The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.
Risk and Resilience: Early Manipulation of Macaque Social Experience and Persistent Behavioral and Neurophysiological Outcomes
Abstract
Objective To review the contributions of research on nonhuman primates, specifically macaque monkeys, to the understanding of early social stress and its effects on behavior and neurophysiology. Method Review and synthesis of two bodies of work on macaque monkeys and early social manipulation: peer rearing and variable foraging demands. The literature was searched with Medline using key terms macaque, variable foraging, and peer rearing. The reference lists of these articles were also used to generate potential studies for review. Results Nonhuman primate macaques show similarities to humans in their social development and functioning. Peer rearing of young macaques and rearing of young macaques with mothers experiencing variable foraging conditions both result in increased anxious, impulsive, and aggressive temperament and behavior; more reactive stress physiology; altered neurotransmitter functioning; and immune and metabolic changes. Functional variants of specific genes that code for neuromodulators are mediators of these effects. Conclusions Disrupted social relations during macaque rearing contribute to the risk for developing emotional and neurophysiological disturbance. In the face of such disruption, certain genotypes contribute to resilience. This can be alternately stated that, for animals of high-risk genotypes, resilience is conferred by quality relationships during rearing. This interaction of genetics with early social environment also applies to child mental h…
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“This is consistent with other primate studies that have found little to no relationship between sociopositive infant care behaviors (e.g., carrying, grooming, anogenital licking, etc.) and later HPA stress response styles (macaque monkeys: review in Parker and Maestripieri, 2011; Stevens et al., 2009; marmoset: Johnson et al., 1996a; Goeldi’s monkey: Dettling et al., 1998).”
From Quality of maternal and paternal care predicts later stress reactivity in the cooperatively-breeding marmoset (Callithrix geoffroyi) (2013) · cites this paper as Stevens et al., 2009
Citations
Cites
Harlow, H. F. (1958) · American Psychologist · doi:10.1037/h0047884 · Cited by 2,022
Behavioral Inhibition: Linking Biology and Behavior within a Developmental Framework
Fox, N. A., Henderson, H. A., Marshall, P. J., Nichols, K. E., & Ghera, M. M. (2005) · Annual Review of Psychology · doi:10.1146/annurev.psych.55.090902.141532 · Cited by 1,040
Strategy for Investigating Interactions Between Measured Genes and Measured Environments
Moffitt, T. E., Caspi, A., & Rutter, M. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.5.473 · Cited by 784
Importance of Early Neglect for Childhood Aggression
Kotch, J. B., Lewis, T., Hussey, J. M., English, D., Thompson, R., Litrownik, A. J., Runyan, D. K., Bangdiwala, S. I., Margolis, B., & Dubowitz, H. (2008) · Pediatrics · doi:10.1542/peds.2006-3622 · Cited by 183
Flagged first, then by citations
Research works printed but not linked: 75
- Rutter, 1998, Some research considerations on intergenerational continuities and discontinuities: comment on the special section, Dev Psychol, 34, 1269, 10.1037/0012-1649.34.6.1269 · DOI
- Ruppenthal, 1976, A 10-year perspective of motherless-mother monkey behavior, J Abnorm Psychol, 85, 341, 10.1037/0021-843X.85.4.341 · DOI
- Newport, 2002, Parental depression: animal models of an adverse life event, Am J Psychiatry, 159, 1265, 10.1176/appi.ajp.159.8.1265 · DOI
- Suomi, 2005, Aggression and social behaviour in rhesus monkeys, Novartis Found Symp, 268, 216, 10.1002/0470010703.ch15 · DOI
- Adler, 2007, Health disparities: what's optimism got to do with it?, J Adolesc Health, 40, 106, 10.1016/j.jadohealth.2006.12.003 · DOI
- Suomi, 1997, Early determinants of behaviour: evidence from primate studies, Br Med Bull, 53, 170, 10.1093/oxfordjournals.bmb.a011598 · DOI
- Seifer, 1994, Infant temperament measured by multiple observations and mother report, Child Dev, 65, 1478, 10.2307/1131512 · DOI
- Suomi, 2003, Gene-environment interactions and the neurobiology of social conflict, Ann N Y Acad Sci, 1008, 132, 10.1196/annals.1301.014 · DOI
- Clarke, 1998, Effects of rearing condition on HPA axis response to fluoxetine and desipramine treatment over repeated social separations in young rhesus monkeys, Psychiatry Res, 79, 91, 10.1016/S0165-1781(98)00032-8 · DOI
- Hirshfeld, 1992, Stable behavioral inhibition and its association with anxiety disorder, J Am Acad Child Adolesc Psychiatry, 31, 103, 10.1097/00004583-199201000-00016 · DOI · Paper page
- Higley, 1996, Stability of interindividual differences in serotonin function and its relationship to severe aggression and competent social behavior in rhesus macaque females, Neuropsychopharmacology, 14, 67, 10.1016/S0893-133X(96)80060-1 · DOI
- Saudino, 2005, Behavioral genetics and child temperament, J Dev Behav Pediatr, 26, 214, 10.1097/00004703-200506000-00010 · DOI
- Rasmussen, 1997, Comparison of physiological measures of Cayo Santiago rhesus monkey females with and between social groups, Primate Rep, 47, 49
- Higley, 1996, CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors, Biol Psychiatry, 40, 1067, 10.1016/S0006-3223(95)00675-3 · DOI
- Placidi, 2001, Aggressivity, suicide attempts, and depression: relationship to cerebro-spinal fluid monoamine metabolite levels, Biol Psychiatry, 50, 783, 10.1016/S0006-3223(01)01170-2 · DOI
- Champoux, 1994, Temperament differences between captive Indian and Chinese-Indian hybrid rhesus macaque neonates, Lab Anim Sci, 44, 351
- Caspi, 1995, Temperamental origins of child and adolescent behavior problems: from age three to age fifteen, Child Dev, 66, 55, 10.2307/1131190 · DOI
- Harlow, 1965, Total social isolation in monkeys, Proc Natl Acad Sci U S A, 54, 90, 10.1073/pnas.54.1.90 · DOI · Paper page
- Clarke, 1996, Rearing experience and biogenic amine activity in infant rhesus monkeys, Biol Psychiatry, 40, 338, 10.1016/0006-3223(95)00663-X · DOI
- Suomi, 1991, Early stress and adult emotional reactivity in rhesus monkeys, Ciba Found Symp, 156, 171
- Meyer, 1975, Behavioral and hormonal effects of attachment object separation in surrogate-peer-reared and mother-reared infant rhesus monkeys, Dev Psychobiol, 8, 425, 10.1002/dev.420080507 · DOI
- Suomi, 2006, Risk, resilience, and gene x environment interactions in rhesus monkeys, Ann N Y Acad Sci, 1094, 52, 10.1196/annals.1376.006 · DOI
- Kraemer, 1979, Interactions of pharmacological agents which alter biogenic amine metabolism and depression—an analysis of contributing factors within a primate model of depression, J Affect Disord, 1, 33, 10.1016/0165-0327(79)90023-5 · DOI
- Kraemer, 1991, Strangers in a strange land: a psychobiological study of infant monkeys before and after separation from real or inanimate mothers, Child Dev, 62, 548, 10.2307/1131130 · DOI
- Higley, 1991, CSF monoamine metabolite concentrations vary according to age, rearing, and sex, and are influenced by the stressor of social separation in rhesus monkeys, Psychopharmacology (Berl), 103, 551, 10.1007/BF02244258 · DOI
- Shannon, 1998, Rearing condition and plasma cortisol in rhesus monkey infants, Am J Primatol, 46, 311, 10.1002/(SICI)1098-2345(1998)46:4<311::AID-AJP3>3.0.CO;2-L · DOI
- Fahlke, 2000, Rearing experiences and stress-induced plasma cortisol as early risk factors for excessive alcohol consumption in nonhuman primates, Alcohol Clin Exp Res, 24, 644, 10.1111/j.1530-0277.2000.tb02035.x · DOI
- Higley, 1992, Cerebrospinal fluid monoamine and adrenal correlates of aggression in free-ranging rhesus monkeys, Arch Gen Psychiatry, 49, 436, 10.1001/archpsyc.1992.01820060016002 · DOI
- Clarke, 1999, Biogenic amine activity in response to fluoxetine and desipramine in differentially reared rhesus monkeys, Biol Psychiatry, 46, 221, 10.1016/S0006-3223(99)00027-X · DOI
- Ginsberg, 1993, The noradrenergic innervation density of the monkey paraventricular nucleus is not altered by early social deprivation, Neurosci Lett, 158, 130, 10.1016/0304-3940(93)90246-H · DOI
- Laudenslager, 2000, Antidepressant treatment during social challenge prior to 1 year of age affects immune and endocrine responses in adult macaques, Psychiatry Res, 95, 25, 10.1016/S0165-1781(00)00165-7 · DOI
- Laudenslager, 1996, Natural cytotoxicity toward K562 cells by macaque lymphocytes from infancy through puberty: effects of early social challenge, Brain Behav Immun, 10, 275, 10.1006/brbi.1996.0024 · DOI
- Lubach, 1995, Effects of early rearing environment on immune responses of infant rhesus monkeys, Brain Behav Immun, 9, 31, 10.1006/brbi.1995.1004 · DOI
- Lewis, 2000, Early social deprivation in nonhuman primates: long-term effects on survival and cell-mediated immunity, Biol Psychiatry, 47, 119, 10.1016/S0006-3223(99)00238-3 · DOI
- Coe, 1989, Influence of early rearing on lymphocyte proliferation responses in juvenile rhesus monkeys, Brain Behav Immun, 3, 47, 10.1016/0889-1591(89)90005-6 · DOI
- Coe, 1992, Early rearing conditions alter immune responses in the developing infant primate, Pediatrics, 90, 505, 10.1542/peds.90.3.505 · DOI
- Shannon, 2005, Maternal absence and stability of individual differences in CSF 5-HIAA concentrations in rhesus monkey infants, Am J Psychiatry, 162, 1658, 10.1176/appi.ajp.162.9.1658 · DOI
- Sanchez, 1998, Differential rearing affects corpus callosum size and cognitive function of rhesus monkeys, Brain Res, 812, 38, 10.1016/S0006-8993(98)00857-9 · DOI
- Huot, 2002, Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats, Brain Res, 950, 52, 10.1016/S0006-8993(02)02985-2 · DOI
- Rosenblum, 1984, The effects of varying environmental demands on maternal and infant behavior, Child Dev, 55, 305, 10.2307/1129854 · DOI
- Andrews, 1991, Attachment in monkey infants raised in variable- and low-demand environments, Child Dev, 62, 686, 10.2307/1131170 · DOI
- Andrews, 1993, Assessment of attachment in differentially reared infant monkeys (Macaca radiata): response to separation and a novel environment, J Comp Psychol, 107, 84, 10.1037/0735-7036.107.1.84 · DOI
- Andrews, 1994, The development of affiliative and agonistic social patterns in differentially reared monkeys, Child Dev, 65, 1398, 10.2307/1131506 · DOI
- Rosenblum, 2001, Response of adolescent bonnet macaques to an acute fear stimulus as a function of early rearing conditions, Dev Psychobiol, 39, 40, 10.1002/dev.1026 · DOI
- 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 · DOI · Paper page
- Coplan, 2005, Synchronized maternal-infant elevations of primate CSF CRF concentrations in response to variable foraging demand, CNS Spectr, 10, 530, 10.1017/S109285290001018X · DOI
- Rosenblum, 1994, Adverse early experiences affect noradrenergic and serotonergic functioning in adult primates, Biol Psychiatry, 35, 221, 10.1016/0006-3223(94)91252-1 · DOI
- Coplan, 2000, Growth hormone response to clonidine in adversely reared young adult primates: relationship to serial cerebrospinal fluid corticotropin-releasing factor concentrations, Psychiatry Res, 95, 93, 10.1016/S0165-1781(00)00173-6 · DOI
- 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 · DOI
- Smith, 2002, Transforming growth factor-beta 1 and cortisol in differentially reared primates, Brain Behav Immun, 16, 140, 10.1006/brbi.2001.0629 · DOI
- Kaufman, 2007, Early-life stress and the development of obesity and insulin resistance in juvenile bonnet macaques, Diabetes, 56, 1382, 10.2337/db06-1409 · DOI · Paper page
- 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 · DOI
- Czeh, 2001, Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine, Proc Natl Acad Sci U S A, 98, 12796, 10.1073/pnas.211427898 · DOI
- Coplan, 2006, Maternal-infant response to variable foraging demand in nonhuman primates: effects of timing of stressor on cerebrospinal fluid corticotropin-releasing factor and circulating glucocorticoid concentrations, Ann N Y Acad Sci, 1071, 525, 10.1196/annals.1364.057 · DOI
- Kaufman, 2006, Brain-derived neurotrophic factor-5-HTTLPR gene interactions and environmental modifiers of depression in children, Biol Psychiatry, 59, 673, 10.1016/j.biopsych.2005.10.026 · DOI · Paper page
- Jaffee, 2007, Gene-environment correlations: a review of the evidence and implications for prevention of mental illness, Mol Psychiatry, 12, 432, 10.1038/sj.mp.4001950 · DOI
- Higley, 2000, Early rearing and genotypic influences on CNS serotonin and behavior in nonhuman primates, Biol Psychiatry, 47, S10, 10.1016/S0006-3223(00)00468-6 · DOI
- Bennett, 2002, Early experience and serotonin transporter gene variation interact to influence primate CNS function, Mol Psychiatry, 7, 118, 10.1038/sj.mp.4000949 · DOI
- Champoux, 2002, Serotonin transporter gene polymorphism, differential early rearing, and behavior in rhesus monkey neonates, Mol Psychiatry, 7, 1058, 10.1038/sj.mp.4001157 · DOI
- Barr, 2003, The utility of the non-human primate; model for studying gene by environment interactions in behavioral research, Genes Brain Behav, 2, 336, 10.1046/j.1601-1848.2003.00051.x · DOI
- Barr, 2004, Sexual dichotomy of an interaction between early adversity and the serotonin transporter gene promoter variant in rhesus macaques, Proc Natl Acad Sci U S A, 101, 12358, 10.1073/pnas.0403763101 · DOI
- Barr, 2004, Rearing condition and rh5-HTTLPR interact to influence limbic-hypothalamic-pituitary-adrenal axis response to stress in infant macaques, Biol Psychiatry, 55, 733, 10.1016/j.biopsych.2003.12.008 · DOI · Paper page
- Barr, 2003, Serotonin transporter gene variation is associated with alcohol sensitivity in rhesus macaques exposed to early-life stress, Alcohol Clin Exp Res, 27, 812, 10.1097/01.ALC.0000067976.62827.ED · DOI
- Barr, 2004, Interaction between serotonin transporter gene variation and rearing condition in alcohol preference and consumption in female primates, Arch Gen Psychiatry, 61, 1146, 10.1001/archpsyc.61.11.1146 · DOI
- Newman, 2005, Monoamine oxidase A gene promoter variation and rearing experience influences aggressive behavior in rhesus monkeys, Biol Psychiatry, 57, 167, 10.1016/j.biopsych.2004.10.012 · DOI
- Nilsson, 2006, Role of monoamine oxidase A genotype and psychosocial factors in male adolescent criminal activity, Biol Psychiatry, 59, 121, 10.1016/j.biopsych.2005.06.024 · DOI
- 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 · DOI
- Suomi, 2004, How gene-environment interactions shape biobehavioral development: lessons from studies with rhesus monkeys, Res Hum Dev, 1, 205, 10.1207/s15427617rhd0103_5 · DOI
- Berman, 2004, Dominance style among Macaca thibetana on Mt. Huangshan, China, Int J Primatol, 25, 1283, 10.1023/B:IJOP.0000043963.77801.c3 · DOI
- Wendland, 2006, Differential functional variability of serotonin transporter and monoamine oxidase a genes in macaque species displaying contrasting levels of aggression-related behavior, Behav Genet, 36, 163, 10.1007/s10519-005-9017-8 · DOI
- Rutter, 2004, Are there biological programming effects for psychological development? Findings from a study of Romanian adoptees, Dev Psychol, 40, 81, 10.1037/0012-1649.40.1.81 · DOI
- Chugani, 2001, Local brain functional activity following early deprivation: a study of post-institutionalized Romanian orphans, Neuroimage, 14, 1290, 10.1006/nimg.2001.0917 · DOI
- 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 · DOI
- Harlow, 1971, Social recovery by isolation-reared monkeys, Proc Natl Acad Sci U S A, 68, 1534, 10.1073/pnas.68.7.1534 · DOI · Paper page
- Gershoff, 2007, Income is not enough: incorporating material hardship into models of income associations with parenting and child development, Child Dev, 78, 70, 10.1111/j.1467-8624.2007.00986.x · DOI · Paper page
Cited by
Sorted by citations
Early-life stress has persistent effects on amygdala function and development in mice and humans
Malter Cohen, M., Jing, D., Yang, R. R., Tottenham, N., Lee, F. S., & Casey, B. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1310163110 · Cited by 307
Telomere length and early severe social deprivation: linking early adversity and cellular aging
Drury, S. S., Theall, K., Gleason, M. M., Smyke, A. T., De Vivo, I., Wong, J. Y. Y., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2012) · Molecular Psychiatry · doi:10.1038/mp.2011.53 · Cited by 316
Feldman, R. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000048 · Cited by 271
DNA methylation and childhood maltreatment: From animal models to human studies
Lutz, P.-E., & Turecki, G. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.07.069 · Cited by 236
Transcriptional modulation of the developing immune system by early life social adversity
Cole, S. W., Conti, G., Arevalo, J. M. G., Ruggiero, A. M., Heckman, J. J., & Suomi, S. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218253109 · Cited by 207
Self-citation
Metadata
- Authors
- Stevens, H. E., Leckman, J. F., Coplan, J. D., & Suomi, S. J.
- Venue
- Journal of the American Academy of Child & Adolescent Psychiatry
- Publisher
- Elsevier BV
- Published
- 2009-02
- Volume
- 48
- Issue
- 2
- Pages
- 114-127
- ISSN
- 0890-8567
- Cited by
- 91
- References
- 4
- Language
- en
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review