Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-848d4c4894-p2v8j Total loading time: 0.001 Render date: 2024-06-01T15:13:12.623Z Has data issue: false hasContentIssue false

10 - Primate models in serotonin transporter research

Published online by Cambridge University Press:  06 July 2010

By
Khalisa N. Herman ,
James T. Winslow  and
Stephen J. Suomi
Edited by
Allan V. Kalueff  and
Justin L. LaPorte
Allan V. Kalueff
Affiliation:
Georgetown University Medical Center
Justin L. LaPorte
Affiliation:
National Institute of Mental Health
Get access

Summary

ABSTRACT

Numerous studies provide persuasive evidence that a polymorphism in the serotonin promoter, 5-HTTLPR, interacts with environmental risk factors to produce heightened rates of depression, anxiety, antisocial and borderline personality disorders, and substance abuse in adults and adolescents. Investigations with the rhesus monkey have demonstrated similar gene–environment (G×E) interactions on both behavioral and biological outcomes. In this chapter, we review the history of primate models in serotonin transporter (5-HTT) research. Work with non-human primates has noted associations between behavioral differences and variation in serotonin metabolism (5-hydroxy-indole acetic acid, 5-HIAA). Investigations in several non-human primate species have also indicated that manipulation of early experience results in changes in behavior along with alterations in serotonergic functioning. These lines of research have contributed to the discovery of short (s) and long (l) forms within the serotonin promoter (rh5-HTTLPR) in the rhesus monkey. Researchers have since documented associations between the l/s or s/s genotypes and reduced cognitive flexibility, greater impulsivity, and anxious-like behavior, as well as higher rates of alcohol consumption. Furthermore, multiple G×E interactions have been documented for levels of 5-HIAA, hypothalamic–pituitary–adrenocortical (HPA) axis activity, alcohol consumption, rates of behavioral pathology, social play, aggression, and infant temperament. In most cases, these interactions were due to worse outcomes in l/s subjects that had been subjected to early maternal deprivation. This program of research demonstrates that l/s monkeys are more vulnerable to the effects of early-life stress, whereas l/l monkeys are more resilient.

Type
Chapter
Information
Experimental Models in Serotonin Transporter Research , pp. 288 - 307
Publisher: Cambridge University Press
Print publication year: 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, G M (2004). Peripheral and central neurochemical effects of the selective serotonin reuptake inhibitors (SSRIs) in humans and nonhuman primates: assessing bioeffect and mechanisms of action. Int J Dev Neurosci 22: 397–404.CrossRefGoogle ScholarPubMed
Barr, C S, Newman, T K, Becker, M L, et al. (2003a). Serotonin transporter gene variation is associated with alcohol sensitivity in rhesus macaques exposed to early-life stress. Alcohol Clin Exp Res 27: 812–7.CrossRefGoogle ScholarPubMed
Barr, C S, Newman, T K, Becker, M L, et al. (2003b). The utility of the non-human primate model for studying gene by environment interactions in behavioral research. Genes Brain Behav 2: 336–40.CrossRefGoogle ScholarPubMed
Barr, C S, Newman, T K, Lindell, S, et al. (2004a). Interaction between serotonin transporter gene variation and rearing condition in alcohol preference and consumption in female primates. Arch Gen Psychiatry 61: 1146–52.CrossRefGoogle ScholarPubMed
Barr, C S, Newman, T K, Schwandt, M, et al. (2004b). Sexual dichotomy of an interaction between early adversity and the serotonin transporter gene promoter variant in rhesus macaques. Proc Natl Acad Sci USA 101: 12 358–63.CrossRefGoogle ScholarPubMed
Beitchman, J H, Davidge, K M, Kennedy, J L, et al. (2003). The serotonin transporter gene in aggressive children with and without ADHD and nonaggressive matched controls. Ann NY Acad Sci 1008: 248–51.CrossRefGoogle ScholarPubMed
Belsky, J (2005). Differential susceptibility to rearing influence: an evolutionary hypothesis and some evidence. In Ellis, B, Bjorklund, D, editors. Origins of the social mind: evolutionary psychology and child development. New York: Guilford Press, pp. 139–63.Google Scholar
Bennett, A J, Lesch, K P, Heils, A, Linnoila, M V (1998a). Serotonin transporter gene variation, CSF 5-HIAA concentrations, and alcohol-related aggression in rhesus monkeys (Macaca mulatta). Am J Primatol 45: 168–9.Google Scholar
Bennett, A J, Lesch, K P, Heils, A, et al. (2002). Early experience and serotonin transporter gene variation interact to influence primate CNS function. Mol Psychiatry 7: 118–22.CrossRefGoogle ScholarPubMed
Bennett, A J, Tsai, T, Pierre, P J, Suomi, S J, Shoaf, S E, Linnoila, M V (1998b). Behavioral response to novel objects varies with CSF monoamine concentrations in rhesus monkeys. Soc Neurosci Abstr 24: 954.Google Scholar
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). Behav Genet 34: 295–307.CrossRefGoogle Scholar
Brazelton, T B, Nugent, J K (1995). Neonatal behavioral assessment scale. Cambridge: Cambridge University Press.Google Scholar
Brocke, B, Armbruster, D, Muller, J, et al. (2006). Serotonin transporter gene variation impacts innate fear processing: acoustic startle response and emotional startle. Mol Psychiatry 11: 1106–12.CrossRefGoogle ScholarPubMed
Caspi, A, Sugden, K, Moffitt, T E, et al. (2003). Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301: 386–9.CrossRefGoogle ScholarPubMed
Chamove, A S, Rosenblum, L A, Harlow, H F (1973). Monkeys (Macaca mulatta) raised only with peers: a pilot study. Anim Behav 21: 316–25.CrossRefGoogle ScholarPubMed
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. Mol Psychiatry 2002: 1058–63.CrossRefGoogle Scholar
Clarke, H F, Dalley, J W, Crofts, H S, Robbins, T W, Roberts, A C (2004). Cognitive inflexibility after prefrontal serotonin depletion. Science 304: 878–80.CrossRefGoogle ScholarPubMed
Coplan, J D, Trost, R C, Owens, M J, et al. (1998). Cerebrospinal fluid concentrations of somatostatin and biogenic amines in grown primates reared by mothers exposed to manipulated foraging conditions. Arch Gen Psychiatry 55: 473–7.CrossRefGoogle ScholarPubMed
Ebrahim, S H, Diekman, S T, Floyd, R L, Decoufle, P (1999). Comparison of binge drinking among pregnant and nonpregnant women, United States, 1991–1995. Am J Obstet Gynecol 180: 1–7.CrossRefGoogle ScholarPubMed
Ebstein, R P (2006). The molecular genetic architecture of human personality: beyond self-report questionnaires. Mol Psychiatry 11: 427–45.CrossRefGoogle ScholarPubMed
Eley, T C, Sugden, K, Corsico, A, et al. (2004). Gene–environment interaction analysis of serotonin system markers with adolescent depression. Mol Psychiatry 9: 908–15.CrossRefGoogle ScholarPubMed
Fairbanks, L A, Melega, W P, Jorgensen, M J, Kaplan, J R, McGuire, M T (2001). Social impulsivity inversely associated with CSF 5-HIAA and fluoxetine exposure in vervet monkeys. Neuropsychopharmacology 24: 370–8.CrossRefGoogle ScholarPubMed
Ferrari, P F, Palanza, P, Parmigiani, S, Almeida, R M, Miczek, K A (2005). Serotonin and aggressive behavior in rodents and nonhuman primates: predispositions and plasticity. Eur J Pharmacol 526: 259–73.CrossRefGoogle ScholarPubMed
Forrest, J D (1994). The role of hormonal contraceptives: epidemiology of unintended pregnancy and contraceptive use. Am J Obstet Gynecol 170: 1485–9.Google Scholar
Fox, N A, Nichols, K E, Henderson, H A, et al. (2005). Evidence for a gene–environment interaction in predicting behavioral inhibition in middle childhood. Psychol Sci 16: 921–6.CrossRefGoogle ScholarPubMed
Fuster, J M (2002). Frontal lobe and cognitive development. J Neurocytol 31: 373–85.CrossRefGoogle ScholarPubMed
Gillespie, N A, Whitfield, J B, Williams, B, Heath, A C, Martin, N G (2005). The relationship between stressful life events, the serotonin transporter (5-HTTLPR) genotype and major depression. Psychol Med 35: 101–11.CrossRefGoogle ScholarPubMed
Gingrich, J A, Hen, R (2001). Dissecting the role of the serotonin system in neuropsychiatric disorders using knockout mice. Psychopharmacology (Berl.) 155: 1–10.CrossRefGoogle ScholarPubMed
Gottesman, I I, Shields, J (1973). Genetic theorizing and schizophrenia. Br J Psychiatry 122: 15–30.CrossRefGoogle Scholar
Grabe, H J, Lange, M, Wolff, B, et al. (2005). Mental and physical distress is modulated by a polymorphism in the 5-HT transporter gene interacting with social stressors and chronic disease burden. Mol Psychiatry 10: 220–4.CrossRefGoogle ScholarPubMed
Grillon, C, Warner, V, Hille, J, et al. (2005). Families at high and low risk for depression: a three-generation startle study. Biol Psychiatry 57: 953–60.CrossRefGoogle ScholarPubMed
Haberstick, B C, Smolen, A, Hewitt, J K (2006). Family-based association test of the 5HTTLPR and aggressive behavior in a general population sample of children. Biol Psychiatry 59: 836–43.CrossRefGoogle Scholar
Hariri, A R, Drabant, E M, Munoz, K E, et al. (2005). A susceptibility gene for affective disorders and the response of the human amygdala. Arch Gen Psychiatry 62: 146–52.CrossRefGoogle ScholarPubMed
Hariri, A R, Mattay, V S, Tessitore, A, et al. (2002). Serotonin transporter genetic variation and the response of the human amygdala. Science 297: 400–3.CrossRefGoogle ScholarPubMed
Heils, A, Teufel, A, Petri, S, et al. (1996). Allelic variation of human serotonin transporter gene expression. J Neurochem 66: 2621–4.CrossRefGoogle ScholarPubMed
Heim, C, Newport, D J, Bonsall, R, Miller, A H, Nemeroff, C B (2001). Altered pituitary–adrenal axis responses to provocative challenge tests in adult survivors of childhood abuse. Am J Psychiatry 158: 575–81.CrossRefGoogle ScholarPubMed
Heinz, A, Braus, D F, Smolka, M N, et al. (2005). Amygdala–prefrontal coupling depends on a genetic variation in the serotonin transporter. Nat Neurosci 8: 20–1.CrossRefGoogle ScholarPubMed
Heinz, A, Higley, J D, Gorey, J G, et al. (1998). In vivo association between alcohol intoxication, aggression, and serotonin transporter availability in nonhuman primates. Am J Psychiatry 155: 1023–8.CrossRefGoogle ScholarPubMed
Heinz, A, Smolka, M N, Braus, D F, et al. (2007). Serotonin transporter genotype (5-HTTLPR): effects of neutral and undefined conditions on amygdala activation. Biol Psychiatry 61: 1011–4.CrossRefGoogle ScholarPubMed
Higley, J D, Linnoila, M, Stoff, D M, Mann, J J (1997). Low central nervous system serotonergic activity is traitlike and correlates with impulsive behavior: a nonhuman primate model investigating genetic and environmental influences on neurotransmission. In Stoff, D M, Mann, J J, editors. Neurobiology of suicide: from the bench to the clinic. Ann NY Acad Sci836: 39–56.Google Scholar
Higley, J D, Mehlman, P T, Higley, S B, et al. (1996a). Excessive mortality in young free-ranging male nonhuman primates with low cerebrospinal fluid 5-hydroxyindoleacetic acid concentrations. Arch Gen Psychiatry 53: 537–43.CrossRefGoogle ScholarPubMed
Higley, J D, Mehlman, P T, Poland, R E, et al. (1996b). CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors. Biol Psychiatry 40: 1067–82.CrossRefGoogle ScholarPubMed
Higley, J D, Suomi, S J, Linnoila, M (1996c). 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. Alcohol Clin Exp Res 20: 643–50.CrossRefGoogle ScholarPubMed
Higley, J D, Suomi, S J, Linnoila, M (1996d). 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 Clin Exp Res 20: 629–42.CrossRefGoogle ScholarPubMed
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 (Berl.) 103: 551–6.CrossRefGoogle ScholarPubMed
Hofer, M A (1994). Early relationships as regulators of infant physiology and behavior. Acta Paediatr (Suppl) 397: 9–18.CrossRefGoogle ScholarPubMed
Howell, S, Westergaard, G, Hoos, B, et al. (2007). Serotonergic influences on life-history outcomes in free-ranging male rhesus macaques. Am J Primatol 69: 851–65.CrossRefGoogle ScholarPubMed
Iarocci, G, Yager, J, Elfers, T (2007). What gene–environment interactions can tell us about social competence in typical and atypical populations. Brain Cogn 65: 112–27.CrossRefGoogle ScholarPubMed
Ichise, M, Vines, D C, Gura, T, 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. J Neurosci 26: 4638–43.CrossRefGoogle ScholarPubMed
Izquierdo, A, Newman, T K, Higley, J D, Murray, E A (2007). Genetic modulation of cognitive flexibility and socioemotional behavior in rhesus monkeys. Proc Natl Acad Sci USA 104: 14 128–33.CrossRefGoogle ScholarPubMed
Kaplan, J R, Martin, L J, Comuzzie, A G, Manuck, S B, Mann, J J, Rogers, J (2000). Heritability of monoaminergic metabolites measured in the cerebrospinal fluid of baboons. Social Neurosci Abstr 26: 1439.Google Scholar
Kaufman, J, Yang, B-z, Douglas-Palumberi, H, et al. (2004). Social supports and serotonin transporter gene moderate depression in maltreated children. Proc Nat Acad Sci 101: 17 316–21.CrossRefGoogle ScholarPubMed
Kendler, K S, Kuhn, J W, Vittum, J, Prescott, C A, Riley, B (2005). The interaction of stressful life events and a serotonin transporter polymorphism in the prediction of episodes of major depression: a replication. Arch Gen Psychiatry 62: 529–35.CrossRefGoogle Scholar
Kinnally, E L (2007). Genetic and environmental factors that impact infant temperamental features and parameters of the serotonergic system associated with adult impulsivity in rhesus macaques (Macaca mulatta). Davis, CA: Department of Psychology, University of California at Davis. 100 pp.Google Scholar
Kinnally, E L, Jensen, H A, Ewing, J H, French, J A (2006). Serotonin function is associated with behavioral response to a novel conspecific in marmosets. Am J Primatol 68: 812–24.CrossRefGoogle ScholarPubMed
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 Behav 7: 481–6.CrossRefGoogle ScholarPubMed
Konno, K, Matsumoto, M, Togashi, H, et al. (2007). Early postnatal stress affects the serotonergic function in the median raphe nuclei of adult rats. Brain Res 1172: 60–6.CrossRefGoogle ScholarPubMed
Kraemer, G W, Clarke, A S (1996). Social attachment, brain function, and aggression. Ann NY Acad Sci 794: 121–35.CrossRefGoogle ScholarPubMed
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. Biol Psychiatry63: 317–24.CrossRefGoogle ScholarPubMed
Kruesi, M J, Rapoport, J L, Hamburger, S, et al. (1990). Cerebrospinal fluid monoamine metabolites, aggression, and impulsivity in disruptive behavior disorders of children and adolescents. Arch Gen Psychiatry 47: 419–26.CrossRefGoogle ScholarPubMed
Lesch, K P, Bengel, D, Heils, A, et al. (1996). Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274: 1527–31.CrossRefGoogle ScholarPubMed
Lesch, K P, Meyer, J, Glatz, K, et al. (1997). The 5-HT transporter gene-linked polymorphic region (5-HTTLPR) in evolutionary perspective: alternative biallelic variation in rhesus monkeys. Rapid communication. J Neural Transm 104: 1259–66.CrossRefGoogle ScholarPubMed
Lucki, I (1998). The spectrum of behaviors influenced by serotonin. Biol Psychiatry 44: 151–62.CrossRefGoogle ScholarPubMed
Lyons-Ruth, K, Holmes, B M, Sasvari-Szekely, M, Ronai, Z, Nemoda, Z, Pauls, D (2007). Serotonin transporter polymorphism and borderline or antisocial traits among low-income young adults. Psychiatr Genet 17: 339–43.CrossRefGoogle ScholarPubMed
MacTurk, R H, Morgan, G A (1995). Mastery motivation: origins, conceptualizations, and applications. Norwood, NJ: Ablex, pp. xiii, 376 pp.Google Scholar
Maestripieri, D, Higley, J D, Lindell, S G, Newman, T K, McCormack, K M, Sanchez, M M (2006a). Early maternal rejection affects the development of monoaminergic systems and adult abusive parenting in rhesus macaques (Macaca mulatta). Behav Neurosci 120: 1017–24.CrossRefGoogle Scholar
Maestripieri, D, Lindell, S G, Higley, J D (2007). Intergenerational transmission of maternal behavior in rhesus macaques and its underlying mechanisms. Dev Psychobiol 49: 165–71.CrossRefGoogle ScholarPubMed
Maestripieri, D, McCormack, K, Lindell, S G, Higley, J D, Sanchez, M M (2006b). Influence of parenting style on the offspring's behavior and CSF monoamine metabolite levels in crossfostered and noncrossfostered female rhesus macaques. Behav Brain Res 175: 90–5.CrossRefGoogle ScholarPubMed
Malison, R T, Price, L H, Berman, R, et al. (1998). Reduced brain serotonin transporter availability in major depression as measured by [123I]-2 beta-carbomethoxy-3 beta-(4-iodophenyl)tropane and single photon emission computed tomography. Biol Psychiatry 44: 1090–8.CrossRefGoogle Scholar
Mathew, S J, Coplan, J D, Smith, E L, et al. (2002). Cerebrospinal fluid concentrations of biogenic amines and corticotropin-releasing factor in adolescent non-human primates as a function of the timing of adverse early rearing. Stress 5: 185–93.CrossRefGoogle ScholarPubMed
McEwen, B S (2006). Protective and damaging effects of stress mediators: central role of the brain. Dialog Clin Neurosci 8: 367–81.Google Scholar
McEwen, B S (2007). Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87: 873–904.CrossRefGoogle Scholar
Mehlman, P T, Higley, J D, Faucher, I, et al. (1995). Correlation of CSF 5-HIAA concentration with sociality and the timing of emigration in free-ranging primates. Am J Psychiatry 152: 907–13.Google ScholarPubMed
Morgan, C A, Grillon, C, Southwick, S M, Davis, M, Charney, D S (1996). Exaggerated acoustic startle reflex in Gulf War veterans with posttraumatic stress disorder. Am J Psychiatry 153: 64–8.Google ScholarPubMed
Murphy, D L, Lerner, A, Rudnick, G, Lesch, K P (2004). Serotonin transporter: gene, genetic disorders, and pharmacogenetics. Mol Interv 4: 109–23.CrossRefGoogle ScholarPubMed
O'Hara, R, Schroder, C M, Mahadevan, R, et al. (2007). Serotonin transporter polymorphism, memory and hippocampal volume in the elderly: association and interaction with cortisol. Mol Psychiatry 12: 544–55.CrossRefGoogle ScholarPubMed
Pezawas, L, Meyer-Lindenberg, A, Drabant, E M, et al. (2005). 5-HTTLPR polymorphism impacts human cingulate–amygdala interactions: a genetic susceptibility mechanism for depression. Nat Neurosci 8: 828–34.CrossRefGoogle Scholar
Pietraszek, M H, Takada, Y, Yan, D, Urano, T, Serizawa, K, Takada, A (1992). Relationship between serotonergic measures in periphery and the brain of mouse. Life Sci 51: 75–82.CrossRefGoogle ScholarPubMed
Rogers, J, Kaplan, J, Garcia, R, Shelledy, W, Nair, S, Cameron, J (2006). Mapping of the serotonin transporter locus (SLC6A4) to rhesus chromosome 16 using genetic linkage. Cytogenet Genome Res 112: 341A.CrossRefGoogle ScholarPubMed
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 Behav 7: 463–9.CrossRefGoogle ScholarPubMed
Rosenblum, L A, Andrews, M (1994). Influences of environmental demand on maternal behavior and infant development. Acta Paediatr 397: 57–63.CrossRefGoogle ScholarPubMed
Rosenblum, L A, Paully, G S (1984). The effects of varying environmental demands on maternal and infant behavior. Child Dev 55: 305–14.CrossRefGoogle ScholarPubMed
Roy, A, Hu, X Z, Janal, M N, Goldman, D (2007). Interaction between childhood trauma and serotonin transporter gene variation in suicide. Neuropsychopharmacology 32: 2046–52.CrossRefGoogle ScholarPubMed
Roy, A, Virkkunen, M, Guthrie, S, Linnoila, M (1986). Indices of serotonin and glucose metabolism in violent offenders, arsonists, and alcoholics. Ann NY Acad Sci 487: 202–20.CrossRefGoogle ScholarPubMed
Rutter, M, Marshall, P J, Fox, N A (2006a). The psychological effects of early institutional rearing. The development of social engagement: neurobiological perspectives. New York: Oxford University Press, pp. 355–91.CrossRefGoogle Scholar
Rutter, M, Moffitt, T E, Caspi, A (2006b). Gene–environment interplay and psychopathology: multiple varieties but real effects. J Child Psychol Psychiatry 47: 226–61.CrossRefGoogle ScholarPubMed
Sakai, J T, Young, S E, Stallings, M C, et al. (2006). Case-control and within-family tests for an association between conduct disorder and 5HTTLPR. Am J Med Genet B Neuropsychiatr Genet 141: 825–32.CrossRefGoogle Scholar
Sanchez, M M (2006). The impact of early adverse care on HPA axis development: nonhuman primate models. Horm Behav 50: 623–31.CrossRefGoogle ScholarPubMed
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 Res 812: 38–49.CrossRefGoogle ScholarPubMed
Schneider, M L, Moore, C F, Suomi, S J, Champoux, M (1991). Laboratory assessment of temperament and environmental enrichment in rhesus monkey infants (Macaca mulatta). Am J Primatol 25: 137–55.CrossRefGoogle Scholar
Shanahan, M J, Hofer, S M (2005). Social context in gene–environment interactions: retrospect and prospect. J Gerontol B Psychol Sci Soc Sci60 Spec No 1: 65–76.CrossRefGoogle Scholar
Shannon, C, Schwandt, M L, Champoux, M, et al. (2005). Maternal absence and stability of individual differences in CSF 5-HIAA concentrations in rhesus monkey infants. Am J Psychiatry 162: 1658–64.CrossRefGoogle ScholarPubMed
Shively, C A, Fontenot, M B, Kaplan, J R (1995). Social status, behavior, and central serotonergic responsivity in female cynomolgus monkeys. Am J Primatol 37: 333–9.CrossRefGoogle Scholar
Sjoberg, R L, Nilsson, K W, Nordquist, N, et al. (2006). Development of depression: sex and the interaction between environment and a promoter polymorphism of the serotonin transporter gene. Int J Neuropsychopharmacol 9: 443–9.CrossRefGoogle Scholar
Spinelli, S, Schwandt, M L, Lindell, S G, et al. (2007). Association between the recombinant human serotonin transporter linked promoter region polymorphism and behavior in rhesus macaques during a separation paradigm. Dev Psychopathol 19: 977–87.CrossRefGoogle ScholarPubMed
Suomi, S J (1979). Peers, play, and primary prevention in primates. In Kent, M, Rolf, J, editors. Primary prevention of psychopathology: Social competence in children. Hanover, NH: Press of New England, pp. 127–49.Google Scholar
Suomi, S J (1987). Genetic and maternal contributions to individual differences in rhesus monkey biobehavioral development. In Krasnegor, N A, Blass, E M, Hofer, M A, editors. Perinatal development: a psychobiological perspective. San Diego, CA: Academic Press, pp. 397–419.Google Scholar
Suomi, S J, Harlow, H F (1972). Social rehabilitation of isolate-reared monkeys. Dev Psychol 6: 487–96.CrossRefGoogle Scholar
Surtees, P G, Wainwright, N W, Willis-Owen, S A, Luben, R, Day, N E, Flint, J (2006). Social adversity, the serotonin transporter (5-HTTLPR) polymorphism and major depressive disorder. Biol Psychiatry 59: 224–9.CrossRefGoogle ScholarPubMed
Thierry, B, Iwaniuk, A N, Pellis, S M (2000). The influence of phylogeny on the social behavior of macaques (Primates: Cercopithecidae, genus Macaca). Ethology 106: 713–28.CrossRefGoogle Scholar
Udenfriend, S, Weissbach, H (1958). Turnover of 5-hydroxytryptamine (serotonin) in tissues. Proc Soc Exp Biol Med 97: 748–51.CrossRefGoogle Scholar
,USDHHS (2000) Mental health: a report of the Surgeon General. In USDoHaH, editor. U.S. Department of Health and Human Services, Substance Abuse and Mental Health Services Administration, Center for Mental Health Services, National Institutes of Health, National Institute of Mental Health.
Wendland, J R, Lesch, K P, Newman, T K, et al. (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: 163–72.CrossRefGoogle ScholarPubMed
Wilhelm, K, Mitchell, P B, Niven, H, et al. (2006). Life events, first depression onset and the serotonin transporter gene. Br J Psychiatry 188: 210–5.CrossRefGoogle ScholarPubMed
Yan, D, Urano, T, Pietraszek, M H, et al. (1993). Correlation between serotonergic measures in cerebrospinal fluid and blood of subhuman primate. Life Sci 52: 745–9.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×