobiology, 2, 233–238.Google ScholarPubMed
Whitaker-Azmitia, P. M., Druse, M., Walker, P., & Lauder, J. M. (1996). Serotonin as a developmental signal. Behavioural Brain Research, 73, 19–29.CrossRefGoogle ScholarPubMed
Winslow, J. T., Noble, P. L., Lyons, C. K., Sterk, S. M., & Insel, T. R. (2003). Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys. Neuropsychopharmacology, 5, 910–918.CrossRefGoogle Scholar
Wismer Fries, A. B, Ziegler, T., Kurian, J., Jacoris, S., & Pollak, S. D. (2005). Early experience in humans is associated with changes in neuro-peptides critical for regulating social behaviour. Proceedings of the National Academy of Sciences of the United States of America, 102, 17237–17240.CrossRefGoogle Scholar
Young, L. J., Wang, Z., Donaldson, R., & Rissman, E. F. (1998). Estrogen receptor alpha is essential for induction of oxytocin receptor by estrogen. NeuroReport, 9, 933–936.CrossRefGoogle ScholarPubMed
Zetterstrom, T. S., Pei, Q., Madhav, T. R., Coppell, A. L., Lewis, L., & Grahame-Smith, D. G. (1999). Manipulations of brain 5-HT levels affect gene expression for BDNF in rat brain. Neuropharmacology, 38, 1063–1073.CrossRefGoogle ScholarPubMed