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Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children

Published online by Cambridge University Press:  09 August 2006

MEGAN R. GUNNAR  and
PHILIP A. FISHER
MEGAN R. GUNNAR
Affiliation:
Institute of Child Development, University of Minnesota
PHILIP A. FISHER
Affiliation:
Oregon Social Learning Center
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Abstract

A major focus in developmental psychopathology is on understanding developmental mechanisms and, armed with this information, intervening to improve children's outcomes. Translational research attempts to bridge the distance between understanding and intervention. In the collaborations that have formed the core of our research network on early experience, stress, and prevention science, we have focused on translating basic research on early experiences and stress neurobiology into preventive interventions for neglected and abused children. Our experiences in attempting to move from bench to bedside have led us to recognize the many challenges that face translational researchers. This review provides a brief synopsis of the animal model literature on early experience and stress neurobiology from which we glean several key bridging issues. We then review what is currently known about the impact of childhood neglect and abuse on stress neurobiology in human adults and children. Next, we describe how this work has informed the evaluation of our preventive interventions with maltreated children. Finally, we discuss several considerations that should facilitate a more complete integration of basic research on early experience and stress neurobiology into preventive intervention strategies.This paper reflects the work of the Early Experience, Stress and Prevention Science Network (R21 MH65046), whose members are Mary Dozier, Philip Fisher, Nathan Fox, Megan Gunnar, Seymour Levine, Charles Neal, Seth Pollak, Paul Plotsky, Mar Sanchez, and Delia Vazquez. Preparation of this manuscript was supported by a Senior Scientist Award (K05 MH66208) to Megan Gunnar, and by MH59780 and MH65046, NIMH, U.S. PHS; MH46690, NIMH and ORMH, U.S. PHS; and DA17592, NIDA, NIH, U.S. PHS to Philip Fisher.

Type
Research Article
Information
Development and Psychopathology , Volume 18 , Issue 3 , September 2006 , pp. 651 - 677
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Alkon, A., Goldstein, L. H., Smider, N., Essex, M. J., Kupfer, D. J., & Boyce, W. T. (2003). Developmental and contextual influences on autonomic reactivity in young children. Developmental Psychobiology, 42, 64–78.Google Scholar
Barr, C. S., Newman, T. K., Shannon, C., Parker, C., Dvoskin, R. L., Becker, M. L., et al. (2004). Rearing condition and rh5-HTTLPR interact to influence limbic–hypothalamic–pituitary–adrenal axis response to stress in infant macaques. Biological Psychiatry, 55, 733–738.Google Scholar
Bauer, A. M., Quas, J. A., & Boyce, T. (2004). Associations between physiological activity and children's behavior: Advantage of a multisystems approach. Journal of Developmental and Behavioral Pediatrics, 23, 102–113.Google Scholar
Berntson, G. G., Cacioppo, J. T., Binkley, P. F., Uchino, B. N., & Quigley, K. S. (1994). Autonomic cardiac control. III. Psychological stress and cardiac response in autonomic space as revealed by psychopharmological blockades. Psychophysiology, 31, 599–608.Google Scholar
Brake, W. G., Zhang, T. Y., Diorio, J., Meaney, M., & Gratton, A. (2004). Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioural responses to psychostimulants and stressors in adult rats. European Journal of Neuroscience, 19, 1863–1874.Google Scholar
Bremner, J. D. (2002). Neuroimaging studies in post-traumatic stress disorder. Current Psychiatry Reports, 4, 254–263.Google Scholar
Bremner, J. D., Licino, J., Darnell, A., Krystal, J. H., Owens, M. J., Southwick, S. M., et al. (1997). Elevated CSF corticotropin-releasing factor concentrations in posttraumatic stress disorder. American Journal of Psychiatry, 154, 624–629.Google Scholar
Bremner, J. D., & Vermetten, E. (2001). Stress and development: Behavioral and biological consequences. Development and Psychopathology, 13, 473–490.Google Scholar
Bremner, J. D., Vythilingam, M., Vermetten, E., Southwick, S. M., McGlashan, T., Nazeer, A., et al. (2003). MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. American Journal of Psychiatry, 160, 924–932.Google Scholar
Brown, S. M., Henning, S., & Wellman, C. L. (2005). Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cerebral Cortex, 15, 1714–1722.Google Scholar
Bruce, J., Kroupina, M., Parker, S., & Gunnar, M. (2000). The relationships between cortisol patterns, growth retardation, and developmental delays in post-institutionalized children. Paper presented at the International Conference on Infant Studies, Brighton, UK.
Bruce, J., Tarullo, A. R., & Gunnar, M. (2005). Disinhibited social behavior among internationally adopted children. Unpublished manuscript.
Carrion, V. G., Weems, C. F., Eliez, S., Patwardhan, A., Brown, W., Ray, R. D., et al. (2001). Attenuation of front asymmetry in pediatric posttraumatic stress disorder. Biological Psychiatry, 50, 943–951.Google Scholar
Carrion, V. G., Weems, C. F., Ray, R. D., Glaser, B., Hessl, D., & Reiss, A. L. (2002). Diurnal salivary cortisol in pediatric posttraumatic stress disorder. Biological Psychiatry, 51, 575–582.Google Scholar
Casey, B. J., Castellanos, F. X., Giedd, J. N., Marsh, W. L., Hamburger, S. D., Schubert, A. B., et al. (1997). Implication of right frontostriatal circuitry in response inhibition and attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 36, 374–383.Google Scholar
Caspi, A., Sugden, K., Moffit, T., Taylor, A., Craig, I. W., Harrington, H., et al. (2003). Influence of life stress on depression: Moderation by a polymorphism in the 5-HTT gene. Science, 301, 386–389.Google Scholar
Chugani, H. T., Behen, M. E., Muzik, O., Juhasz, C., Nagy, F., & Chugani, D. C. (2001). Local brain functional activity following early deprivation: A study of postinstitutionalized Romanian orphans. NeuroImage, 14, 1290–1301.Google Scholar
Cicchetti, D. (1989). Developmental psychopathology: Past, present, and future. In D. Cicchetti (Ed.), Emergence of a discipline: Rochester Symposium on Developmental Psychopathology (Vol. 1, pp. 1–12). Hillsdale, NJ: Erlbaum.
Cicchetti, D. (1996). Child maltreatment: Implications for developmental theory and research. Human Development, 39, 18–39.Google Scholar
Cicchetti, D. (2005, August). Translating interdisciplinary research with high-risk families into preventive interventions. Paper presented at the American Psychological Association, Washington, DC.
Cicchetti, D., & Rogosch, F. A. (1997). The role of self-organization in the promotion of resilience in maltreated children. Development and Psychopathology, 9, 797–815.Google Scholar
Cicchetti, D., & Rogosch, F. A. (2001). Diverse patterns of neuroendocrine activity in maltreated children. Development and Psychopathology, 13, 677–693.Google Scholar
Cicchetti, D., & Tucker, D. (1994). Development and self-regulatory structures of the mind. Development and Psychopathology, 6, 533–549.Google Scholar
Curtis, W. J., & Cicchetti, D. (2003). Moving research on resilience into the 21st century: Theoretical and methodological considerations in examining the biological contributors to resilience. Development and Psychopathology, 15, 773–810.Google Scholar
Davidson, R. J. (2002). Anxiety and affective style: Role of prefrontal cortex and amygdala. Biological Psychiatry, 51, 68–80.Google Scholar
Davis, M., Walker, D. L., & Lee, Y. (1997). Roles of the amygdala and bed nucleus of the stria teminalis in fear and anxiety measured with the acoustic startle reflex. Annals of the New York Academy of Sciences, 821, 305–331.Google Scholar
De Bellis, M. D. (2001). Developmental traumatology: The psychobiological development of maltreated children and its implications for research, treatment, and policy. Development and Psychopathology, 13, 539–564.Google Scholar
De Bellis, M. D. (2005). The psychobiology of neglect. Child Maltreatment, 10, 150–172.Google Scholar
De Bellis, M. D., Baum, A. S., Birmaher, B., Keshavan, M. S., Eccard, C. H., Boring, A. M., et al. (1999). Developmental traumatology, Part 1: Biological stress systems. Biological Psychiatry, 9, 1259–1270.Google Scholar
De Bellis, M. D., Chrousos, G. P., Dorn, L. D., Burke, L., Helmers, K., Kling, M. A., et al. (1994). Adrenal axis dysregulation in sexually abused girls. Journal of Clinical Endocrinology and Metabolism, 78, 249–255.Google Scholar
De Bellis, M. D., Keshavan, M. S., Clark, D. B., Casey, B. J., Giedd, J. B., Boring, A. M., et al. (1999). Developmental traumatology, Part 2: Brain development. Biological Psychiatry, 45, 1271–1284.Google Scholar
de Kloet, E. R., Vreugdenhil, E., Oitzl, M., & Joels, A. (1998). Brain corticosteroid receptor balance in health and disease. Endocrine Reviews, 19, 269–301.Google Scholar
Dobbing, J. (1981). The later development of the brain and its vulnerability. In J. A. Davis & J. Dobbing (Eds.), Scientific foundations of paediatrics (pp. 744–759). London: Heinemann Medical Books.
Dozier, M. (2003). Attachment-based treatment for vulnerable children. Attachment and Human Development, 5, 253–257.Google Scholar
Dozier, M., Albus, K., Fisher, P. A., & Sepulveda, S. (2002). Intervention for foster parents: Implications for developmental theory. Development and Psychopathology, 14, 843–860.Google Scholar
Dozier, M., Peloso, E., Gordon, M. K., Manni, M., Gunnar, M. R., Stovall-McClough, K. C., et al. (in press). Foster children's diurnal production of cortisol: An exploratory study. Child Maltreatment.
Dozier, M., Peloso, E., Sepulveda, S., Manni, M., Lindhiem, O., Ackerman, J., et al. (in press). Preliminary evidence from a randomized clinical trial: Intervention effects on behavioral and biobehavioral regulation of young foster children. Journal of Social Issues.
Egeland, B., Yates, T., Appleyard, K., & van Dulmen, M. (2002). The long-term consequences of maltreatment in the early years: A developmental pathway model to antisocial behavior. Children's Services: Social Policy, Research, and Practice, 5, 249–260.Google Scholar
Fisher, P. A. (2005). Translational research on underlying mechanisms of risk among foster children: Implications for prevention science. Paper presented at the Society for Research on Child Development, Washington, DC.
Fisher, P. A., Burraston, B., & Pears, K. (2005). The early intervention foster care program: Permanent placement outcomes from a randomized trial. Child Maltreatment, 10, 61–71.Google Scholar
Fisher, P. A., Gunnar, M. R., Chamberlain, P., and Reid, J. B. (2000). Preventative intervention for maltreated preschoolers: Impact on children's behavior, neuroendocrine activity, and foster parent functioning. Journal of the American Academy of Child and Adolescent Psychiatry, 39, 1356–1364.Google Scholar
Fisher, P. A., Martin, J., Bruce, J., & Fox, N.A. (2006). Neurobehavioral functioning in preschool-aged foster children: Mapping risk and recovery. Manuscript submitted for publication.
Fowles, D., & Kochanska, G. (2000). Temperament as a moderator of pathways to conscience in children: The contribution of electrodermal activity. Psychophysiology, 37, 788–795.Google Scholar
Francis, D., Diorio, J., Plotsky, P. M., & Meaney, M. J. (2002). Environmental enrichment reverses the effects of maternal separation on stress reactivity. Journal of Neuroscience, 22, 7840–7843.Google Scholar
Friese, E., Hesse, J., Hellhammer, J., & Hellhammer, D. (2005). A new view on hypocortisolism. Psychoneuoendocrinology, 30, 1010–1016.Google Scholar
Girdler, S. S., Sherwood, A., Hinderliter, A., Leserman, J., Costello, N., Straneva, P. A., et al. (2003). Biologic correlates of abuse in women with premenstrual dysphoric disorder and healthy controls. Psychosomatic Medicine, 65, 849–856.Google Scholar
Goodyer, I. M., Park, R. J., Netherton, C. M., & Herbert, J. (2001). Possible role of cortisol and dehydroepiandrosterone in human development and psychopathology. British Journal of Psychiatry, 173, 243–249.Google Scholar
Granger, D., Kivlighan, K. T., Blair, C., El-Sheikh, M., Mize, J., Lisonbee, J. A., et al. (in press). Integrating the measure of salivary A-Amylase into studies of child health, development, and social relationships. Journal of Personal and Social Relationships.
Granger, D. A., Schwartz, E. B., Booth, A., Curran, M., & Zakaria, D. (1999). Assessing dehydroepiandrosterone in saliva: A simple radioimmunoassay for use in studies of children, adolescents and adults. Psychoneuroendocrinology, 24, 567–579.Google Scholar
Grillon, C., Pine, D., Bass, J. P., Lawley, M., Ellis, V., & Charney, D. (2005). Cortisol and DHEA-S associated with potentiated startle during aversive conditioning in humans. Psychopharmacology, 29, 1–8 [web preprint].Google Scholar
Gunnar, M. (2003). Integrating neuroscience and psychosocial approaches in the study of early experiences. In J. A. King, C. F. Ferris, & I. I. Lederhendler (Eds.), Roots of mental illness in children (Vol. 1008, pp. 238–247). New York: New York Academy of Sciences.
Gunnar, M., Broderson, L., Nachmias, M., Buss, K. A., & Rigatuso, J. (1996). Stress reactivity and attachment security. Developmental Psychobiology, 29, 191–204.Google Scholar
Gunnar, M., & Davis, E. P. (2003). The developmental psychobiology of stress and emotion in early childhood. In I. B. Weiner (Ser. Ed.) & R. M. Lerner, M. A. Easterbrooks, & J. Mistry (Vol. Eds.), Comprehensive handbook of psychology: Vol. 6. Developmental psychology (pp. 113–143). New York: Wiley.
Gunnar, M., & Donzella, B. (2002). Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology, 27, 199–220.Google Scholar
Gunnar, M., Morison, S. J., Chisholm, K., & Schuder, M. (2001). Long-term effects of institutional rearing on cortisol levels in adopted Romanian children. Development and Psychopathology, 13, 611–628.Google Scholar
Gunnar, M., & Vazquez, D. M. (2001). Low cortisol and a flattening of expected daytime rhythm: Potential indices of risk in human development. Development and Psychopathology, 13, 515–538.Google Scholar
Gunnar, M., & Vazquez, D. M. (2006). Stress neurobiology and developmental psychopathology. In D. Cicchetti & D. Cohen (Eds.), Developmental psychopathology: Developmental neuroscience (2nd ed., Vol. 2, pp. 533–577). New York: Wiley.
Hane, A. A., & Fox, N. A. (in press). Natural variations in maternal caregiving of human infants influence stress reactivity. Psychological Science.
Hariri, A., Mattay, V., Tessitore, A., Kolachana, B., Fera, F., Goldman, D., et al. (2002). Serotonin transporter genetic variation and the response of the human amygdala. Science, 297, 400–402.Google Scholar
Heim, C., Newport, D. J., Heit, S., Graham, Y. P., Wilcox, M. B., R., Miller, A. H., 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.Google Scholar
Heim, C., Owen, M. J., Plotsky, P. M., & Nemeroff, C. B. (1997). The role of early adverse life events in the etiology of depression and posttraumatic stress disorder: Focus on corticotropin-releasing factor. Annals of the New York Academy of Sciences, 821, 194–207.Google Scholar
Heim, C., Plotsky, P., & Nemeroff, C. B. (2004). The importance of studying the contributions of early adverse experiences to the neurobiological findings in depression. Neuropsychopharmacology, 29, 641–648.Google Scholar
Heinrichs, S. C., & Koob, G. F. (2004). Corticotropin-releasing factor in brain: A role in activation, arousal, and affect regulation. Journal of Pharmacology and Experimental Therapeutics, 311, 427–440.Google Scholar
Herman, J. P., & Cullinan, W. E. (1997). Neurocircuitry of stress: Central control of the hypothalamo–pituitary–adrenocortical axis. Trends in Neurosciences, 20, 78–84.Google Scholar
Indredavikm, M. S., Vik, T., Heyerdahl, S., Kulseng, S., & Brubakk, A. M. (2005). Psychiatric symptoms in low birth weight adolescents, assessed by screening questionnaires. European Child and Adolescent Psychiatry, 14, 226–236.Google Scholar
Ito, Y., Teicher, M. H., Glod, C. A., & Ackerman, E. (1998). Preliminary evidence for aberrant cortical development in abused children: A quantitative EEG study. Journal of Neuropsychiatry and Clinical Neuroscience, 10, 298–307.Google Scholar
Kalin, N. H., Larson, C., Shelton, S. E., & Davidson, R. J. (1998). Asymmetric frontal brain activity, cortisol, and behavior associated with fearful temperament in rhesus monkeys. Behavioral Neuroscience, 112, 286–292.Google Scholar
Kaufman, J., Birmaher, B., Perel, J., Dahl, R. E., Moreci, P., Nelson, B., et al. (1997). The corticotropin-releasing hormone challenge in depressed abused, depressed nonabused, and normal control children. Biological Psychiatry, 42, 669–679.Google Scholar
Kaufman, J., Yang, B. Z., Douglas-Palumberi, H., Houshyar, S., Lipschitz, D. K., J.H., &Gelernter, J. (2004). Social supports and serotonin transporter gene moderate depression in maltreated children. Proceedings of the National Academy of Sciences, 101, 17316–17321.Google Scholar
Kertes, D. A., Gunnar, M., & Madsen, N. J. (2006). Early deprivation and home basal cortisol levels: A study of internationally-adopted children. Unpublished manuscript.
Kinard, E. M. (1998). Methodological issues in assessing resilience in maltreated children. Child Abuse and Neglect, 22, 669–680.Google Scholar
Kivlighan, K. T., Wewerka, S., Gunnar, M., & Granger, D. A. (2006). Salivary alpha-amylase reactivity to the trier social stress test in children: Relation to cortisol and autonomic activity. Paper presented at the Society for Research in Adolescence, San Francisco.
Kreppner, J. A., O'Connor, T. G., & Rutter, M. (2001). Can inattention/overactivity be an institutional deprivation syndrome? Journal of Abnormal Child Psychology, 29, 513–528.Google Scholar
Lee, L. Y., Schulkin, J., & Davis, M. (1994). Effect of corticosterone on the enhancement of the acoustic startle reflex by corticotropin-releasing hormone. Brain Research, 666, 93–98.Google Scholar
Levine, S. (2005a). Stress: An historical perspective. In T. Steckler, N. Kalin, & J. M. H. M. Reul (Eds.), Handbook on stress, immunology and behavior (pp. 1–30). Amsterdam: Elsevier.
Levine, S. (2005b). Developmental determinants of sensitivity and resistance to stress. Psychoneuoendocrinology, 30, 939–946.Google Scholar
Lovic, V., & Fleming, A. S. (2004). Artificially-reared female rats show reduced prepulse inhibition and deficits in the attentional set shifting task-reversal of effects with maternal-like licking stimulation. Behavioural and Brain Research, 148, 209–219.Google Scholar
Lyons-Ruth, K. (2003). Dissociation and the parent–infant dialogue: A longitudinal perspective from attachment research. Journal of the American Psychoanalytic Association, 51, 883–911.Google Scholar
Makino, S., Gold, P. W., & Schulkin, J. (1994). Corticosterone effects on corticotropin-releasing hormone mRNA in the central nucleus of the amygdala and the parvocellular region of the paraventricular nucleus of the hypothalamus. Brain Research, 640, 105–112.Google Scholar
Manly, J. T., Kim, J. E., Rogosch, F. A., & Cicchetti, D. (2001). Dimensions of child maltreatment and children's adjustment: Contributions of developmental timing and subtype. Development and Psychopathology, 13, 759–782.Google Scholar
Marshall, P. J., Fox, N. A., & The Bucharest Early Intervention Project Core Group (2004). A comparison of the electroencephalogram between institutionalized and community children in Romania. Journal of Cognitive Neuroscience, 16, 1327–1338.Google Scholar
McCormack, K., Maestripieri, D., Plotsky, P. M., & Sánchez, M. M. (2003). Infant maltreatment in rhesus monkeys: Behavioral and neuroendocrine outcomes. Paper presented at the 40th Annual Meeting of the American College of Neuropsychopharmacology, Nashville, TN.
McEwen, B. (2000). Allostasis and allostatic load: Implications for neuropsychopharmacology. Neuropsychophrarmacology, 22, 108–124.Google Scholar
McFarlane, A., Clark, C. R., Bryant, R. A., Williams, L. M., Niaura, R., Paul, R. H., et al. (2005). The impact of early life stress on psychophysiological, personality and behavioral measures in 740 non-clinical subjects. Journal of Integrative Neuroscience, 4, 27–40.Google Scholar
Meaney, M., & Szyf, M. (2005). Environmental programming of stress responses through DNA methylation: Life at the interface between a dynamic environment and a fixed genome. Dialogues in Clinical Neuroscience, 7, 103–123.Google Scholar
Nachmias, M., Gunnar, M., Mangelsdorf, S., Parritz, R., & Buss, K. (1996). Behavioral inhibition and stress reactivity: Moderating role of attachment security. Child Development, 67, 508–522.Google Scholar
Nater, U. M., Rohleder, N., Gaab, J., Berger, S., Jud, A., Kirschbaum, C., et al. (2005). Human salivary alpha-amylase reactivity in a psychosocial stress paradigm. International Journal of Psychophysiology, 55, 333–342.Google Scholar
Nelson, E. E., McClure, E. B., Monk, C. S., Zarahn, E., Leibenluft, E., Pine, D. S., et al. (2003). Developmental differences in neuronal engagement during implicit encoding of emotional faces: An event-related fMRI study. Journal of Child Psychology and Psychiatry, 44, 1015–1024.Google Scholar
Page, T. (1999). The attachment partnership as conceptual base for exploring the impact of child maltreatment. Child and Adolescent Social Work Journal, 16, 419–437.Google Scholar
Palkovits, M. (1987). Organization of the stress response at the anatomical level. In E. R. de Kloet, V. M. Wiegant, & D. de Wied (Eds.), Progress in brain research (Vol. 72, pp. 47–55). Amsterdam: Elsevier Science.
Patterson, G. R., DeBaryshe, B. D., & Ramsey, E. (1989). A developmental perspective on antisocial behavior. American Psychologist, 44, 329–335.Google Scholar
Pears, K., & Fisher, P. A. (2005). Developmental, cognitive, and neuropsychological functioning in preschool-aged foster children: Associations with prior maltreatment and placement history. Journal of Developmental and Behavioral Pediatrics, 26, 112–122.Google Scholar
Phillips, D. I., Walker, B. R., Reynolds, R. M., Flanagan, D. E., Wood, P. J., Osmond, C., et al. (2000). Low birth weight predicts elevated plasma cortisol concentrations in adults from 3 populations. Hypertension, 35, 1301–1306.Google Scholar
Pollak, S. D. (2005). Early adversity and mechanisms of plasticity: Integrating affective neuroscience with developmental approaches to psychopathology. Development and Psychopathology, 17, 735–752.Google Scholar
Posner, M. I., & Petersen, S. E. (1990). The attention system of the human brain. Annual Review of Neuroscience, 13, 25–42.Google Scholar
Price, J. M., & Glad, K. (2003). Hostile attributional tendencies in maltreated children. Journal of Abnormal Child Psychology, 31, 329–343.Google Scholar
Putnam, F. W. (2003). Ten-year research update review: Child sexual abuse. Journal of the American Academy of Child and Adolescent Psychiatry, 42, 269–278.Google Scholar
Reid, J. B., & Eddy, J. M. (1997). The prevention of antisocial behavior: Some considerations in the search for effective interventions. In D. Stoff, J. Breiling, & J. Maser (Eds.), Handbook of antisocial behavior (pp. 343–356). New York: Wiley.
Reid, J. B., & Kavanagh, K. M. (1985). A social interactional approach to child abuse: Risk, prevention, and treatment. In M. Chesney & R. Rosenman (Eds.), Anger and hostility in behavioral and cardiovascular disorders (pp. 241–257). New York: McGraw–Hill.
Rinne, T., de Kloet, E. R., Wouters, L., Goekoop, J. G., DeRijk, R. H., & van den Brink, W. (2002). Hyperresponsiveness of hypothalamic–pituitary–adrenal axis to combined dexamethasone/corticotropin releasing hormone challenge in female borderline personality disorder subjects with a history of sustained child abuse. Biological Psychiatry, 52, 1102–1112.Google Scholar
Roceri, M., Cirulli, F., Pessina, C., Peretto, P., Racagni, G., & Riva, M. A. (2004). Postnatal repeated maternal deprivation produces age-dependent changes in brain-derived neurotrophic factor expression in selected rat brain regions. Biological Psychiatry, 55, 708–714.Google Scholar
Rosenblum, L., Smith, E., Altemus, M., Scharf, B., Owens, M., Nemeroff, C., et al. (2002). Differing concentrations of corticotropin-releasing factor and oxytocin in the cerebrospinal fluid of bonnet and pigtail macaques. Psychoneuroendocrinology, 27, 651–660.Google Scholar
Rosenfeld, P., Suchecki, D., & Levine, S. (1992). Multifactorial regulation of the hypothalamic–pituitary–adrenal axis during development. Neuroscience and Biobehavioral Reviews, 16, 553–568.Google Scholar
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, 419–450.Google Scholar
Sanchez, M. M., Lyon, C. K., Noble, P. L., Crawford, J. L., Boudreau, M., Higley, J. D., et al. (2005). Maternal separation alters the HPA axis function in rhesus macaques: Effects of sex and serotonin transporter gene variation. Abstract presented at the 60th Annual Meeting of the Society of Biological Psychiatry, Atlanta, GA.
Sanchez, M. M., McCormack, K., Plotsky, P. M., & Maestripieri, D. (2004). The effects of abuse and neglect on diurnal plasma cortisol rhythms in year-old rhesus monkeys. Paper presented at The Network on Early Experiences, Stress, and Prevention Science, Madison, WI.
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 nonhuman primates with adverse rearing. Biological Psychiatry, 57, 373–381.Google Scholar
Sapolsky, R. M., & Meaney, M. J. (1986). Maturation of the adrenocortical stress response: Neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Research Reviews, 11, 65–76.Google Scholar
Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21, 55–89.Google Scholar
Scheeringa, M. S., Zeanah, C. H., Myers, L., & Putnam, F. W. (2005). Predictive validity in a prospective follow-up of PTSD in preschool children. Journal of the American Academy of Child and Adolescent Psychiatry, 44, 899–906.Google Scholar
Schrijver, N. C., Pallier, P. M., Brown, V. J., & Wurbel, H. (2004). Double dissociation of social and environmental stimulation on spatial learning and reversal learning in rats. Behavioral Brain Research, 152, 307–314.Google Scholar
Schulkin, J., McEwen, B. S., & Gold, P. W. (1994). Allostasis, amygdala, and anticipatory angst. Neuroscience and Biobehavioral Reviews, 18, 385–396.Google Scholar
Shea, A., Walsh, C., Macmillan, H., & Steiner, M. (2005). Child maltreatment and HPA axis dysregulation: Relationship to major depressive disorder and post traumatic stress disorder in females. Psychoneuoendocrinology, 30, 162–178.Google Scholar
Siegel, S. J., Ginsberg, S. D., Hof, P. R., Foote, S. L., Young, W. G., Kraemer, G., et al. (1993). Effects of social deprivation in prepubescent rhesus monkeys: Immunohistochemical analysis of neurofilament protein triplet in the hippocampal formation. Brain Research, 13, 229–305.Google Scholar
Stovall, K. C., & Dozier, M. (2000). The development of attachment in new relationships: Single subject analyses for 10 foster infants. Development and Psychopathology, 12, 133–156.Google Scholar
Strauman, T. J., & Merrill, K. A. (2004). The basic science/clinical science interface and treatment development. Clinical Psychology: Science and Practice, 11, 263–266.Google Scholar
Suchecki, D., Rosenfeld, P., & Levine, S. (1993). Maternal regulation of the hypothalamic–pituitary–adrenal axis in the rat: The roles of feeding and stroking. Developmental Brain Research, 75, 185–192.Google Scholar
Sullivan, R. M., & Gratton, A. (2002). Prefrontal cortical regulation of hypothalamic–pituitary–adrenal function in the rat and implications for psychopathology: Side matters. Psychoneuroendocrinology, 27, 99–114.Google Scholar
Teicher, M. H., Andersen, S. L., Polcarri, A., Anderson, C. M., & Navalta, C. P. (2002). Developmental neurobiology of childhood stress and trauma. Psychiatric Clinics of North America, 25, 397–426.Google Scholar
Teicher, M. H., Ito, Y., Glod, C. A., Andersen, S. L., Dumont, N., & Ackerman, E. (1997). Preliminary evidence for abnormal cortical development in physically and sexually abused children using EEG coherence and MRI. Annals of the New York Academy of Sciences, 821, 160–175.Google Scholar
Thompson, R. J., Goldstein, R. F., Oehler, J. M., Gustafson, K. E., Catlett, T., & Brazy, J. E. (1994). Developmental outcome of very low birth weight infants as a function of biological risk and psychosocial risk. Development and Behavioral Pediatrics, 15, 91–96.Google Scholar
Tieman, W., van der Ende, J., & Verhulst, F. C. (2005). Psychiatric disorders in young adult intercountry adoptees: An epidemiological study. American Journal of Psychiatry, 162, 592–598.Google Scholar
Van Bockstaele, E. J., Colago, E. E., & Valentino, R. J. (1998). Amygdaloid corticotropin-releasing factor targets locus coeruleus dendrites: Substrate for the co-ordination of emotional and cognitive limbs of the stress response. Journal of Neuroendocrinology, 10, 743–757.Google Scholar
van de Wiel, N. M., van Goozen, S. H., Matthys, W., Snoek, H., & van Engeland, H. (2004). Cortisol and treatment effect in children with disruptive behavior disorders: A preliminary study. Journal of the American Academy of Child and Adolescent Psychiatry, 43, 1011–1018.Google Scholar
van Goozen, S. H., Matthys, W., Cohen-Kettenis, P. T., Buittelaar, J. K., & van Engeland, H. (2000). Hypothalamic–pituitary–adrenal axis and autonomic nervous system activity in disruptive children and matched controls. Journal American Academy of Child and Adolescent Psychiatry, 39, 1438–1445.Google Scholar
Wadhwa, P. D. (2005). Psychoneuroendocrine processes in human pregnancy influence fetal development and health. Psychoneuoendocrinology, 30, 724–743.Google Scholar
Weaver, I. C., Champagne, F. A., Brown, S. E., Dymov, S., Sharma, S., Meaney, M. J., et al. (2005). Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: Altering epigenetic marking later in life. Journal of Neuroscience, 25, 11045–11054.Google Scholar
Yehuda, R. (2000). Biology of posttraumatic stress disorder. Journal of Clinical Psychiatry, 61(Suppl. 7), 15–21.Google Scholar
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.Google Scholar
Zeanah, C. H., Nelson, C. A., Fox, N. A., Smyke, A. T., Marshall, P. M., Parker, S. W., et al. (2003). Designing research to study the effects of institutionalization on brain and behavioral development: The Bucharest Early Intervention Project. Development and Psychopathology, 15, 885–907.Google Scholar