Advertisement

Reactivity and Behavioral Inhibition as Personality Traits in Nonhuman Primates

  • Stephen J. SuomiEmail author
  • Andrew C. Chaffin
  • J. Dee Higley
Chapter
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)

Abstract

While the history of the study of personality dates back to the early 1900s, most animal research, particularly on nonhuman primates, is much more recent. That personality in animals reflects our common evolutionary history is not surprising, and given our close genetic relatedness, should be expected. The personality trait that has received the most research in nonhuman primates is what we have called elsewhere, reactivity (others have referred to it as fearfulness, timidity, shyness, etc.). While several methods have been used to study it (including personality rating scales), generally, reactivity in nonhuman primates is most often measured using behavior codings. Two paradigms have received the most research: social separations and the human intruder paradigm. Individual differences in reactivity are stable across time and situations. Reactivity can also predict multiple behavioral outcomes, including enduring anxiety, low social dominance rank and submissiveness, high alcohol intake, and other forms of affective psychopathology. One major advantage of using nonhuman primates to model personality is that the underlying physiology and central nervous system foundations can be more readily studied than in humans. These studies show the importance of the amygdala and frontal cortex, as well as the HPA Axis, central norepinephrine, and serotonin in regulating reactivity. Studies also show the importance of early parental influence and genes on reactivity. Recent studies using molecular genetics show that the serotonin transporter and corticotrophin releasing hormone genes probably play important roles in its etiology but interact with early rearing history and situations to modulate reactivity.

Keywords

Nonhuman Primate Rhesus Macaque Corticotrophin Release Hormone Short Allele Pigtail Macaque 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abbott DH, Keverne EB, Bercovitch FB et al. (2003) Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 43:67–82PubMedGoogle Scholar
  2. Ainsworth MDS, Blehar MC, Waters E et al. (1978) Patterns of attachment: A psychological study of the strange situation. Lawrence Erlbaum Associates, HillsdaleGoogle Scholar
  3. Anderson GM, Bennett AJ, Weld KP et al. (2002) Serotonin in cisternal cerebrospinal fluid of rhesus monkeys: Basal levels and effects of sertraline administration. Psychopharmacology 161:95–99PubMedGoogle Scholar
  4. Arango V, Underwood MD, Boldrini M et al. (2001) Serotonin 1A receptors, serotonin transporter binding and serotonin transporter mRNA expression in the brainstem of depressed suicide victims. Neuropsychopharmacology 25:892–903PubMedGoogle Scholar
  5. Arango V, Underwood MD, Mann JJ (2002) Serotonin brain circuits involved in major depression and suicide. Prog Brain Res 136:443–453PubMedGoogle Scholar
  6. Barr CS, Dvoskin RL, Yuan Q et al. (2008a) 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. Arch Gen Psychiatry 65:934–944PubMedGoogle Scholar
  7. Barr CS, Newman TK, Lindell S et al. (2004a) Early experience and sex interact to influence limbic-hypothalamic-pituitary-adrenal-axis function after acute alcohol administration in rhesus macaques (Macaca mulatta). Alcohol Clin Exp Res 28:1114–1119PubMedGoogle Scholar
  8. Barr CS, Newman TK, Lindell S et al. (2004b) Interaction between serotonin transporter gene variation and rearing condition in alcohol preference and consumption in female primates. Arch Gen Psychiatry 61:1146–1152PubMedGoogle Scholar
  9. Barr CS, Newman TK, Schwandt M et al. (2004c) Sexual dichotomy of an interaction between early adversity and the serotonin transporter gene promoter variant in rhesus macaques. Proc Natl Acad Sci USA 101:12358–12363PubMedGoogle Scholar
  10. Barr CS, Newman TK, Shannon C et al. (2004d) Rearing condition and rh5-HTTLPR interact to influence limbic-hypothalamic-pituitary-adrenal axis response to stress in infant macaques. Biol Psychiatry 55:733–738PubMedGoogle Scholar
  11. Barr CS, Schwandt ML, Lindell SG et al. (2008b) Variation at the mu-opioid receptor gene (OPRM1) influences attachment behavior in infant primates. Proc Natl Acad Sci USA 105:5277–5281PubMedGoogle Scholar
  12. Bayart F, Hayashi KT, Faull KF et al. (1990) Influence of maternal proximity on behavioral and physiological responses to separation in infant rhesus monkeys (Macaca mulatta). Behav Neurosci 104:98–107PubMedGoogle Scholar
  13. Becker ML, Bernhards DE, Chisholm KL et al. (2004) Calling rate as a measure of stress reactivity in mother- and nursery-reared rhesus infants (Macaca mulatta). Am J Primatol 62:60Google Scholar
  14. Becker MS, Suomi SJ, Marra L et al. (1984) Developmental data as predictors of depression in infant rhesus monkeys. Infant Behav Dev 7:26Google Scholar
  15. Bennett AJ, Lesch KP, Heils A et al. (2002) Early experience and serotonin transporter gene variation interact to influence primate CNS function. Mol Psychiatry 7:118–122PubMedGoogle Scholar
  16. Bernstein IS, Schusterman RJ, Sharpe LG (1963) A comparison of rhesus monkey and gibbon responses to unfamiliar situations. J Comp Physiol Psychol 56:914–916PubMedGoogle Scholar
  17. Bethea CL, Streicher JM, Coleman K et al. (2004) Anxious behavior and fenfluramine-induced prolactin secretion in young rhesus macaques with different alleles of the serotonin reuptake transporter polymorphism (5HTTLPR). Behav Genet 34:295–307PubMedGoogle Scholar
  18. Biederman J, Hirshfeld-Becker DR, Rosenbaum JF et al. (2001) Further evidence of association between behavioral inhibition and social anxiety in children. Am J Psychiatry 158:1673–1679PubMedGoogle Scholar
  19. Biederman J, Rosenbaum JF, Bolduc-Murphy EA et al. (1993) A 3-year follow-up of children with and without behavioral inhibition. J Am Acad Child Adolesc Psychiatry 32:814–821PubMedGoogle Scholar
  20. Blizard DA (1981) The Maudsley reactive and nonreactive strains: a North American perspective. Behav Genet 11:469–489PubMedGoogle Scholar
  21. Blizard DA (1989) Analysis of stress susceptibility using the Maudsley reactive and non-reactive strains. In: Palermo DS (ed) Coping with uncertainty: Behavioral and developmental perspectives. Lawrence Erlbaum Associates, HillsdaleGoogle Scholar
  22. Bolig R, Price CS, O’Neill PL et al. (1992) Subjective assessment of reactivity level and personality traits of rhesus monkeys. Int J Primatol 13:287–306Google Scholar
  23. Bowlby J (1973) Attachment and loss: Separation. Basic Books, Inc., New YorkGoogle Scholar
  24. Bush DS, Steffen SL, Higley JD et al. (1987) Continuity of social separation responses in rhesus monkeys (Macaca mulatta) reared under different conditions. Am J Primatol 18:138Google Scholar
  25. Buss KA, Schumacher JR, Dolski I et al. (2003) Right frontal brain activity, cortisol, and withdrawal behavior in 6-month-old infants. Behav Neurosci 117:11–20PubMedGoogle Scholar
  26. Byrne EA, DiGregorio G, Thompson WW (1988) The effect of rearing environment on infant rhesus monkeys’ physiological and behavioral adaptation to novelty. Infant Behav Dev 11:43Google Scholar
  27. Capitanio JP (2004) Personality factors between and within species. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: A model for the study of social organizations. Cambridge University Press, CambridgeGoogle Scholar
  28. Capitanio JP (2008) Personality and disease. Brain Behav Immun 22:647–650PubMedGoogle Scholar
  29. Capitanio JP, Rasmussen KL, Snyder DS et al. (1986) Long-term follow-up of previously separated pigtail macaques: Group and individual differences in response to novel situations. J Child Psychol Psychiatry 27:531–538PubMedGoogle Scholar
  30. Capitanio JP, Widaman KF (2005) Confirmatory factor analysis of personality structure in adult male rhesus monkeys (Macaca mulatta). Am J Primatol 65:289–294PubMedGoogle Scholar
  31. Chamove AS, Eysenck HJ, Harlow HF (1972) Personality in monkeys: Factor analyses of rhesus social behaviour. Q J Exp Psychol 24:496–504PubMedGoogle Scholar
  32. Chamove AS, Rosenblum LA, Harlow HF (1973) Monkeys (Macaca mulatta) raised with only peers. A pilot study. Anim Behav 21:316–325PubMedGoogle Scholar
  33. Champoux M (1988a) Behavioral development and temporal stability of reactivity to stressors in mother-reared and nursery/peer-reared rhesus macaques. University of Wisconsin, MadisonGoogle Scholar
  34. Champoux M (1988b) Behavioral development of nursery-reared rhesus monkeys (Macaca mulatta) neonates. Infant Behav Dev 11:367–371Google Scholar
  35. Champoux M, Bennett A, Shannon C et al. (2002) Serotonin transporter gene polymorphism, differential early rearing, and behavior in rhesus monkey neonates. Mol Psychiatry 7:1058–1063PubMedGoogle Scholar
  36. Champoux M, Higley JD, Suomi SJ (1997) Behavioral and physiological characteristics of Indian and Chinese-Indian hybrid rhesus macaque infants. Dev Psychobiol 31:49–63PubMedGoogle Scholar
  37. Champoux M, Suomi SJ, Schneider ML (1994) Temperament differences between captive Indian and Chinese-Indian hybrid rhesus macaque neonates. Lab Anim Sci 44:351–357PubMedGoogle Scholar
  38. Clarke AS, Boinski S (1995) Temperament in nonhuman primates. Am J Primatol 37:103–125Google Scholar
  39. Clarke AS, Hedeker DR, Ebert MH et al. (1996) Rearing experience and biogenic amine activity in infant rhesus monkeys. Biol Psychiatry 40:338–352PubMedGoogle Scholar
  40. Clarke AS, Mason WA, Moberg GP (1988) Interspecific contrasts in responses of macaques to transport cage training. Lab Anim Sci 38:305–309PubMedGoogle Scholar
  41. Cloninger CR (1986) A unified biosocial theory of personality and its role in the development of anxiety states. Psychiatr Dev 3:167–226Google Scholar
  42. Cloninger CR (1994) Temperament and personality. Curr Opin Neurobiol 4:266–273PubMedGoogle Scholar
  43. Critchley HD, Simmons A, Daly EM et al. (2000) Prefrontal and medial temporal correlates of repetitive violence to self and others. Biol Psychiatry 47:928–934PubMedGoogle Scholar
  44. Cross N, Rogers LJ (2006) Mobbing vocalizations as a coping response in the common marmoset. Horm Behav 49:237–245PubMedGoogle Scholar
  45. Davidson RJ, Fox NA (1989) Frontal brain asymmetry predicts infants’ response to maternal separation. J Abnorm Psychol 98:127–131PubMedGoogle Scholar
  46. Doudet D, Hommer D, Higley JD et al. (1995) Cerebral glucose metabolism, CSF 5-HIAA levels, and aggressive behavior in rhesus monkeys. Am J Psychiatry 152:1782–1787PubMedGoogle Scholar
  47. Erickson K, Gabry KE, Lindell S et al. (2005) Social withdrawal behaviors in nonhuman primates and changes in neuroendocrine and monoamine concentrations during a separation paradigm. Dev Psychobiol 46:331–339PubMedGoogle Scholar
  48. Erickson K, Lindell S, Champoux M et al. (2001) Relationships between behavior and neurochemical changes in rhesus macaques during a separation paradigm. Soc Neurosci Abstr 27, program 572:14Google Scholar
  49. Eysenck HJ, Eysenck MW (1985) Personality and individual differences. A natural science approach. Plenum, New YorkGoogle Scholar
  50. Eysenck HJ, Eysenck SBG (1976) Psychoticism as a dimension of personality. Hodder and Stoughton, LondonGoogle Scholar
  51. Fahlke C, Lorenz JG, Long J et al. (2000) Rearing experiences and stress-induced plasma cortisol as early risk factors for excessive alcohol consumption in nonhuman primates. Alcohol Clin Exp Res 24:644–650PubMedGoogle Scholar
  52. Fairbanks LA (2001) Individual differences in response to a stranger: Social impulsivity as a dimension of temperament in vervet monkeys (Cercopithecus aethiops sabaeus). J Comp Psychol 115:22–28PubMedGoogle Scholar
  53. Fox AS, Oakes TR, Shelton SE et al. (2005) Calling for help is independently modulated by brain systems underlying goal-directed behavior and threat perception. Proc Natl Acad Sci USA 102:4176–4179PubMedGoogle Scholar
  54. Francois MH, Nosten BM, Roubertoux PL et al. (1990) Opponent strain effect on eliciting attacks in NZB mice: Physiological correlates. Physiol Behav 47:1181–1185PubMedGoogle Scholar
  55. Gabry KE, Erickson K, Champoux M et al. (unpublished manuscript) Increased CSF corticotropin-releasing hormone and decreased neuropeptide Y concentrations in response to psychosocial stressGoogle Scholar
  56. Gibbs RA, Rogers J, Katze MG et al. (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science 316:222–234PubMedGoogle Scholar
  57. Gonda X, Fountoulakis KN, Juhasz G et al. (2009) Association of the s allele of the 5-HTTLPR with neuroticism-related traits and temperaments in a psychiatrically healthy population. Eur Arch Psychiatry Clin Neurosci 259:106–113PubMedGoogle Scholar
  58. Gray JA (1987) The psychology of fear and stress. Cambridge University Press, New YorkGoogle Scholar
  59. Habib KE, Weld KP, Rice KC et al. (2000) Oral administration of a corticotropin-releasing hormone receptor antagonist significantly attenuates behavioral, neuroendocrine, and autonomic responses to stress in primates. Proc Natl Acad Sci USA 97:6079–6084PubMedGoogle Scholar
  60. Hariri AR, Mattay VS, Tessitore A et al. (2002) Serotonin transporter genetic variation and the response of the human amygdala. Science 297:400–403PubMedGoogle Scholar
  61. Harlow HF (1969) Age-mate or peer affectional system. Adv Study Behav 2:333–383Google Scholar
  62. Harlow HF, Harlow MK (1965) The affectional systems. In: Schrier AM, Harlow HF, Stollinitz F (eds) Behavior of nonhuman primates. Academic, New YorkGoogle Scholar
  63. Harris RA, Rogers J, Milosavljevic A (2007) Human-specific changes of genome structure detected by genomic triangulation. Science 316:235–237PubMedGoogle Scholar
  64. Heilig M, Koob GF, Ekman R et al. (1994) Corticotropin-releasing factor and neuropeptide Y: Role in emotional integration. Trends Neurosci 17:80–85PubMedGoogle Scholar
  65. Hernandez RD, Hubisz MJ, Wheeler DA et al. (2007) Demographic histories and patterns of linkage disequilibrium in Chinese and Indian rhesus macaques. Science 316:240–243PubMedGoogle Scholar
  66. Higley JD (1985) Continuity of social separation behaviors in rhesus monkeys from infancy to adolescence. University of Wisconsin, MadisonGoogle Scholar
  67. Higley JD, Danner GR (1988) Attachment in rhesus monkeys reared either with only peers or with their mothers as assessed by the Ainsworth Strange Situation procedure. Infant Behav Dev 11:139Google Scholar
  68. Higley JD, Hasert MF, Suomi SJ et al. (1991a) Nonhuman primate model of alcohol abuse: Effects of early experience, personality, and stress on alcohol consumption. Proc Natl Acad Sci USA 88:7261–7265PubMedGoogle Scholar
  69. Higley JD, Hopkins WD, Thompson WW et al. (1992a) Peers as primary attachment sources in yearling rhesus monkeys (Macaca mulatta). Dev Psychol 28:1163–1171Google Scholar
  70. Higley JD, Linnoila M (1997a) Low central nervous system serotonergic activity is traitlike and correlates with impulsive behavior. A nonhuman primate model investigating genetic and environmental influences on neurotransmission. Ann N Y Acad Sci 836:39–56PubMedGoogle Scholar
  71. Higley JD, Linnoila M (1997b) A nonhuman primate model of excessive alcohol intake: Personality and neurobiological parallels of Type I- and Type II-like alcoholism. Recent Dev Alcohol 13:192–219Google Scholar
  72. Higley JD, Linnoila M, Suomi SJ (1994) Ethological contributions: Experiential and genetic contributions to the expression and inhibition of aggression in primates. In: Hersen M, Ammerman RT, Sisson L (eds) Handbook of aggressive and destructive behavior in psychiatric patients. Plenum Press, New YorkGoogle Scholar
  73. Higley JD, Mehlman PT, Higley SB et al. (1996a) Excessive mortality in young free-ranging male nonhuman primates with low cerebrospinal fluid 5-hydroxyindoleacetic acid. Arch Gen Psychiatry 53:537–543PubMedGoogle Scholar
  74. Higley JD, Mehlman PT, Poland RE et al. (1996b) CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors. Biol Psychiatry 40:1067–1082PubMedGoogle Scholar
  75. Higley JD, Mehlman PT, Taub DM et al. (1992b) Cerebrospinal fluid monoamine and adrenal correlates of aggression in free-ranging rhesus monkeys. Arch Gen Psychiatry 49:436–441PubMedGoogle Scholar
  76. Higley JD, Suomi SJ, Linnoila M (1990) Parallels in aggression and serotonin: Consideration of development, rearing history, and sex differences. In: van Praag HM, Plutchik R, Apter A (eds) Violence and suicidality: Perspectives in clinical and psychobiological research. Brunner/Mazel, New YorkGoogle Scholar
  77. Higley JD, Suomi SJ, Linnoila M (1991b) CSF monoamine metabolite concentrations vary according to age, rearing, and sex, and are influenced by the stressor of social separation in rhesus monkeys. Psychopharmacology 103:551–556PubMedGoogle Scholar
  78. Higley JD, Suomi SJ, Linnoila M (1992c) A longitudinal assessment of CSF monoamine metabolite and plasma cortisol concentrations in young rhesus monkeys. Biol Psychiatry 32:127–145PubMedGoogle Scholar
  79. Higley JD, Suomi SJ, 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 20:643–650PubMedGoogle Scholar
  80. Higley JD, Suomi SJ, 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 20:629–642PubMedGoogle Scholar
  81. Higley JD, Suomi SJ, Scanlan JM et al. (1982) Plasma cortisol as a predictor of individual depressive behavior in rhesus monkeys (Macaca mulatta). Paper presented at the meeting of Society for Neuroscience, Minneapolis, MNGoogle Scholar
  82. Higley JD, Thompson WW, Champoux M et al. (1993) Paternal and maternal genetic and environmental contributions to cerebrospinal fluid monoamine metabolites in rhesus monkeys (Macaca mulatta). Arch Gen Psychiatry 50:615–623PubMedGoogle Scholar
  83. Hill SY, Lowers L, Locke J et al. (1999) Behavioral inhibition in children from families at high risk for developing alcoholism. J Am Acad Child Adolesc Psychiatry 38:410–417PubMedGoogle Scholar
  84. Hinde RA, Simpson MJA (1967) Qualities of mother-infant relationships in monkeys. Ciba Found Symp 33:39–68Google Scholar
  85. Holmes A, le Guisquet AM, Vogel E et al. (2005) Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neurosci Biobehav Rev 29:1335–1346PubMedGoogle Scholar
  86. Howell S, Westergaard G, Hoos B et al. (2007) Serotonergic influences on life-history outcomes in free-ranging male rhesus macaques. Am J Primatol 69:851–865PubMedGoogle Scholar
  87. Ichise M, Vines DC, Gura T et al. (2006) Effects of early life stress on [11 C]DASB positron emission tomography imaging of serotonin transporters in adolescent peer- and mother-reared rhesus monkeys. J Neurosci 26:4638–4643PubMedGoogle Scholar
  88. Insel TR, Hill JL (1987) Infant separation distress in genetically fearful rats. Biol Psychiatry 22:786–789PubMedGoogle Scholar
  89. Jarrell H, Hoffman JB, Kaplan JR et al. (2008) Polymorphisms in the serotonin reuptake transporter gene modify the consequences of social status on metabolic health in female rhesus monkeys. Physiol Behav 93:807–819PubMedGoogle Scholar
  90. Jedema HP, Gianaros PJ, Greer PJ et al. (2010) Cognitive impact of genetic variation of the serotonin transporter in primates is associated with differences in brain morphology rather than serotonin neurotransmission. Mol Psychiatry 15:512–522, 446Google Scholar
  91. Kagan J (1992) Behavior, biology, and the meanings of temperamental constructs. Pediatrics 90:510–513PubMedGoogle Scholar
  92. Kagan J (1994) On the nature of emotion. Monogr Soc Res Child Dev 59:7–24PubMedGoogle Scholar
  93. Kagan J, Reznick JS, Snidman N (1987) The physiology and psychology of behavioral inhibition in children. Child Dev 58:1459–1473PubMedGoogle Scholar
  94. Kagan J, Reznick JS, Snidman N (1988) Biological bases of childhood shyness. Science 240:167–171PubMedGoogle Scholar
  95. Kalin NH (1993) The neurobiology of fear. Sci Am 268:94–101PubMedGoogle Scholar
  96. Kalin NH (1999) Primate models to understand human aggression. J Clin Psychiatry 60, Supplement 15:29–32Google Scholar
  97. Kalin NH, Larson C, Shelton SE et al. (1998a) Asymmetric frontal brain activity, cortisol, and behavior associated with fearful temperament in rhesus monkeys. Behav Neurosci 112:286–292PubMedGoogle Scholar
  98. Kalin NH, Shelton SE (1989) Defensive behaviors in infant rhesus monkeys: Environmental cues and neurochemical regulation. Science 243:1718–1721PubMedGoogle Scholar
  99. Kalin NH, Shelton SE (2003) Nonhuman primate models to study anxiety, emotion regulation, and psychopathology. Ann N Y Acad Sci 1008:189–200PubMedGoogle Scholar
  100. Kalin NH, Shelton SE, Barksdale CM (1988) Opiate modulation of separation-induced distress in non-human primates. Brain Res 440:285–292PubMedGoogle Scholar
  101. Kalin NH, Shelton SE, Barksdale CM (1989) Behavioral and physiologic effects of CRH administered to infant primates undergoing maternal separation. Neuropsychopharmacology 2:97–104PubMedGoogle Scholar
  102. Kalin NH, Shelton SE, Davidson RJ (2000) Cerebrospinal fluid corticotropin-releasing hormone levels are elevated in monkeys with patterns of brain activity associated with fearful temperament. Biol Psychiatry 47:579–585PubMedGoogle Scholar
  103. Kalin NH, Shelton SE, Davidson RJ (2004) The role of the central nucleus of the amygdala in mediating fear and anxiety in the primate. J Neurosci 24:5506–5515PubMedGoogle Scholar
  104. Kalin NH, Shelton SE, Davidson RJ (2007) Role of the primate orbitofrontal cortex in mediating anxious temperament. Biol Psychiatry 62:1134–1139PubMedGoogle Scholar
  105. Kalin NH, Shelton SE, Fox AS et al. (2005) Brain regions associated with the expression and contextual regulation of anxiety in primates. Biol Psychiatry 58:796–804PubMedGoogle Scholar
  106. Kalin NH, Shelton SE, Fox AS et al. (2008) The serotonin transporter genotype is associated with intermediate brain phenotypes that depend on the context of eliciting stressor. Mol Psychiatry 13:1021–1027PubMedGoogle Scholar
  107. Kalin NH, Shelton SE, Kraemer GW et al. (1983) Corticotropin-releasing factor administered intraventricularly to rhesus monkeys. Peptides 4:217–220PubMedGoogle Scholar
  108. Kalin NH, Shelton SE, Rickman M et al. (1998b) Individual differences in freezing and cortisol in infant and mother rhesus monkeys. Behav Neurosci 112:251–254PubMedGoogle Scholar
  109. Kalin NH, Shelton SE, Snowdon CT (1992) Affiliative vocalizations in infant rhesus macaques (Macaca mulatta). J Comp Psychol 106:254–261PubMedGoogle Scholar
  110. Kalin NH, Shelton SE, Takahashi LK (1991) Defensive behaviors in infant rhesus monkeys: Ontogeny and context-dependent selective expression. Child Dev 62:1175–1183PubMedGoogle Scholar
  111. Keverne EB, Martensz ND, Tuite B (1989) Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinology 14:155–161PubMedGoogle Scholar
  112. King JE, Figueredo AJ (1997) The Five-Factor Model plus Dominance in chimpanzee personality. J Res Pers 31:271–271Google Scholar
  113. Kinnally EL, Lyons LA, Abel K et al. (2008) Effects of early experience and genotype on serotonin transporter regulation in infant rhesus macaques. Genes Brain Behav 7:481–486PubMedGoogle Scholar
  114. Kraemer GW (1997) Psychobiology of early social attachment in rhesus monkeys. Clinical implications. Ann N Y Acad Sci 807:401–418PubMedGoogle Scholar
  115. Kraemer GW, Ebert MH, Schmidt DE et al. (1989) A longitudinal study of the effect of different social rearing conditions on cerebrospinal fluid norepinephrine and biogenic amine metabolites in rhesus monkeys. Neuropsychopharmacology 2:175–189PubMedGoogle Scholar
  116. Lee AS, Gutierrez-Arcelus M, Perry GH et al. (2008) Analysis of copy number variation in the rhesus macaque genome identifies candidate loci for evolutionary and human disease studies. Hum Mol Genet 17:1127–1136PubMedGoogle Scholar
  117. Levine S, Wiener SG (1988) Psychoendocrine aspects of mother-infant relationships in nonhuman primates. Psychoneuroendocrinology 13:143–154PubMedGoogle Scholar
  118. Levine S, Wiener SG, Coe CL et al. (1987) Primate vocalization: A psychobiological approach. Child Dev 58:1408–1419PubMedGoogle Scholar
  119. Liang B, Blizard DA (1978) Central and peripheral norepinephrine concentrations in rat strains selectively bred for differences in response to stress: Confirmation and extension. Pharmacol Biochem Behav 8:75–80PubMedGoogle Scholar
  120. Lopez JF, Higley JD (2002) The effect of early experience on brain corticosteroid and serotonin receptors in rhesus monkeys. Biol Psychiatry 51:100S–100SGoogle Scholar
  121. Lopez JF, Vazquez DM, Zimmer CA et al. (2001) Chronic unpredictable stress and antidepressant modulation of mineralocorticoid, and glucocorticoid receptors. Soc Neurosci Abstr 27, program 352Google Scholar
  122. Lyons DM, Martel FL, Levine S et al. (1999) Postnatal experiences and genetic effects on squirrel monkey social affinities and emotional distress. Horm Behav 36:266–275PubMedGoogle Scholar
  123. Machado CJ, Emery NJ, Capitanio JP et al. (2008) Bilateral neurotoxic amygdala lesions in rhesus monkeys (Macaca mulatta): Consistent pattern of behavior across different social contexts. Behav Neurosci 122:251–266PubMedGoogle Scholar
  124. Mason WA, Capitanio JP, Machado CJ et al. (2006) Amygdalectomy and responsiveness to novelty in rhesus monkeys (Macaca mulatta): Generality and individual consistency of effects. Emotion 6:73–81PubMedGoogle Scholar
  125. McCormack K, Newman TK, Higley JD et al. (2009) Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants. Horm Behav 55:538–547PubMedGoogle Scholar
  126. McKinney WT, Jr., Suomi SJ, Harlow HF (1972) Repetitive peer separations of juvenile-age rhesus monkeys. Arch Gen Psychiatry 27:200–203PubMedGoogle Scholar
  127. Mineka S, Davidson M, Cook M et al. (1984) Observational conditioning of snake fear in rhesus monkeys. J Abnorm Psychol 93:355–372PubMedGoogle Scholar
  128. Mineka S, Suomi SJ (1978) Social separation in monkeys. Psychol Bull 85:1376–1400PubMedGoogle Scholar
  129. Mineka S, Suomi SJ, DeLizio R (1981) Multiple separations in adolescent monkeys: An opponent-process interpretation. J Exp Psychol Gen 110:56–85PubMedGoogle Scholar
  130. Munafo MR, Brown SM, Hariri AR (2008) Serotonin transporter (5-HTTLPR) genotype and amygdala activation: A meta-analysis. Biol Psychiatry 63:852–857PubMedGoogle Scholar
  131. Newman TK, Syagailo YV, Barr CS et al. (2005) Monoamine oxidase A gene promoter variation and rearing experience influences aggressive behavior in rhesus monkeys. Biol Psychiatry 57:167–172PubMedGoogle Scholar
  132. Norcross JL, Newman JD (1999) Effects of separation and novelty on distress vocalizations and cortisol in the common marmoset (Callithrix jacchus). Am J Primatol 47:209–222PubMedGoogle Scholar
  133. Novak MA, Harlow HF (1975) Social recovery of monkeys isolated for the first year of life: 1. Rehabilitation and therapy. Dev Psychol 11:453–465Google Scholar
  134. Popova NK (2006) From genes to aggressive behavior: The role of serotonergic system. Bioessays 28:495–503PubMedGoogle Scholar
  135. Popova NK, Kulikov AV, Nikulina EM et al. (1991a) Serotonin metabolism and serotonergic receptors in Norway rats selected for low aggressiveness towards man. Aggress Behav 17:207–213Google Scholar
  136. Popova NK, Voitenko NN, Kulikov AV et al. (1991b) Evidence for the involvement of central serotonin in mechanism of domestication of silver foxes. Pharmacol Biochem Behav 40:751–756PubMedGoogle Scholar
  137. Popova NK, Voitenko NN, Trut LN (1976) Changes in the content of serotonin and 5-hydroxyindoleacetic acid in the brain in the selection of silver foxes according to behavior. Neurosci Behav Physiol 7:72–74PubMedGoogle Scholar
  138. Porrino L, Crane AM, Goldman-Rakic PS (1981) Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys. J Comp Neurol 198:121–136PubMedGoogle Scholar
  139. Raine A, Meloy JR, Bihrle S et al. (1998) Reduced prefrontal and increased subcortical brain functioning assessed using positron emission tomography in predatory and affective murderers. Behav Sci Law 16:319–332PubMedGoogle Scholar
  140. Rogers J, Shelton SE, Shelledy W et al. (2008) Genetic influences on behavioral inhibition and anxiety in juvenile rhesus macaques. Genes Brain Behav 7:463–469PubMedGoogle Scholar
  141. Rosenbaum JF, Biederman J, Hirshfeld DR et al. (1991) Further evidence of an association between behavioral inhibition and anxiety disorders: Results from a family study of children from a non-clinical sample. J Psychiatr Res 25:49–65PubMedGoogle Scholar
  142. Rosenblum LA, Kaufman IC (1967) Laboratory observations of early mother-infant relations in pigtail and bonnet macaques. In: Altmann SA (ed) Social communication among primates. University of Chicago Press, ChicagoGoogle Scholar
  143. Rouff JH, Sussman RW, Strube MJ (2005) Personality traits in captive lion-tailed macaques (Macaca silenus). Am J Primatol 67:177–198Google Scholar
  144. Ruchkin VV, Eisemann M, Hagglof B et al. (1998) Interrelations between temperament, character, and parental rearing in male delinquent adolescents in northern Russia. Compr Psychiatry 39:225–230PubMedGoogle Scholar
  145. Sandnabba NK (1996) Selective breeding for isolation-induced intermale aggression in mice: Associated responses and environmental influences. Behav Genet 26:477–488PubMedGoogle Scholar
  146. Scanlan JM (1984) Adrenocortical and behavioral responses to acute novel and stressful conditions: The influence of gonadal status, time course of response, age, and motor activity. University of Wisconsin, MadisonGoogle Scholar
  147. Scanlan JM (1987) Social dominance as a predictor of behavioral and pituitary-adrenal response to social separation in rhesus monkey infants. Society for Research in Child Development, Baltimore.Google Scholar
  148. Scanlan JM (1988) Continuity of stress responsivity in infant rhesus monkeys (Macaca mulatta): State, hormonal, dominance, and genetic influences. University of Wisconsin, Madison.Google Scholar
  149. Scanlan JM, Suomi SJ (1986) Social dominance as a predictor of behavioral and pituitary-adrenal response to social separation in rhesus monkey infants. International Society for Developmental Psychobiology, AnnapolisGoogle Scholar
  150. Scanlan JM, Suomi SJ (1988) Neonatal predictors of separation response in rhesus monkeys. Paper presented at the meeting of the American Society of Primatologists, New Orleans, LAGoogle Scholar
  151. Schneider ML, Suomi SJ (1992) Neurobehavioral assessment in rhesus monkey neonates (Macaca mulatta): Developmental changes, behavioral stability, and early experiences. Infant Behav Dev 15:155–177Google Scholar
  152. Schwartz CE, Wright CI, Shin LM et al. (2003) Inhibited and uninhibited infants “grown up”: Adult amygdalar response to novelty. Science 300:1952–1953PubMedGoogle Scholar
  153. Scott JP, Fuller JL (1965) Genetics and the social behavior of the dog. University of Chicago Press, ChicagoGoogle Scholar
  154. Scott PA, Cierpial MA, Kilts CD et al. (1996) Susceptibility and resistance of rats to stress-induced decreases in swim-test activity: a selective breeding study. Brain Res 725:217–230PubMedGoogle Scholar
  155. Seay B, Harlow HF (1965) Maternal separation in the rhesus monkey. J Nerv Ment Dis 140:434–444PubMedGoogle Scholar
  156. Sen S, Burmeister M, Ghosh D (2004) Meta-analysis of the association between a serotonin transporter promoter polymorphism (5-HTTLPR) and anxiety-related personality traits. Am J Med Genet B Neuropsychiatr Genet 127B:85–89PubMedGoogle Scholar
  157. Shannon C, Schwandt ML, Champoux M et al. (2005) Maternal absence and stability of individual differences in CSF 5-HIAA concentrations in rhesus monkey infants. Am J Psychiatry 162:1658–1664PubMedGoogle Scholar
  158. Singh R (1992) Ontogeny of behavioral dynamics among free-ranging rhesus monkeys (Macaca mulatta) theory and observation. In: Seth PK, Seth S (eds) Perspectives in primate biology. Today & Tomorrow’s Printers and Publisher’s, New DelhiGoogle Scholar
  159. Soubrié P (1986) Reconciling the role of central serotonin neurons in human and animal behavior. Behav Brain Sci 9:319–364Google Scholar
  160. Southwick SM, Vythilingam M, Charney DS (2005) The psychobiology of depression and resilience to stress: Implications for prevention and treatment. Ann Rev Clin Psychol 1:255–291Google Scholar
  161. Stallings MC, Hewitt JK, Cloninger CR et al. (1996) Genetic and environmental structure of the Tridimensional Personality Questionnaire: Three or four temperament dimensions? J Pers Soc Psychol 70:127–140PubMedGoogle Scholar
  162. Stevenson-Hinde J, Simpson MJA (1980) Subjective assessment of rhesus monkeys over four successive years. Primates 21:66–82Google Scholar
  163. Stevenson-Hinde J, Stillwell-Barnes R, Zunz M (1980) Individual differences in young rhesus monkeys: Consistency and change. Primates 21:498–509Google Scholar
  164. Stevenson-Hinde J, Zunz M (1978) Subjective assessment of individual rhesus monkeys. Primates 19:473–482Google Scholar
  165. Strome EM, Wheler GH, Higley JD et al. (2002) Intracerebroventricular corticotropin-releasing factor increases limbic glucose metabolism and has social context-dependent behavioral effects in nonhuman primates. Proc Natl Acad Sci USA 99:15749–15754PubMedGoogle Scholar
  166. Suomi SJ (1983) Social development in rhesus monkeys: Consideration of individual differences. In: Oliverio A, Zappella M (eds) The behavior of human infants. Plenum Press, New YorkGoogle Scholar
  167. Suomi SJ, Collins ML, Harlow HF et al. (1976) Effects of maternal and peer separations on young monkeys. J Child Psychol Psychiatry 17:101–112PubMedGoogle Scholar
  168. Suomi SJ, Harlow HF, Domek CJ (1970) Effect of repetitive infant-infant separation of young monkeys. J Abnorm Psychol 76:161–172PubMedGoogle Scholar
  169. Suomi SJ, Harlow HF, Novak MA (1974) Reversal of social deficits produced by isolation rearing in monkeys. J Hum Evol 3:527–534Google Scholar
  170. Suomi SJ, Kraemer GW, Baysinger CM et al. (1981) Inherited and experiential factors associated with individual differences in anxious behavior displayed by rhesus monkeys. In: Klein DF, Rabkin J (eds) Anxiety: New research and changing concepts. Raven Press, New YorkGoogle Scholar
  171. Suomi SJ, Mineka S, DeLizio RD (1983) Short- and long-term effects of repetitive mother-infant separations on social development in rhesus monkeys. Dev Psychol 19:770–786Google Scholar
  172. Suomi SJ, Scanlan JM, Rasmussen KL et al. (1989) Pituitary – adrenal response to capture in Cayo Santiago – derived group M rhesus monkeys. P R Health Sci J 8:171–176PubMedGoogle Scholar
  173. Thompson WW, Higley JD, Byrne EA et al. (1986) Behavioral inhibition in nonhuman primates: Psychobiological correlates and continuity over time. Paper presented at the meeting of the International Society for Developmental Psychobiology, Annapolis, MDGoogle Scholar
  174. Urry HL, van Reekum CM, Johnstone T et al. (2006) Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. J Neurosci 26:4415–4425PubMedGoogle Scholar
  175. van Oortmerssen GA, Bakker TC (1981) Artificial selection for short and long attack latencies in wild Mus musculus domesticus. Behav Genet 11:115–126PubMedGoogle Scholar
  176. van Stegeren AH (2008) The role of the noradrenergic system in emotional memory. Acta Psychol (Amst) 127:532–541Google Scholar
  177. Wahlestedt C, Pich EM, Koob GF et al. (1993) Modulation of anxiety and neuropeptide Y-Y1 receptors by antisense oligodeoxynucleotides. Science 259:528–531PubMedGoogle Scholar
  178. Watson KK, Ghodasra JH, Platt ML (2009) Serotonin transporter genotype modulates social reward and punishment in rhesus macaques. PLoS ONE 4:e4156PubMedGoogle Scholar
  179. Weinstein TAR, Capitanio JP, Gosling SD (2008) Personality in animals. In: John OP, Robins RW, Pervin LA (eds) Handbook of personality: Theory and research. Guilford Press, New YorkGoogle Scholar
  180. Weiss A, Adams MJ, Widdig A, Gerald MS (2011) Rhesus macaques (Macaca mulatta) as living fossils of hominoid personality and subjective well-being. J Comp Psychol 125:72–83Google Scholar
  181. Weiss JM, West CH, Emery MS et al. (2008) Rats selectively-bred for behavior related to affective disorders: proclivity for intake of alcohol and drugs of abuse, and measures of brain monoamines. Biochem Pharmacol 75:134–159PubMedGoogle Scholar
  182. Westergaard GC, Izard MK, Drake JH et al. (1999a) Rhesus macaque (Macaca mulatta) group formation and housing: Wounding and reproduction in a specific pathogen free (SPF) colony. Am J Primatol 49:339–347PubMedGoogle Scholar
  183. Westergaard GC, Mehlman PT, Shoaf SE et al. (1999b) CSF 5-HIAA and aggression in female macaque monkeys: Species and interindividual differences. Psychopharmacology 146:440–446PubMedGoogle Scholar
  184. Wiener SG, Bayart F, Faull KF et al. (1990) Behavioral and physiological responses to maternal separation in squirrel monkeys (Saimiri sciureus). Behav Neurosci 104:108–115PubMedGoogle Scholar
  185. Zajicek KB, Higley JD, Suomi SJ et al. (1997) Rhesus macaques with high CSF 5-HIAA concentrations exhibit early sleep onset. Psychiatry Res 73:15–25PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Stephen J. Suomi
    • 1
    Email author
  • Andrew C. Chaffin
    • 2
  • J. Dee Higley
    • 2
  1. 1.Laboratory of Comparative EthologyNational Institute of Child Health and Human DevelopmentBethesdaUSA
  2. 2.Department of PsychologyBrigham Young UniversityProvoUSA

Personalised recommendations