Chapter 12
Nonhuman Primate Research Contributions to Understanding Genetic and Environmental Influences on Phenotypic Outcomes across Development
Book Editor(s):Kathryn E. Hood, Carolyn Tucker Halpern,
Gary Greenberg, Richard M. Lerner,
Carolyn Tucker Halpern
University of North Carolina at Chapel Hill, USA
Search for more papers by this authorSummary
This chapter contains sections titled:
-
Nonhuman Primates in Developmental Research
-
Environmental Manipulations in Nonhuman Primate Behavioral Genetic Research
-
Nonhuman Primate Model for Early Childhood Adversity
-
Nonhuman Primate Research on Specific Genetic Variation
-
Association Studies in Nonhuman Primates
-
Review of 5HTTLPR Findings in Macaques
-
Allele Frequencies and Comparative Considerations
-
Organization of Review of 5HTTLPR Macaque Studies
-
Major Findings across 5HTTLPR Macaque Studies
-
Other Genes
-
Summary and Conclusions
-
References
References
- Almli, C. R., Rivkin, M. J., & McKinstry, R. C. (2007). The NIH MRI study of normal brain development (Objective-2): Newborns, infants, toddlers, and preschoolers. Neuroimage, 35, 308–325.
- Ames, E. W., Fraser, S., & Burnaby, B. C. (1997). The development of Romanian orphanage children adopted to Canada. British Columbia: Simon Fraser University.
- Anand, K. J., & Scalzo, F. M. (2000). Can adverse neonatal experiences alter brain development and subsequent behavior? Biology of the Neonate, 77, 69–82.
- Bailey, J. N., Breidenthal, S. E., Jorgensen, M. J., McCracken, J. T., & Fairbanks, L. A. (2007). The association of DRD4 and novelty seeking is found in a nonhuman primate model. Psychiatry and Genetics, 17, 23–27.
- Barr, C. S., Dvoskin, R. L., Yuan, Q., Lipsky, R. H., Gupte, M., Hu, X., et al. (2008). CRH haplotype as a factor influencing cerebrospinal fluid levels of corticotropin-releasing hormone, hypothalamic-pituitary-adrenal axis activity, temperament, and alcohol consumption in rhesus macaques. Archives of General Psychiatry, 65, 934–944.
- Barr, C. S., Newman, T. K., Becker, M. L., Champoux, M., Lesch, K. P., Suomi, S. J., et al. (2003). Serotonin transporter gene variation is associated with alcohol sensitivity in rhesus macaques exposed to early-life stress. Alcohol Clinical and Experimental Research, 27, 812–817.
- 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.
- Barr, C. S., Newman, T. K., Lindell, S., Shannon, C., Champoux, M., Lesch, K. P., et al. (2004). Interaction between serotonin transporter gene variation and rearing condition in alcohol preference and consumption in female primates. Archives of General Psychiatry, 61, 1146–1152.
- Barr, C. S., Newman, T. K., Schwandt, M., Shannon, C., Dvoskin, R. L., Lindell, S. G., et al. (2004). Sexual dichotomy of an interaction between early adversity and the serotonin transporter gene promoter variant in rhesus macaques. Proceedings of the National Academy of Sciences of the United States of America, 101, 12358–12363.
- 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 limbichypothalamic-pituitary-adrenal axis response to stress in infant macaques. Biological Psychiatry, 55, 733–738.
- Barr, C. S., Schwandt, M., Lindell, S. G., Chen, S. A., Goldman, D., Suomi, S. J., et al. (2007). Association of a functional polymorphism in the mu-opioid receptor gene with alcohol response and consumption in male rhesus macaques. Archives of General Psychiatry, 64, 369–376.
- Barr, C. S., Schwandt, M. L., Lindell, S. G., Higley, J. D., Maestripieri, D., Goldman, D., et al. (2008). Variation at the mu-opioid receptor gene (OPRM1) influences attachment behavior in infant primates. Proceedings of the National Academy of the Sciences USA, 105, 5277–5281.
- Barr, C. S., Schwandt, M. L., Newman, T. K., & Higley, J. D. (2004). The use of adolescent nonhuman primates to model human alcohol intake: Neurobiological, genetic, and psychological variables. Annals of the New York Academy of Sciences, 1021, 221–233.
- Beauchamp, A. J., & Gluck, J. P. (1988). Associative processes in differentially reared monkeys (Macaca mulatta): Sensory preconditioning. Developmental Psychobiology, 21, 355–364.
- Beauchamp, A. J., Gluck, J. P., Fouty, H. E., & Lewis, M. H. (1991). Associative processes in differentially reared rhesus monkeys (Macaca mulatta): Blocking. Developmental Psychobiology, 24, 175–189.
- Beckett, C., Maughan, B., Rutter, M., Castle, J., Colvert, E., Groothues, C., et al. (2006). Do the effects of early severe deprivation on cognition persist into early adolescence? Findings from the English and Romanian adoptees study. Child Development, 77, 696–711.
- Bennett, A. J. (2008). Gene environment interplay: Nonhuman primate models in the study of resilience and vulnerability. Developmental Psychobiology, 50, 48–59.
- Bennett, A. J., Kaiss, K. M., Laudenslager, M. L., Kaplan, J. R., Robbins, K., Ma, R., et al. (2004). Comparison of allele frequencies in Macaca fascicularis, M. mulatta, M. nemestrina, and M. radiata using an enhanced method for detecting the short and long promoter alleles of the Macaca. American Journal of Primatology, 62(Supplement 1), 100–101.
- Bennett, A. J., Lesch, K. P., Heils, A., Long, J. C., Lorenz, J. G., Shoaf, S. E., et al. (2002). Early experience and serotonin transporter gene variation interact to influence primate CNS function. Molecular Psychiatry, 7, 118–122.
- Bercovitch, F. B., & Goy, R. W. (1990). The socioendocrinology of reproductive development and reproductive success in macaques. In T. E. Ziegler (Ed.), Socioendocrinology of primate reproduction (pp. 59–93). New York: Wiley-Liss.
- Bethea, C. L., Streicher, J. M., Coleman, K., Pau, F. K., Moessner, R., & Cameron, J. L. (2004). Anxious behavior and fenfluramine-induced prolactin secretion in young rhesus macaques with different alleles of the serotonin reuptake transporter polymorphism (5HTTLPR). Behavior Genetics, 34, 295–307.
- Bobb, A. J., Castellanos, F. X., Addington, A. M., & Rapoport, J. L. (2006). Molecular genetic studies of ADHD: 1991 to 2004. American Journal of Medical Genetics (Neuropsychiatric Genetics), 141B, 551–565.
- Bolter, D., & Zihlman, A. (2007). Primate growth and development: A functional and evolutionary approach. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 408–422). New York: Oxford University Press.
- Bremner, J. D., Southwick, S. M., Johnson, D. R., Yehuda, R., & Charney, D. S. (1993). Childhood physical abuse and combat-related posttraumatic stress disorder in Vietnam veterans. American Journal of Psychiatry, 150, 235–239.
- 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.
- Capitanio, J. P. (1984). Early experience and social processes in rhesus macaques (Macaca mulatta): I. Dyadic social interaction. Journal of Comparative Psychology, 98, 35–44.
- Capitanio, J. P. (1985). Early experience and social processes in rhesus macaques (Macaca mulatta): II. Complex social interaction. Journal of Comparative Psychology, 99, 133–144.
- Capitanio, J. P., Abel, K., Mendoza, S. P., Blozis, S. A., McChesney, M. B., Cole, S. W., et al. (2008). Personality and serotonin transporter genotype interact with social context to affect immunity and viral set-point in simian immunodeficiency virus disease. Brain, Behavior, and Immunity, 22, 676–689.
- Capitanio, J. P., & Emborg, M. E. (2008). Contributions of non-human primates to neuroscience research. Lancet, 371, 1126–1135.
- Caspi, A., McClay, J., Moffitt, T. E., Mill, J., Martin, J., Craig, I. W., et al. (2002). Role of genotype in the cycle of violence in maltreated children. Science, 297, 851–854.
- Caspi, A., Sugden, K., Moffitt, T. E., 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.
- Champoux, M., Bennett, A., Shannon, C., Higley, J. D., Lesch, K. P., & Suomi, S. J. (2002). Serotonin transporter gene polymorphism, differential early rearing, and behavior in rhesus monkey neonates. Molecular Psychiatry, 7, 1058–1063.
- Clarke, A. S. (1993). Social rearing effects on HPA axis activity over early development and in response to stress in rhesus monkeys. Developmental Psychobiology, 26, 433–446.
- Clarke, A. S., Ebert, M. H., Schmidt, D. E., McKinney, W. T., & Kraemer, G. W. (1999). Biogenic amine activity in response to fluoxetine and desipramine in differentially reared rhesus monkeys. Biological Psychiatry, 46, 221–228.
- Clarke, A. S., Hedeker, D. R., Ebert, M. H., Schmidt, D. E., McKinney, W. T., & Kraemer, G. W. (1996). Rearing experience and biogenic amine activity in infant rhesus monkeys. Biological Psychiatry, 40, 338–352.
- Clarke, A. S., Kammerer, C. M., George, K. P., Kupfer, D. J., McKinney, W. T., Spence, M. A. et al. (1995). Evidence for heritability of biogenic amine levels in the cerebrospinal fluid of rhesus monkeys. Biological Psychiatry, 38, 572–577.
- Clarke, A. S., Kraemer, G. W., & Kupfer, D. J. (1998). Effects of rearing condition on HPA axis response to fluoxetine and desipramine treatment over repeated social separations in young rhesus monkeys. Psychiatry Research, 79, 91–104.
- Clarke, A. S., & Schneider, M. L. (1993). Prenatal stress has long-term effects on behavioral responses to stress in juvenile rhesus monkeys. Developmental Psychobiology, 26, 293–304.
- Clarke, A. S., & Snipes, M. (1998). Early behavioral development and temperamental traits in mother- vs peer-reared rhesus monkeys. Primates, 39, 433–448.
- Cohen, R. A., Grieve, S., Hoth, K. F., Paul, R. H., Sweet, L., Tate, D., et al. (2006). Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biological Psychiatry, 59, 975–982.
- Costello, E. J., Sung, M., Worthman, C., & Angold, A. (2007). Pubertal maturation and the development of alcohol use and abuse. Drug and Alcohol Dependence, 88(Suppl 1), S50–S59.
- Courchesne, E., Chisum, H. J., Townsend, J., Cowles, A., Covington, J., Egaas, B., et al. (2000). Normal brain development and aging: Quantitative analysis at in vivo MR imaging in healthy volunteers. Radiology, 216, 672–682.
- Dahl, R. E. (2004). Adolescent brain development: A period of vulnerabilities and opportunities. Keynote address. Annals of the New York Academy of Sciences, 1021, 1–22.
- De Bellis, M. D. (2002). Developmental traumatology: A contributory mechanism for alcohol and substance use disorders. Psychoneuroendocrinology, 27, 155–170.
- De Bellis, M. D., Keshavan, M. S., Clark, D. B., Casey, B. J., Giedd, J. N., Boring, A. M., et al. (1999). Developmental traumatology Part II: Brain development. Biological Psychiatry, 45, 1271–1284.
- De Bellis, M. D., Keshavan, M. S., Frustaci, K., Shifflett, H., Iyengar, S., Beers, S. R., et al. (2002). Superior temporal gyrus volumes in maltreated children and adolescents with PTSD. Biological Psychiatry, 51, 544–552.
- De Bellis, M. D., & Kuchibhatla, M. (2006). Cerebellar volumes in pediatric maltreatment-related posttraumatic stress disorder. Biological Psychiatry, 60, 697–703.
- Deckert, J., Catalano, M., Heils, A., Di, B. D., Friess, F., Politi, E., et al. (1997). Functional promoter polymorphism of the human serotonin transporter: Lack of association with panic disorder. Psychiatry and Genetics, 7, 45–47.
- Denenberg, V. H., Brumaghim, J. T., Haltmeyer, G. C., & Zarrow, M. X. (1967). Increased adrenocortical activity in the neonatal rat following handling. Endocrinology, 81, 1047–1052.
- Fahlke, C., Lorenz, J. G., Long, J., Champoux, M., Suomi, S. J., & Higley (2000). Rearing experiences and stress-induced plasma cortisol as early risk factors for excessive alcohol consumption in nonhuman primates. Alcohol Clinical and Experimental Research, 24, 644–650.
- Felitti, V. J., Anda, R. F., Nordenberg, D., Williamson, D. F., Spitz, A. M., Edwards, V., et al. (1998). Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) Study. American Journal of Preventive Medicine, 14, 245–258.
- Flaherty, E. G., Thompson, R., Litrownik, A. J., Theodore, A., English, D. J., Black, M. M., et al. (2006). Effect of early childhood adversity on child health. Archives of Pediatric Adolescent Medicine, 160, 1232–1238.
- Giedd, J. N. (2008). The teen brain: Insights from neuroimaging. Journal of Adolescent Health, 42, 335–343.
- Ginsberg, S. D., Hof, P. R., McKinney, W. T. & Morrison, J. H. (1993). The noradrenergic innervation density of the monkey paraventricular nucleus is not altered by early social deprivation. Neuroscience Letters, 158, 130–134.
- Gluck, J., Harlow, H. F., & Schiltz, K. A. (1973). Differential effect of early enrichment and deprivation on learning in the rhesus monkey (Macaca mulatta). Journal of Comparative and Physiological Psychology, 84, 598–604.
- Gluck, J., & Sackett, G. (1976). Extinction deficits in socially isolated rhesus monkeys (Macaca mulatta). Developmental Psychology, 12, 173–174.
- Gottesman, I. I., & Hanson, D. R., (2005). Human development: Biological and genetic processes. Annual Review of Psychology, 56, 263–286.
- Grant, K. A., & Bennett, A. J. (2003). Advances in nonhuman primate alcohol abuse and alcoholism research. Pharmacology and Therapeutics, 100, 235–255.
- Grant, K. A., Leng, X., Green, H. L., Szeliga, K. T., Rogers, L. S., & Gonzales, S. W., (2008). Drinking typography established by scheduled induction predicts chronic heavy drinking in a monkey model of ethanol self-administration. Alcohol Clinical and Experimental Research, 32, 1824–1838.
-
Greenberg, B. D., Tolliver, T. J., Huang, S. J., Li, Q., Bengel, D., & Murphy, D. L. (1999). Genetic variation in the serotonin transporter promoter region affects serotonin uptake in human blood platelets. American Journal of Medical Genetics, 88, 83–87.
10.1002/(SICI)1096-8628(19990205)88:1<83::AID-AJMG15>3.0.CO;2-0 CAS PubMed Web of Science® Google Scholar
- Griffin, G. A., & Harlow, H. F. (1966). Effects of three months of total social deprivation on social adjustment and learning in the rhesus monkey. Child Development, 37, 533–547.
- Gunnar, M., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145–173.
- Hahn, M. K., & Blakely, R. D. (2007). The functional impact of SLC6 transporter genetic variation. Annual Review of Pharmacology and Toxicology, 47, 401–441.
- Hariri, A. R., Drabant, E. M., Munoz, K. E., Kolachana, B. S., Mattay, V. S., Egan, M. F., et al. (2005). A susceptibility gene for affective disorders and the response of the human amygdala. Archives of General Psychiatry, 62, 146–152.
- Harlow, H. F., & Harlow, M. K. (1965a). Effects of various mother-infant relationships on rhesus monkey behaviors. In B. M. Foss (Ed.), Determinants of infant behaviour (pp. 15–36). London: Methuen.
-
Harlow, H. F., & Harlow, M. K. (1965b). The affectional systems. In A. M. Schrier (Ed.), Behavior of Nonhuman Primates, Volume 2, (pp. 287–334). New York: Academic Press.
10.1016/B978-1-4832-2821-1.50008-2 Google Scholar
- Harlow, H. F., Plubell, P. E., & Baysinger, C. M. (1973). Induction of psychological death in rhesus monkeys. Journal of Autism and Childhood Schizophrenia, 3, 299–307.
- Harlow, H. F., Schiltz, K. A., & Harlow, M. K. (1969). Effects of social isolation on the learning performance of rhesus monkeys (Vol. 1,) New York: Karger.
- Harlow, H. F., & Suomi, S. J. (1974). Induced depression in monkeys. Behavioral Biology, 12, 273–296.
- Harlow, H. F., & Zimmermann, R. R. (1959). Affectional responses in the infant monkey. Science, 130, 421–432.
- Heils, A., Teufel, A., Petri, S., Stober, G., Riederer, P., Bengel, D., et al. (1996). Allelic variation of human serotonin transporter gene expression. Journal of Neurochemistry, 66, 2621–2624.
- Higley, J. D., & Bennett, A. J. (1999). Central nervous system serotonin and personality as variables contributing to excessive alcohol consumption in non-human primates. Alcohol and Alcoholism, 34, 402–18.
- Higley, J. D., Hasert, M. F., Suomi, S. J., & Linnoila, M. (1991). Nonhuman primate model of alcohol abuse: Effects of early experience, personality, and stress on alcohol consumption. Proceedings of the National Academy of Sciences of the United States of America, 88, 7261–7265.
- Higley, J. D., & Linnoila, M. (1997). A nonhuman primate model of excessive alcohol intake. Personality and neurobiological parallels of type I- and type II-like alcoholism. Recent Developments in Alcoholism, 13, 191–219.
-
Higley, J. D., Linnoila, M., & Suomi, S. J. (1994). Ethological contributions. In M. Hersen, R. T. Ammerman, & L. A. Sisson (Eds.) Handbook of aggressive and destructive behavior in psychiatric patients (pp. 17–32) New York: Plenum Press.
10.1007/978-1-4615-2403-8_2 Google Scholar
- Higley, J. D., Mehlman, P., Taub, D., Higley, S. B., Suomi, S. J., Vickers, J. H., et al. (1992). Cerebrospinal fluid monoamine and adrenal correlates of aggression in free-ranging rhesus monkeys. Archives of General Psychiatry, 49, 436–441.
- Higley, J. D., Suomi, S. J., & Linnoila, M. (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, 103, 551–556.
- Higley, J. D., Suomi, S. J., & Linnoila, M. (1996a). 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.
- Higley, J. D., Suomi, S. J., & Linnoila, M. (1996b). A nonhuman primate model of type II excessive alcohol consumption? Part 1. Low cerebrospinal fluid 5-hydroxyindoleacetic acid concentrations and diminished social competence correlate with excessive alcohol consumption. Alcohol Clinical and Experimental Research, 20, 629–642.
- Higley, J. D., Thompson, W. W., Champoux, M., Goldman, D., Hasert, M. F., Kraemer, G. W., et al. (1993). Paternal and maternal genetic and environmental contributions to cerebrospinal fluid monoamine metabolites in rhesus monkeys (Macaca mulatta). Archives of General Psychiatry, 50, 615–623.
- Hofer, M. A. (1970). Physiological responses of infant rats to separation from their mothers. Science, 168, 871–873.
- Hoffman, J. B., Kaplan, J. R., Kinkead, B., Berga, S. L., & Wilson, M. E. (2007). Metabolic and reproductive consequences of the serotonin transporter promoter polymorphism (5-HTTLPR) in adult female rhesus monkeys (Macaca mulatta). Endocrine Journal, 31, 202–211.
- Ichise, M. Vines, D. C., Gura, T., Anderson, G. M., Suomi, S. J., Higley, J. D., et al. (2006). Effects of early life stress on [11C]DASB positron emission tomography imaging of serotonin transporters in adolescent peer- and mother-reared rhesus monkeys. Journal of Neuroscience, 26, 4638–4643.
- Jarrell, H., Hoffman, J. B., Kaplan, J. R., Berga, S., Kinkead, B., & Wilson, M. E. (2008). Polymorphisms in the serotonin reuptake transporter gene modify the consequences of social status on metabolic health in female rhesus monkeys. Physiology and Behavior, 93, 807–819.
- Johnson, D. E. (2000). Medical and developmental sequelae of early childhood institutionalization in eastern European adoptees. In C. A. Nelson (Ed.), The effects of early adversity on neurobehavioral development (pp. 113–162). Mahwah: Erlbaum.
- Kalin, N. H., Shelton, S. E., Fox, A. S., Rogers, J., Oakes, T. R., & Davidson, R. J. (2008). The serotonin transporter genotype is associated with intermediate brain phenotypes that depend on the context of eliciting stressor. Molecular Psychiatry, 13, 1021–1027.
- Kaplan, J. R., Chen, H., & Manuck, S. B. (2009). The relationship between social status and atherosclerosis in male and female monkeys as revealed by meta-analysis. American Joural of Primatology, 71, 1–10.
- Karere, G. M., Kinnally, E. L., Sanchez, J. N., Famula, T. R., Lyons, L. A., & Capitanio, J. P. (2009). What is an “adverse” environment? Interactions of rearing experiences and MAOA genotype in rhesus monkeys. Biological Psychiatry, 65, 770–777.
- Karlamangla, A. S., Singer, B. H., McEwen, B. S., Rowe, J. W., & Seeman, T. E. (2002). Allostatic load as a predictor of functional decline MacArthur studies of successful aging. Journal of Clinical Epidemiology, 55, 696–710.
- Kaufman, I. C., & Rosenblum, L. A. (1969). Effects of separation from mother on the emotional behavior of infant monkeys. Annals of New York Academy of Sciences, 159, 681–695.
- Kendler, K. S., & Prescott, C. A. (2006). Genes, environment, and psychopathology: Understanding the causes of psychiatric and substance use disorders. New York: The Guilford Press.
- Kinnally, E. L., Lyons, L. A., Abel, K., Mendoza, S., & Capitanio, J. P. (2008). Effects of early experience and genotype on serotonin transporter regulation in infant rhesus macaques. Genes, Brain, and Behavior, 7, 481–486.
- Kitayama, N., Brummer, M., Hertz, L., Quinn, S., Kim, Y., & Bremner, J. D. (2007). Morphologic alterations in the corpus callosum in abuse-related posttraumatic stress disorder: A preliminary study. Journal of Nervous and Mental Disease, 195, 1027–1029.
- Kraemer, G. W. (1992). A psychobiological theory of attachment. Behavioral and Brain Sciences, 15, 493–541.
- Kraemer, G. W., & Bachevalier, J. (1998). Cognitive changes associated with persisting behavioral effects of early psychosocial stress in rhesus monkeys: A view from psychobiology. In B. P. Dohrenwend (Ed.), Adversity, stress, and psychopathology (pp. 438–462) New York: Oxford University Press.
- Kraemer, G. W., Ebert, M. H., Schmidt, D. E., & McKinney, W. T. (1989). A longitudinal study of the effects of different rearing environments on cerebrospinal fluid norepinephrine and biogenic amine metabolites in rhesus monkeys. Neuropsychopharmacology, 2, 175–189.
- Kraemer, G. W., Moore, C. F., Newman, T. K., Barr, C. S., & Schneider, M. L. (2008). Moderate level fetal alcohol exposure and serotonin transporter gene promoter polymorphism affect neonatal temperament and limbic-hypothalamic-pituitary-adrenal axis regulation in monkeys. Biological Psychiatry, 63, 317–324.
- Krawczak, M., Trefilov, A., Berard, J., Bercovitch, F., Kessler, M., Sauermann, U., et al. (2005). Male reproductive timing in rhesus macaques is influenced by the 5HTTLPR promoter polymorphism of the serotonin transporter gene. Biology of Reproduction, 72, 1109–1113.
- Lenroot, R. K., & Giedd, J. N. (2006). Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging. Neuroscience and Biobehavioral Reviews, 30, 718–729.
- Lesch, K. P., Bengel, D., Heils, A., Sabol, S. Z., Greenberg, B. D., Petri, S. et al. (1996). Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science, 274, 1527–1531.
- Lesch, K. P., Greenberg, B. D., Higley, J. D., Bennett, A., & Murphy, D. L. (2002). Serotonin transporter, personality, and behavior: Toward a dissection of gene–gene and gene–environment interaction. In J. Benjamin, R. Ebstein, & R. H. Belmaker (Eds.), Molecular genetics and the human personality (pp. 109–135) Washington, DC: American Psychiatric Publishing.
- Lesch, K. P., & Gutknecht, L. (2005). Pharmacogenetics of the serotonin transporter. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 29, 1062–1073.
- Lesch, K. P., Meyer, J., Glatz, K., Flugge, G., Hinney, A., Hebebrand, J. et al. (1997). The 5-HT transporter gene-linked polymorphic region (5-HTTLPR) in evolutionary perspective: Alternative biallelic variation in rhesus monkeys. Journal of Neural Transmission, 104, 1259–1266.
- Lewis, M. H., Gluck, J. P., Petitto, J. M., Hensley, L. L., & Ozer, H. (2000). Early social deprivation in nonhuman primates: Long-term effects on survival and cell-mediated immunity. Biological Psychiatry, 47, 119–126.
- Little, K. Y., McLaughlin, D. P., Zhang, L., Livermore, C. S., Dalack, G. W., McFinton, P. R. et al. (1998). Cocaine, ethanol, and genotype effects on human midbrain serotonin transporter binding sites and mRNA levels. American Journal of Psychiatry, 155, 207–213.
- 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.
-
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.
10.1002/(SICI)1098-2302(199805)32:4<285::AID-DEV3>3.0.CO;2-J CAS PubMed Web of Science® Google Scholar
- Machado, C. J., & Bachevalier, J. (2003). Non-human primate models of childhood psychopathology: The promise and the limitations. Journal of Child Psychology and Psychiatry, 44, 64–87.
- Macri, S., Spinelli, S., Adriani, W., Dee Higley, J., & Laviola, G. (2007). Early adversity and alcohol availability persistently modify serotonin and hypothalamic-pituitary-adrenal-axis metabolism and related behavior: What experimental research on rodents and primates can tell us. Neuroscience & Biobehavioral Reviews, 31, 172–180.
- Malkova, L., Heuer, E., & Saunders, R. C. (2006). Longitudinal magnetic resonance imaging study of rhesus monkey brain development. European Journal of Neuroscience, 24, 3204–3212.
- Manuck, S. B., Flory, J. D., Ferrell, R. E., & Muldoon, M. F. (2004). Socio-economic status covaries with central nervous system serotonergic responsivity as a function of allelic variation in the serotonin transporter gene-linked polymorphic region. Psychoneuroendocrinology, 29, 651–668.
- Marshall, W. A., & Tanner, J. M. (1969). Variations in pattern of pubertal changes in girls. Archives of Disease in Childhood, 44, 291–303.
- Marshall, W. A., & Tanner, J. M. (1970). Variations in the pattern of pubertal changes in boys. Archives of Disease in Childhood, 45, 13–23.
- Martin, L. J., Spicer, D. M., Lewis, M. H., Gluck, J. P., & Cork, L. C. (1991). Social deprivation of infant rhesus monkeys alters the chemoarchitecture of the brain: I. Subcortical regions. Journal of Neuroscience, 11, 3344–3358.
- 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.
- McEwen, B. S. (2003). Early life influences on life-long patterns of behavior and health. Mental Retardation and Developmental Disabilities Research Reviews, 9, 149–154.
- Melchior, M., Moffitt, T. E., Milne, B. J., Poulton, R., & Caspi, A. (2007). Why do children from socioeconomically disadvantaged families suffer from poor health when they reach adulthood? A life-course study. American Journal of Epidemiology, 166, 966–974.
- Miura, H., Qiao, H., & Ohta, T., (2002). Attenuating effects of the isolated rearing condition on increased brain serotonin and dopamine turnover elicited by novelty stress. Brain Research, 926, 10–17.
- Murphy, D. L., Fox, M. A., Timpano, K. R., Moya, P. R., Ren-Patterson, R., Andrews, A. M. et al. (2008). How the serotonin story is being rewritten by new gene-based discoveries principally related to SLC6A4, the serotonin transporter gene, which functions to influence all cellular serotonin systems. Neuropharmacology, 55, 932–960.
- Naylor, L., Dean, B., Pereira, A., Mackinnon, A., Kouzmenko, A., & Copolov, D. (1998). No association between the serotonin transporter-linked promoter region polymorphism and either schizophrenia or density of the serotonin transporter in human hippocampus. Molecular Medicine, 4, 671–674.
-
Nelson, C. A. (2000). The effects of early adversity on neurobehavioral development: The Minnesota Symposia on Child Psychology (Vol. 31,) Mahwah, NJ: Erlbaum.
10.4324/9781410605344 Google Scholar
- Nelson, E. E., & Winslow, J. T. (2009). Non-human primates: Model animals for developmental psychopathology. Neuropsychopharmacology, 34, 90–105.
- Newman, T. K., Syagailo, Y. V., Barr, C. S., Wendland, J. R., Champoux, M., Graessle, M. et al. (2005). Monoamine oxidase A gene promoter variation and rearing experience influences aggressive behavior in rhesus monkeys. Biological Psychiatry, 57, 167–172.
- O'Connor, T. G., Rutter, M., Beckett, C., Keaveney, L., & Kreppner, J. M. (2000). The effects of global severe privation on cognitive competence: Extension and longitudinal follow-up. Child Development, 71, 376–390.
- Paiardini, M., Hoffman, J., Cervasi, B., Ortiz, A. M., Stroud, F., Silvestri, G. et al. (2009). T-cell phenotypic and functional changes associated with social subordination and gene polymorphisms in the serotonin reuptake transporter in female rhesus monkeys. Brain, Behavior, and Immunity, 23, 286–293.
- Paus, T. Collins, D. L., Evans, A. C., Leonard, G., Pike, B., & Zijdenbos, A. (2001). Maturation of white matter in the human brain: A review of magnetic resonance studies. Brain Research Bulletin, 54, 255–266.
- Perry, J. C., Sigal, J. J., Boucher, S., Pare, N., Ouimet, M. C., Normand, J. et al. (2005). Personal strengths and traumatic experiences among institutionalized children given up at birth (Les Enfants de Duplessis – Duplessis' children) II: Adaptation in late adulthood. Journal of Nervous and Mental Disease, 193, 783–789.
- Pierre, P. J., Hopkins, W. D., Taglialatela, J. P., Lees, C. J., & Bennett, A. J. (2008). Age-related neuroanatomical differences from the juvenile period to adulthood in mother-reared macaques (Macaca radiata). Brain Research, 1226, 56–60.
- Plotsky, P. M., & Meaney, M. J. (1993). Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Research Molecular Brain Research, 18, 195–200.
- Reiss, D., & Leve, L. D. (2007). Genetic expression outside the skin: Clues to mechanisms of genotype x environment interaction. Development and Psychopathology, 19, 1005–1027.
-
Renner, M. J., & Rosenzweig, M. R. (1987). Enriched and impoverised environments: Effects on brain and behavior. New York: Springer-Verlag.
10.1007/978-1-4612-4766-1 Google Scholar
- Resko, J. A., Goy, R. W., Robinson, J. A., & Norman, R. L. (1982). The pubescent rhesus monkey: Some characteristics of the menstrual cycle. Biology of Reproduction, 27, 354–361.
- Rogers, J., Martin, L. J., Comuzzie, A. G., Mann, J. J., Manuck, S. B., Leland, M. et al. (2004). Genetics of monoamine metabolites in baboons: Overlapping sets of genes influence levels of 5-hydroxyindolacetic acid, 3-hydroxy-4-methoxyphenylglycol, and homovanillic acid. Biological Psychiatry, 55, 739–744.
- Rogers, J., Shelton, S. E., Shelledy, W., Garcia, R., & Kalin, N. H. (2008). Genetic influences on behavioral inhibition and anxiety in juvenile rhesus macaques. Genes, Brain, and Behavior, 7, 463–469.
- Rosenblum, L. A., & Kaufman, I. C. (1968). Variations in infant development and response to maternal loss in monkeys. American Journal Orthopsychiatry, 38, 418–426.
- Rosenblum, L. A., & Paully, G. S. (1984). The effects of varying environmental demands on maternal and infant behavior. Child Development, 55, 305–314.
- Rutter, M. (1998). Developmental catch-up, and deficit, following adoption after severe global early privation. The English and Romanian adoptees (ERA) study team. Journal of Child Psychology and Psychiatry, 39, 465–476.
- Sabatini, M. J., Ebert, P., Lewis, D. A., Levitt, P., Cameron, J. L., & Mirnics, K. (2007). Amygdala gene expression correlates of social behavior in monkeys experiencing maternal separation. Journal of Neuroscience, 27, 3295–3304.
- Sabol, S. Z., Hu, S., & Hamer, D. (1998). A functional polymorphism in the monoamine oxidase A gene promoter. Human Genetics, 103, 273–279.
- Sackett, G. P. (1965). Effects of rearing conditions upon the behavior of rhesus monkeys (Macaca mulatta). Child Development, 36, 855–868.
- Sackett, G. P. (1972). Exploratory behavior of rhesus monkeys as a function of rearing experiences and sex. Developmental Psychology, 6, 260–270.
- Sackett, G. P. (1984). A nonhuman primate model of risk for deviant development. American Journal of Mental Deficiency, 88, 469–476.
- Sackett, G. P., Gunderson, V., & Baldwin, D. (1982). Studying the ontogeny of primate behavior. In J. L. Fobes & J. E. King (Eds.), Primate behavior (pp. 135–169) New York: Academic Press.
-
G. P. Sackett, G. C. Ruppenthal, & K. Elias (Eds.). (2006). Nursery rearing of nonhuman primates in the 21st century. New York: Springer.
10.1007/978-0-387-25640-5 Google Scholar
- Sackett, G. P., Ruppenthal, G. C., Fahrenbruch, C. E., Holm, R. A., & Greenough, W. T. (1981). Social isolation rearing effects in monkeys vary with genotype. Developmental Psychology, 17, 313–318.
- Sanchez, M. M., Hearn, E. F., Do, D. Rilling, J. K., & Herndon, J. G. (1998). Differential rearing affects corpus callosum size and cognitive function of rhesus monkeys. Brain Research, 812, 38–49.
- 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.
- Seay, B., & Harlow, H. F. (1965). Maternal separation in the rhesus monkey. Journal of Nervous and Mental Disease, 140, 434–441.
- Seckfort, D. L., Paul, R., Grieve, S. M., Vandenberg, B., Bryant, R. A., Williams, L. M. et al. (2008). Early life stress on brain structure and function across the lifespan: A preliminary study. Brain Imaging and Behavior, 2, 49–58.
- Seeman, T. E., Crimmins, E., Huang, M. H., Singer, B., Bucur, A., Gruenewald, T. et al. (2004). Cumulative biological risk and socio-economic differences in mortality: MacArthur studies of successful aging. Socal Science and Medicine, 58, 1985–1997.
- Serretti, A., Calati, R., Mandelli, L., De and Ronchi, D. (2006). Serotonin transporter gene variants and behavior: A comprehensive review. Current Drug Targets, 7, 1659–1669.
- Shanahan, M. J., & Hofer, S. M. (2005). Social context in gene–environment interactions: retrospect and prospect. Journals of Gerontology, 60B(Spec No 1), 65–76.
- Shaw, P., Kabani, N. J., Lerch, J. P., Eckstrand, K., Lenroot, R., Gogtay, N., et al. (2008). Neurodevelopmental trajectories of the human cerebral cortex. Journal of Neuroscience, 28, 3586–3594.
- Siegel, S. J., Ginsberg, S. D., Hof, P. R., Foote, S. L., Young, W. G., Kraemer, G. W., et al. (1993). Effects of social deprivation in prepubescent rhesus monkeys: Immunohistochemical analysis of the neurofilament protein triplet in the hippocampal formation. Brain Research, 619, 299–305.
- Spear, L. P. (2000a). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24, 417–463.
- Spear, L. P. (2000b). Modeling adolescent development and alcohol use in animals. Alcohol Research and Health, 24, 115–123.
- Spinelli, S., Schwandt, M. L., Lindell, S. G., Newman, T. K., Heilig, M., Suomi, S. J., et al. (2007). Association between the recombinant human serotonin transporter linked promoter region polymorphism and behavior in rhesus macaques during a separation paradigm. Developmental Psychopathology, 19, 977–987.
- Suomi, S. J. (1987). Genetic and maternal contributions to individual differences in rhesus monkey biobehavioral development. In N. A. Krasnegor, E. M. Blass, M. A. Hofer, & W. Smotherman, (Eds.), Perinatal development: A psychobiological perspective (pp. 397–419) Orlando: Academic Press.
- Suomi, S. J. (1997). Early determinants of behaviour: evidence from primate studies. British Medical Bulletin, 53, 170–184.
- Suomi, S. J. (2006). Risk, resilience, and gene x environment interactions in rhesus monkeys. Annals of the New York Academy of Sciences, 1094, 52–62.
- Suomi, S. J., DeLizio, R., & Harlow, H. F. (1976). Social rehabilitation of separation-induced depressive disorders in monkeys. American Journal of Psychiatry, 133, 1279–1285.
- Taylor, A., & Kim-Cohen, J. (2007). Meta-analysis of gene–environment interactions in developmental psychopathology. Development and Psychopathology, 19, 1029–1037.
- 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 Behavioral Reviews, 27, 33–44.
- Tigges, J., Gordon, T. P., McClure, H. M., Hall, E. C., & Peters, A. (1988). Survival rate and life span of rhesus monkeys at the Yerkes Regional Primate Research Center. American Journal of Primatology, 15, 263–273.
- Trefilov, A., Berard, J., Krawczak, M., & Schmidtke, J. (2000). Natal dispersal in rhesus macaques is related to serotonin transporter gene promoter variation. Behavior Genetics, 30, 295–301.
- Uher, R., & McGuffin, P. (2008). The moderation by the serotonin transporter gene of environmental adversity in the aetiology of mental illness: Review and methodological analysis. Molecular Psychiatry, 13, 131–146.
- Van Tol, H. H., Wu, C. M., Guan, H. C., Ohara, K., Bunzow, J. R., Civelli, O. et al. (1992). Multiple dopamine D4 receptor variants in the human population. Nature, 358, 149–152.
- Van Wagenen, G., & Catchpole, H. R. (1954). Physical growth of the rhesus monkey (Macaca mulatta). American Journal of Physical Anthropology, 14, 245–273.
- Veenstra-VanderWeele, J., Anderson, G. M., & Cook E. H., Jr. (2000). Pharmacogenetics and the serotonin system: Initial studies and future directions. European Journal of Pharmacology, 410, 165–181.
- Vivian, J. A., Green, H. L., Young, J. E., Majerksy, L. S., Thomas, B. W., Shively, C. A. et al. (2001). Induction and maintenance of ethanol self-administration in cynomolgus monkeys (Macaca fascicularis): long-term characterization of sex and individual differences. Alcohol Clinical and Experimental Research, 25, 1087–1097.
- Volkow, N. D., & Li, T. K. (2005). Drugs and alcohol: Treating and preventing abuse, addiction and their medical consequences. Pharmacology and Therapeutics, 108, 3–17.
- Wendland, J. R., Lesch, K. P., Newman, T. K., Timme, A., Gachot-Neveu, H., Thierry, B., et al. (2006). Differential functional variability of serotonin transporter and monoamine oxidase a genes in macaque species displaying contrasting levels of aggression-related behavior. Behavior Genetics, 36, 163–172.
- Werge, T., Elbaek, Z., Andersen, M. B., Lundbaek, J. A., & Rasmussen, H. B. (2003). Cebus apella, a nonhuman primate highly susceptible to neuroleptic side effects, carries the GLY9 dopamine receptor D3 associated with tardive dyskinesia in humans. The Pharmacogenomics Journal, 3, 97–100.
- Widom, C. S., Ireland, T., & Glynn, P. J. (1995). Alcohol abuse in abused and neglected children followed-up: Are they at increased risk? Journal of Studies on Alcohol, 56, 207–217.
- Wilson, M. E. (1989). Relationship between growth and puberty in the rhesus monkey. In H. A. Delemarre van de Wall, T. M. Plant, G. P. van Rees, & J. Shoemaker (Eds.), Control of the onset of puberty III (pp. 137–149) Amsterdam: Elsevier Science.
- Wilson, M. E., & Kinkead, B. (2008). Gene–environment interactions, not neonatal growth hormone deficiency, time puberty in female rhesus monkeys. Biology of Reproduction, 78, 736–743.
- Winstanley, C. A., Dalley, J. W., Theobald, D. E., & Robbins, T. W. (2004). Fractionating impulsivity: Contrasting effects of central 5-HT depletion on different measures of impulsive behavior. Neuropsychopharmacology, 29, 1331–1343.
- Witt, E. D. (1994). Mechanisms of alcohol abuse and alcoholism in adolescents: A case for developing animal models. Behavioral and Neural Biology, 62, 168–177.
- Witt, E. D. (2007). Puberty, hormones, and sex differences in alcohol abuse and dependence. Neurotoxicology and Teratology, 29, 81–95.