When mothering goes awry: Challenges and opportunities for utilizing evidence across rodent, nonhuman primate and human studies to better define the biological consequences of negative early caregiving

Hormones and Behavior - Tập 77 - Trang 182-192 - 2016
Stacy S. Drury1, Mar M. Sánchez2,3, Andrea Gonzalez4
1Tulane University School of Medicine, Department of Psychiatry and Behavioral Sciences, 1430 Tulane Ave, #8055, New Orleans, LA 70112, United States
2Department of Psychiatry & Behavioral Science, School of Medicine, Emory University, Atlanta, GA 20322, United States
3Yerkes National Primate Research Center, Emory University, Atlanta, GA 20329, United States
4Offord Centre for Child Studies, McMaster University, Department of Psychiatry and Behavioural Neurosciences, 1280 Main Street West, Hamilton, ON, L8S 4K1, Canada

Tài liệu tham khảo

Allman, 1998, Parenting and survival in anthropoid primates: caretakers live longer, Proc. Natl. Acad. Sci., 95, 6866, 10.1073/pnas.95.12.6866 Andersen, 2003, Trajectories of brain development: point of vulnerability or window of opportunity?, Neurosci. Biobehav. Rev., 27, 3, 10.1016/S0149-7634(03)00005-8 Anderson, 2012, Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation, J. Nutr. Biochem., 23, 853, 10.1016/j.jnutbio.2012.03.003 Arabadzisz, 2010, Primate early life stress leads to long-term mild hippocampal decreases in corticosteroid receptor expression, Biol. Psychiat., 67, 1106, 10.1016/j.biopsych.2009.12.016 Arata, 2007, Differential correlates of multi-type maltreatment among urban youth, Child Abuse Negl., 31, 393, 10.1016/j.chiabu.2006.09.006 Atkinson, 2012, Maternal sensitivity and infant and mother adrenocortical function across challenges, Psychoneuroendocrinology, 38, 2943, 10.1016/j.psyneuen.2013.08.001 Avishai-Eliner, 2002, Stressed-out, or in (utero)?, Trends Neurosci., 25, 518, 10.1016/S0166-2236(02)02241-5 Avishai-Eliner, 1995, Effects of maternal and sibling deprivation on basal and stress induced hypothalamic-pituitary-adrenal components in the infant rat, Neurosci. Lett., 192, 49, 10.1016/0304-3940(95)11606-W Bale, 2010, Early life programming and neurodevelopmental disorders, Biol. Psychiatry, 68, 314, 10.1016/j.biopsych.2010.05.028 Beach, 2010, Methylation at SLC6A4 is linked to a family history of child abuse: an examination of the Iowa adoptee sample. American Journal of Medical Genetics B, Neuropsychiatr. Gen., 153B, 710 Belay, 2011, Early adversity and serotonin transporter genotype interact with hippocampal glucocoricoid receptor mRNA expression, corticosterone, and behavior in adult male rats, Behav. Neurosci., 125, 150, 10.1037/a0022891 Bernard, 2014, Intervening to enhance cortisol regulation among children at risk for neglect: results of a randomized clinical trial, Dev. Psychopathol., 1-13 Bernard, 2012, Enhancing attachment organization among maltreated children: results of a randomized clinical trial, Child Dev., 83, 623, 10.1111/j.1467-8624.2011.01712.x Bernard, 2015, Intervention effects on diurnal cortisol rhythms of child protective services–referred infants in early childhood preschool follow-up results of a randomized clinical trial, JAMA Pediatr., 169, 112, 10.1001/jamapediatrics.2014.2369 Bick, 2015, Effect of early institutionalization and foster care on long-term white matter development: a randomized clinical trial, JAMA Pediatr., 10.1001/jamapediatrics.2014.3212 Bick, 2015, A randomized clinical trial of foster care as an intervention for early institutionalization: long term improvements in white matter microstructure, JAMA Pediatr., 169, 211, 10.1001/jamapediatrics.2014.3212 Brent, 2002, Abnormal, abusive, and stress-related behaviors in baboon mothers, Biol. Psychiat., 52, 1047, 10.1016/S0006-3223(02)01540-8 Brett, 2015, Using cross species comparisons and a neurobiological framework to understand early social deprivation effects on behavioral development, Dev. Psychopathol., 27, 347, 10.1017/S0954579415000036 Brett, 2014, A neurogenetics approach to defining differential susceptibility to institutional care. International, J. Behav. Dev. Bremner, 2003, Long-term effects of childhood abuse on brain and neurobiology, Child and adolescent psychiatric clinics of North America, 12, 271, 10.1016/S1056-4993(02)00098-6 Bremner, 2007 Brunson, 2005, Mechanisms of late-onset cognitive decline after early-life stress., J. Neurosci., 25, 9328, 10.1523/JNEUROSCI.2281-05.2005 Bublitz, 2012, Childhood sexual abuse is associated with cortisol awakening response over pregnancy: preliminary findings, Psychoneuroendocrinology, 37, 1425, 10.1016/j.psyneuen.2012.01.009 Burghy, 2012, Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence, Nature Neurosci., 15, 1736, 10.1038/nn.3257 Burton, 2007, Prenatal restraint stress and motherless rearing disrupts expression of plasticity markers and stress-induced corticosterone release in adult female Sprague–Dawley rats, Brain Res., 1158, 28, 10.1016/j.brainres.2007.05.003 Cao-Lei, 2014, DNA methylation signatures triggered by prenatal maternal stress exposure to a natural disaster: project ice storm, PLoS One, 9, e107653, 10.1371/journal.pone.0107653 Carpenter, 2007, Decreased adrenocorticotropic hormone and cortisol responses to stress in healthy adults reporting a significant childhood maltreatment, Biol. Psychiatry, 62, 1080, 10.1016/j.biopsych.2007.05.002 Carpenter, 2011, Effect of childhood physical abuse on cortisol stress response, Psychopharmacology, 214, 367, 10.1007/s00213-010-2007-4 Champagne, 2003, Variations in maternal care in the rat as a mediating influence for the effects of environment on development, Physiol. Behav., 79, 359, 10.1016/S0031-9384(03)00149-5 Cohen, 2013, Early-life stress has persistent effects on amygdala function and development in mice and humans, Proc. Natl. Acad. Sci., 110, 18274, 10.1073/pnas.1310163110 Coplan, 2010, The role of early life stress in development of the anterior limb of the internal capsule in nonhuman primates, Neurosci. Lett., 480, 93, 10.1016/j.neulet.2010.06.012 Coplan, 2001, Variable foraging demand rearing: sustained elevations in cisternal cerebrospinal fluid corticotropin-releasing factor concentrations in adult primates, Biol. Psychiatry, 50, 200, 10.1016/S0006-3223(01)01175-1 Coplan, 1998, Cerebrospinal fluid concentrations of somatostatin and biogenic amines in grown primates reared by mothers exposed to manipulated foraging conditions, Arch. Gen. Psychiatry, 55, 473, 10.1001/archpsyc.55.5.473 Coplan, 1996, Persistent elevations of cerebrospinal fluid concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors: implications for the pathophysiology of mood and anxiety disorders, Proc. Natl. Acad. Sci. U. S. A., 93, 1619, 10.1073/pnas.93.4.1619 Daniels, 2009, Maternal separation alters nerve growth factor and corticosterone levels but not the DNA methylation status of the exon 17 glucocorticoid receptor promoter region, Metab. Brain Dis., 24, 615, 10.1007/s11011-009-9163-4 Dannlowski, 2012, Limbic scars: long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging, Biol. Psychiatry, 71, 286, 10.1016/j.biopsych.2011.10.021 De Bellis, 2005, The psychobiology of neglect, Child Maltreat., 10, 150, 10.1177/1077559505275116 De Bellis, 1999, A.E. Bennett Research Award. Developmental traumatology. Part I: biological stress systems, Biol. Psychaitry, 45, 1259, 10.1016/S0006-3223(99)00044-X De Bellis, 1999, A.E, Bennett Research Award. Developmental traumatology. Part II: brain development, Biol. Psychiatry, 45 Desarnaud, 2008, Stress downregulates hippocampal expression of the adhesion molecules NCAM and CHL1 in mice by mechanisms independent of DNA methylation of their promoters, Cell Adhes. Migr., 2, 38, 10.4161/cam.2.1.6013 Dettling, 2002, Repeated parental deprivation in the infant common marmoset (Callithrix jacchus, primates) and analysis of its effects on early development, Biol. Psychiatry, 52, 1037, 10.1016/S0006-3223(02)01460-9 Devlin, 2010, Prenatal exposure to maternal depressed mood and the mthfr c677t variant affect SLC6A4 methylation in infants at birth, PLoS One, 5, e12201, 10.1371/journal.pone.0012201 Doom, 2014, Longitudinal patterns of cortisol regulation differ in maltreated and nonmaltreated children, J. Am. Acad. Child Adolesc. Psychiatry, 53, 1206, 10.1016/j.jaac.2014.08.006 Dozier, 2008, Effects of an attachment-based intervention on the cortisol production of infants and toddlers in foster care, Dev. Psychopathol., 20, 845, 10.1017/S0954579408000400 Drevets, 2008, Neuroimaging studies of mood, Neurobiol. Ment. Illn., 461 Eads, 2000, MethyLight: a high-throughput assay to measure DNA methylation, Nucleic Acids Res., 28, 10.1093/nar/28.8.e32 Eghbal-Ahmadi, 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, J. Neurosci., 19, 3982, 10.1523/JNEUROSCI.19-10-03982.1999 Fallon, 2010, Methodological challenges in measuring child maltreatment, Child Abuse Negl., 34, 70, 10.1016/j.chiabu.2009.08.008 Fan, 2014, Early life stress modulates amygdala-prefrontal functional connectivity: implications for oxytocin effects, Hum. Brain Mapp., 35, 5328, 10.1002/hbm.22553 Felitti, 1998, Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults: the Adverse Childhood Experiences (ACE) Study, Am. J. Prev. Med., 14, 245, 10.1016/S0749-3797(98)00017-8 Feng, 2011, Maternal separation produces lasting changes in cortisol and behavior in rhesus monkeys, Proc. Natl. Acad. Sci. U. S. A., 109, 1 Fenoglio, 2005, Enduring, handling-evoked enhancement of hippocampal memory function and glucocorticoid receptor expression involves activation of the corticotropin-releasing factor type 1 receptor, Endocrinology, 146, 4090, 10.1210/en.2004-1285 Fisher, 1955 Fisher, 2007, Effects of a therapeutic intervention for foster preschoolers on diurnal cortisol activity, Psychoneuroendocrinology, 32, 892, 10.1016/j.psyneuen.2007.06.008 Fisher, 2011, Mitigating HPA axis dysregulation associated with placement changes in foster care, Psychoneuroendocrinology, 36, 531, 10.1016/j.psyneuen.2010.08.007 Francis, 1999, Nongenomic transmission across generations of maternal behavior and stress responses in the rat, Science, 286, 1155, 10.1126/science.286.5442.1155 Gee, 2014, Maternal buffering of human amygdala-prefrontal circuitry during childhood but not during adolescence, Psychol. Sci., 10.1177/0956797614550878 Gee, 2013, A developmental shift from positive to negative connectivity in human amygdala–prefrontal circuitry, J. Neurosci., 33, 4584, 10.1523/JNEUROSCI.3446-12.2013 Giedd, 2004, Structural magnetic resonance imaging of the adolescent brain, Ann. N. Y. Acad. Sci., 1021, 77, 10.1196/annals.1308.009 Giedd, 2010, Structural MRI of pediatric brain development: what have we learned and where are we going?, Neuron, 67, 728, 10.1016/j.neuron.2010.08.040 Gogtay, 2004, Dynamic mapping of human cortical development during childhood through early adulthood, Proc. Natl. Acad. Sci. U. S. A., 101, 8174, 10.1073/pnas.0402680101 Gonzalez, 2001, Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats, Dev. Psychobiol., 38, 11, 10.1002/1098-2302(2001)38:1<11::AID-DEV2>3.0.CO;2-B Gunnar, 2002, Social regulation of the cortisol levels in early human development, Psychoneuroendocrinology, 27, 199, 10.1016/S0306-4530(01)00045-2 Gunnar, 2006, Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children, Dev. Psychopathol., 18, 651, 10.1017/S0954579406060330 Gunnar, 2015, Parental buffering of fear and stress neurobiology: reviewing parallels across rodent, NHP and human models, Soc. Neurosci., 1 Guo, 2011, Neuronal activity modifies the DNA methylation landscape in the adult brain, Nat. Neurosci., 14, 1345, 10.1038/nn.2900 Harlow, 1965, The affectional systems Harris, 2010, Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications, Nat. Biotechnol., 28, 1097, 10.1038/nbt.1682 Heim, 2001, The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies, Biol. Psychiatry, 49, 1023, 10.1016/S0006-3223(01)01157-X Heim, 2002, The role of early adverse experience and adulthood stress in the prediction of neuroendocrine stress reactivity in women: a multiple regression analysis, Depress. Anxiety, 15, 117, 10.1002/da.10015 Helfer, 1997 Hemmingsson, 2014, Effects of childhood abuse on adult obesity: a systematic review and meta-analysis, Obesity Rev., 15, 882, 10.1111/obr.12216 Herman, 2003, Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo–pituitary–adrenocortical responsiveness, Front. Neuroendocrinol., 24, 151, 10.1016/j.yfrne.2003.07.001 Herman, 2005, Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis, Prog. Neuro-Psychopharmacol. Biol. Psychiatry, 29, 1201, 10.1016/j.pnpbp.2005.08.006 Herringa, 2013, Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence, Proc. Natl. Acad. Sci., 110, 19119, 10.1073/pnas.1310766110 Hofer, 1984, Relationships as regulators: a psychobiologic perspective on bereavement, Psychosom. Med., 46, 183, 10.1097/00006842-198405000-00001 Hostinar, 2014, Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: a review of animal models and human studies across development, Psychol. Bull., 140, 256, 10.1037/a0032671 Howell, 2014, Early adverse experience increases emotional reactivity in juvenile rhesus macaques: relation to amygdala volume, Dev. Sychobiol., 56, 1735, 10.1002/dev.21237 Howell, 2013, Brain white matter microstructure alterations in adolescent rhesus monkeys exposed to early life stress: associations with high cortisol during infancy, Biol. Mood Anxiety Disord., 3, 10.1186/2045-5380-3-21 Howell, 2011, Understanding behavioral effects of early life stress using the reactive scope and allostatic load models, Dev. Sychopathol., 23, 1001, 10.1017/S0954579411000460 Humphreys, 2014, Deviations from the expectable environment in early childhood and emerging psychopathology, Neuropsychopharmacology Ivy, 2008, Dysfunctional nurturing behaivor in rat dams with limited access to nesting material: a clinically relevant model of early-life stress., Neuroscience, 154, 1132, 10.1016/j.neuroscience.2008.04.019 Jackowski, 2011, Early-life stress, corpus callosum development, hippocampal volumetrics, and anxious behavior in male nonhuman primates, Psychiatry Res. Neuroimaging, 192, 37, 10.1016/j.pscychresns.2010.11.006 Jansen, 2010, Cortisol reactivity in young infants, Psychoneuroendocrinology, 35, 329, 10.1016/j.psyneuen.2009.07.008 Johnson, 1996, Effects of early parenting on growth and development in a small primate, Pediatrc. Res., 39, 999, 10.1203/00006450-199606000-00012 Kaffman, 2007, Neurodevelopmental sequelae of postnatal maternal care in rodents: clinical and research implications of molecular insights, J. Child Psychol. Psychiatry, 48, 224, 10.1111/j.1469-7610.2007.01730.x Kember, 2012, Maternal separation is associated with strain-specific responses to stress and epigenetic alterations to Nr3c1, Avp, and Nr4a1 in mouse, Brain Behav., 2, 455, 10.1002/brb3.69 Kinnally, 2014, Epigenetic plasticity following early stress predicts long-term health outcomes in rhesus macaques, Am. Phys. Anthropol., 155, 192, 10.1002/ajpa.22565 Kinnally, 2010, Epigenetic regulation of serotonin transporter expression and behavior in infant rhesus macaques, Genes Brain Behav., 9, 575, 10.1111/j.1601-183X.2009.00533.x Knudsen, 2004, Sensitive periods in the development of the brain and behavior, J. Cogn. Neurosci., 16, 1412, 10.1162/0898929042304796 Koch, 2014, The development of the hypothalamic-pituitary-adrenal axis in rhesus monkeys: effects of age, sex, and early experience, Dev. Psychobiol., 56, 86, 10.1002/dev.21093 Korosi, 2009, The pathways from mother's love to baby's future, Front. Behav. Neurosci., 3, 10.3389/neuro.08.027.2009 Kuhn, 1991, Tactile-kinesthetic stimulation effects on sympathetic and adrenocortical function in preterm infants, J. Pediatr., 119, 434, 10.1016/S0022-3476(05)82059-1 Kundakovic, 2013, Sex-specific and strain-dependent effects of early life adversity on behavioral and epigenetic outcomes, Front. Psychiatry, 4 Ladd, 2004, Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation, Biol. Psychiatry, 55, 367, 10.1016/j.biopsych.2003.10.007 Laurent, 2014, HPA stability for children in foster care: mental health implications and moderation by early intervention, Dev. Psychobiol., 56, 1406 Law, 2009, Gene expression in the anterior cingulate cortex and amygdala of adolescent marmoset monkeys following parental separations in infancy, Int. J. Neuropsychopharmacol., 12, 761, 10.1017/S1461145708009723 Law, 2009, Early parental deprivation in the marmoset monkey produces long-term changes in hippocampal expression of genes involved in synaptic plasticity and implicated in mood disorder, Neuropsychopharmacology, 34, 1381, 10.1038/npp.2008.106 Lister, 2009, Human DNA methylomes at base resolution show widespread epigenomic differences, Nature, 462, 315, 10.1038/nature08514 Liu, 2000, Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus, J. Neuroendocrinol., 12, 5, 10.1046/j.1365-2826.2000.00422.x Lupien, 2009, Effects of stress throughout the lifespan on the brain, behaviour and cognition, Nat. Rev. Neurosci., 10, 434, 10.1038/nrn2639 Machado, 2003, Non-human primate models of childhood psychopathology: the promise and the limitations, J. Child Psychol. Psychiatry, 44, 64, 10.1111/1469-7610.00103 Maestripieri, 1998, Parenting styles of abusive mothers in group-living rhesus macaques, Animal Behav., 55, 1, 10.1006/anbe.1997.0578 Maestripieri, 2005, Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys, Proc. Natl. Acad. Sci., 102, 9726, 10.1073/pnas.0504122102 Maestripieri, 1998, Risk factors for infant abuse and neglect in group-living rhesus monkeys, Psychol. Sci., 9, 143-143, 10.1111/1467-9280.00027 Maestripieri, 2000, Adoption and maltreatment of foster infants by rhesus macaque abusive mothers, Dev. Sci., 3, 287, 10.1111/1467-7687.00122 Massart, 2014, The genome-wide landscape of DNA methylation and hydroxymethylation in response to sleep deprivation impacts on synaptic plasticity genes, Transl. Psychiatry, 4, e347, 10.1038/tp.2013.120 Massart, 2014, Hydroxymethylation and DNA methylation profiles in the prefrontal cortex of the non-human primate rhesus macaque and the impact of maternal deprivation on hydroxymethylation, Neuroscience, 268, 139, 10.1016/j.neuroscience.2014.03.021 Mathew, 2003, A magnetic resonance spectroscopic imaging study of adult nonhuman primates exposed to early-life stressors, Biol. Psychiatry, 54, 727, 10.1016/S0006-3223(03)00004-0 McCormack, 2003, Behavioral and neuroendocrine outcomes of infant maltreatment in rhesus monkeys: the first four months, Soc. Neurosci., 14 McCormack, 2006, Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6months of life, Devel. Psychobiol., 48, 537, 10.1002/dev.20157 McCrory, 2012, The link between child abuse and psychopathology: a review of neurobiological and genetic research, J. R. Soc. Med., 105, 151, 10.1258/jrsm.2011.110222 McCrory, 2013 McGowan, 2009, Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse, Nat. Neurosci., 12, 342, 10.1038/nn.2270 McGowan, 2011, Broad epigenetic signature of maternal care in the brain of adult rats, PLoS One, 6, e14739, 10.1371/journal.pone.0014739 McLaughlin, 2014, Childhood adversity and neural development: deprivation and threat as distinct dimensions of early experience, Neurosci. Biobehav. Rev., 47, 578, 10.1016/j.neubiorev.2014.10.012 McLaughlin, 2015, Causal effects of the early caregiving environment on development of stress response systems in children, Proc. Natl. Acad. Sci., 201423363 Meaney, 2001, Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations, Annu. Rev. Neurosci., 24, 1161, 10.1146/annurev.neuro.24.1.1161 Mehta, 2013, Childhood maltreatment is associated with distinct genomic and epigenetic profiles in posttraumatic stress disorder, Proc. Natl. Acad. Sci., 110, 8302, 10.1073/pnas.1217750110 Merrick, 2013, Examining the role of safe, stable, and nurturing relationships in the intergenerational continuity of child maltreatment—introduction to the special issue, J. Adolesc. Health, 53, S1, 10.1016/j.jadohealth.2013.06.017 Molet, 2014, Naturalistic rodent models of chronic early-life stress, Dev. Psychobiol., 56, 1675, 10.1002/dev.21230 Moriceau, 2005, Neurobiology of infant attachment, Devel. Psychobiol., 47, 230, 10.1002/dev.20093 Nieratschker, 2014, MORC1 exhibits cross-species differential methylation in association with early life stress as well as genome-wide association with MDD, Transl. Psychiatry, 4, e429, 10.1038/tp.2014.75 Nikulina, 2014, Do race, neglect, and childhood poverty predict physical health in adulthood? A multilevel prospective analysis, Child Abuse Negl., 38, 414, 10.1016/j.chiabu.2013.09.007 Non, 2015 Numata, 2012, DNA methylation signatures in development and aging of the human prefrontal cortex, Am. J. Hum. Gen., 90, 260, 10.1016/j.ajhg.2011.12.020 O'Connor, 2006, Translating research findings on early experience to prevention: animal and human evidence on early attachment relationships, Am. J. Prevent. Med., 31, 175, 10.1016/j.amepre.2006.07.005 Parker, 2011, Identifying key features of early stressful experiences that produce stress vulnerability and resilience in primates, Neurosc. Biobehav. Rev., 35, 1466, 10.1016/j.neubiorev.2010.09.003 Perroud, 2014, Childhood maltreatment and methylation of the glucocorticoid receptor gene NR3C1 in bipolar disorder, Br. J. Psychiatry, 204, 30, 10.1192/bjp.bp.112.120055 Perroud, 2013, Response to psychotherapy in borderline personality disorder and methylation status of the BDNF gene, Transl. Psychiatry, 3, e207, 10.1038/tp.2012.140 Perry, 2014, Neurobiology of attachment to an abusive caregiver: Short-term benefits and long-term costs, Dev. psychobiol., 56, 1626, 10.1002/dev.21219 Provençal, 2012, The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells, J. Neurosci., 32, 15626, 10.1523/JNEUROSCI.1470-12.2012 Power, 2012, Childhood psychosocial adversity and adult cortisol patterns, Br. J. Psychiatry, 201, 199, 10.1192/bjp.bp.111.096032 Pryce, 2008, Postnatal ontogeny of expression of the corticosteroid receptor genes in mammalian brains: inter-species and intra-species differences, Brain Res. Rev., 57, 596, 10.1016/j.brainresrev.2007.08.005 Pryce, 2005, Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research, Neurosci. Biobehav. Rev., 29, 649, 10.1016/j.neubiorev.2005.03.011 Raineki, 2012, Effects of early life abuse differ across development: infant social behavior deficits are followed by adolescent depressive-like behaviors mediated by the amygdala, J. Neurosci., 32, 7758, 10.1523/JNEUROSCI.5843-11.2012 Raineki, 2014, Neonatal handling: an overview of the positive and negative effects, Dev. Psychobiol., 56, 1613, 10.1002/dev.21241 Raineki, 2010, Developing a neurobehavioral animal model of infant attachment to an abusive caregiver, Biol. Psychiatry, 67, 1137, 10.1016/j.biopsych.2009.12.019 Raper, 2014, Neonatal amygdala lesions lead to increased activity of brain CRF systems and hypothalamic-pituitary-adrenal axis of juvenile rhesus monkeys, J. Neurosci., 34, 11452, 10.1523/JNEUROSCI.0269-14.2014 Rice, 2008, A novel mouse model for acute and long-lasting consequences of early life stress, Endocrinology, 149, 4892, 10.1210/en.2008-0633 Rice, 2000, Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models, Environ. Health Perspect., 108, 511 Rich-Edwards, 2012, Physical and sexual abuse in childhood as predictors of early onset cardiovascular events in women, Circulation, 10.1161/CIRCULATIONAHA.111.076877 Rincon-Cortes, 2014, Early life trauma and attachment: immediate and enduring effects on neurobehavioral and stress axis development, Front. Endocrinol., 5, 33 Romens, 2014 Rosenfeld, 1992, Multifactorial regulation of the hypothalamic-pituitary-adrenal axis during development, Neurosci. Biobehav. Rev., 16, 553, 10.1016/S0149-7634(05)80196-4 Roth, 2014, Bdnf DNA methylation modifications in the hippocampus and amygdala of male and female rats exposed to different caregiving environments outside the homecage, Dev. Psychobiol., 10.1002/dev.21218 Roth, 2009, Lasting epigenetic influence of early-life adversity on BDNF gene, Biol. Psychiatry, 65, 760, 10.1016/j.biopsych.2008.11.028 Sanchez, 2010, Cerebral blood flow velocity and language functioning in pediatric sickle cell disease, J. Int. Neuropsychol. Soc., 16, 326, 10.1017/S1355617709991366 Sanchez, 2006, The impact of early adverse care on HPA axis development: nonhuman primate models, Horm. Behav., 50, 623, 10.1016/j.yhbeh.2006.06.012 Sanchez, 2010, Effects of sex and early maternal abuse on adrenocorticotropin hormone and cortisol responses to the corticotropin-releasing hormone challenge during the first 3years of life in group-living rhesus monkeys, Dev. Psychopathol., 22, 45, 10.1017/S0954579409990253 Sanchez, 2015, Social Buffering of Stress Responses in Nonhuman Primates: Maternal Regulation of Development of Emotional Egulatory Brain Circuits, Soc. Neurosci, 10, 474, 10.1080/17470919.2015.1087426 Sanchez, 2005, Alterations in diurnal cortisol rhythm and acoustic startle response in nonhuman primates wtih adverse rearing, Biol. Psychiatry, 57, 373, 10.1016/j.biopsych.2004.11.032 Sánchez, 2001, Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models, Dev. Psychopathol., 13, 419, 10.1017/S0954579401003029 Sarro, 2014, Maternal regulation of infant brain state, Curr. Biol., 24, 1664, 10.1016/j.cub.2014.06.017 Schwarz, 2010, Developmental and hormone-induced epigenetic changes to estrogen and progesterone receptor genes in brain are dynamic across the life span, Endocrinology, 151, 4871, 10.1210/en.2010-0142 Sclafani, 2015, Development of space perception in relation to the maturation of the motor system in infant rhesus macaques (Macaca mulatta), Neuropsychologia, 70, 429, 10.1016/j.neuropsychologia.2014.12.002 Shaw, 2008, Neurodevelopmental trajectories of the human cerebral cortex, J. Neurosci., 28, 3586, 10.1523/JNEUROSCI.5309-07.2008 Sheridan, 2010, Early institutionalization: neurobiological consequences and genetic modifiers, Neuropsychol. Rev., 20, 414, 10.1007/s11065-010-9152-8 Sheridan, 2012, Variation in neural development as a result of exposure to institutionalization early in childhood, Proc. Natl. Acad. Sci. U. S. A., 109, 12927, 10.1073/pnas.1200041109 Shirtcliff, 2012, Longitudinal stability and developmental properties of salivary cortisol levels and circadian rhythms from childhood to adolescence, Dev. Psychobiol., 54, 493, 10.1002/dev.20607 Shonkoff, 2012, Early childhood adversity, toxic stress, and the role of the pediatrician: translating developmental science into lifelong health, Pediatrics, 129, e232, 10.1542/peds.2011-2663 Slopen, 2014, Interventions to improve cortisol regulation in children: a systematic review, Pediatrics, 2013-1632 Smith, 2015, DNA extracted from saliva for methylation studies of psychiatric traits: evidence tissue specificity and relatedness to brain, Am. J. Med. Genet. B Neuropsychiatr. Genet., 168, 36, 10.1002/ajmg.b.32278 Sroufe, 1977, Attachment as an organizational construct, Child Dev., 1184, 10.2307/1128475 Stanton, 1988, Maternal deprivation potentiates pituitary-adrenal stress responses in infant rats, Behav. Neurosci., 102, 692, 10.1037/0735-7044.102.5.692 Steiger, 2013, Methylation of the glucocorticoid receptor gene promoter in bulimic women: associations with borderline personality disorder, suicidality, and exposure to childhood abuse, Int. J. Eat. Disord., 46, 246, 10.1002/eat.22113 Suderman, 2014, Childhood abuse is associated with methylation of multiple loci in adult DNA, BMC Med. Genet., 7, 13 Sullivan, 2010 Teicher, 2003, The neurobiological consequences of early stress and childhood maltreatment, Neurosci. Biobehav. Rev., 27, 33, 10.1016/S0149-7634(03)00007-1 Teicher, 2014, Childhood maltreatment: altered network centrality of cingulate, precuneus, temporal pole and insula, Biol. Psychiatry, 76, 297, 10.1016/j.biopsych.2013.09.016 Tottenham, 2009, A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing, Front. Hum. Neurosci., 3, 68 Trickett, 2010, Attenuation of cortisol across development for victims of sexual abuse, Dev. Psychopathol., 22, 165, 10.1017/S0954579409990332 Turecki, 2014 Tyrka, 2012, Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: preliminary findings in healthy adults, PLoS One, 7, e30148, 10.1371/journal.pone.0030148 Ulrich-Lai, 2009, Neural regulation of endocrine and autonomic stress responses, Nat. Rev. Neurosci., 10, 397, 10.1038/nrn2647 van Harmelen, 2010, Reduced medial prefrontal cortex volume in adults reporting childhood emotional maltreatment, Biol. Psychiatry, 68, 832, 10.1016/j.biopsych.2010.06.011 Vasquez, 1998, Stress and the developing limbic-hypothalamic-pituitary-adrenal axis, Psychoneuroendocrinology, 23, 663, 10.1016/S0306-4530(98)00029-8 Veer, 2012, Endogenous cortisol is associated with functional connectivity between the amygdala and medial prefrontal cortex, Psychoneuroendocrinology, 37, 1039, 10.1016/j.psyneuen.2011.12.001 Walker, 1991, The pituitary-adrenocortical system of neonatal rats is responsive to stress througout development in a time-dependent and stressor-specific fashion, Endocrinology, 128, 1385, 10.1210/endo-128-3-1385 Weaver, 2004, Epigenetic programming by maternal behavior, Nat. Neurosci., 7, 847, 10.1038/nn1276 Weder, 2014, Child abuse, depression, and methylation in genes involved with stress, neural plasticity, and brain circuitry, J. Am. Acad. Child Adolesc. Psychiatry, 53, 417, 10.1016/j.jaac.2013.12.025 Widom, 2012, A prospective investigation of physical health outcomes in abused and neglected children: new findings from a 30-year follow-up, Am. J. Public Health, 102, 1135, 10.2105/AJPH.2011.300636 Workman, 2013, Modeling transformations of neurodevelopmental sequences across mammalian species, J. Neurosci., 33, 7368, 10.1523/JNEUROSCI.5746-12.2013 Yang, 2013, Child abuse and epigenetic mechanisms of disease risk, Am. J. Prev. Med., 44, 101, 10.1016/j.amepre.2012.10.012 Yi, 1994, Corticotrophin-releasing hormone mediates the response to cold stress in the neonatal rat without compensatory enhancement of the peptide's gene expression, Endocrinology, 135, 2364, 10.1210/endo.135.6.7988418 Zeanah, 2009, Institutional rearing and psychiatric disorders in Romanian preschool children, Am. J. Psychiatry, 166, 777, 10.1176/appi.ajp.2009.08091438 Zhang, 2013, Profiling of childhood adversity-associated DNA methylation changes in alcoholic patients and healthy controls, PLoS One, 8, e65648, 10.1371/journal.pone.0065648