Impulsivity and Aggression as Personality Traits in Nonhuman Primates

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


Studies of macaques show that aggressiveness, along with its related cousin impulsivity, is trait-like, showing stable interindividual differences across time and situations. Two variations of aggressive temperament have been described: The first, aggressive temperament or overall aggressiveness, is characterized as competitive, marked by competition and a goal to win. While competitive and aggressive, such individuals seldom engage in violence. In competitive interchanges they often emerge as winners, and are typically high in social dominance. A second type of aggressive temperament leads to impulsive and unrestrained violence. This form of aggression has a strong relationship with impulse-control deficits. Evidence suggests that the two different forms of aggressiveness are mediated by differing systems, with competitive aggression mediated by testosterone. Impulsive aggression is mediated, at least in part by deficits in the serotonin system, with clear genetic and environmental underpinnings. These serotonin-impaired macaques show a variety of antisocial-like personality differences, exhibiting social alienation, sociosexual impairments, as well as impulse-control deficits, violence, and premature death, typically due to violent means. A variety of new molecular genetic studies show that the second form of aggressiveness is modulated, at least in part, by genetic  ×  environmental interactions.


Nonhuman Primate Rhesus Macaque Serotonin Transporter Social Dominance Short Allele 
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.


  1. Apter A, van Praag HM, Plutchik R et al. (1990) Interrelationships among anxiety, aggression, impulsivity, and mood: A serotonergically linked cluster? Psychiatry Res 32:191–199PubMedCrossRefGoogle Scholar
  2. Archer J (1991) The influence of testosterone on human aggression. Br J Psychol 82:1–28PubMedCrossRefGoogle Scholar
  3. Barr CS, Newman TK, Becker ML et al. (2003) The utility of the non-human primate; model for studying gene by environment interactions in behavioral research. Genes Brain Behav 2:336–340PubMedCrossRefGoogle Scholar
  4. 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 28:1114–1119PubMedCrossRefGoogle Scholar
  5. 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 61:1146–1152PubMedCrossRefGoogle Scholar
  6. 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 101:12358–12363PubMedCrossRefGoogle Scholar
  7. 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 55:733–738PubMedCrossRefGoogle Scholar
  8. Bastian ML, Sponberg AC, Suomi SJ et al. (2003) Long-term effects of infant rearing condition on the acquisition of dominance rank in juvenile and adult rhesus macaques (Macaca mulatta). Dev Psychobiol 42:44–51PubMedCrossRefGoogle Scholar
  9. Bennett AJ, Lesch KP, Heils A et al. (2002) Early experience and serotonin transporter gene variation interact to influence primate CNS function. Mol Psychiatry 7:118–122PubMedCrossRefGoogle Scholar
  10. Bennett AJ, Tsai T, Pierre PJ et al. (1998) Behavioral response to novel objects varies with CSF monoamine concentrations in rhesus monkeys. Soc Neurosci Abstr 24:954Google Scholar
  11. Berman CM, Ionica CS, Jin-Hua LI (2004) Dominance style among Macaca thibetana on Mt. Huangshan, China. Int J Primatol 25:214–227CrossRefGoogle Scholar
  12. Bernstein IS (1981) Dominance: The baby and the bathwater. Behav Brain Sci 4:419–457CrossRefGoogle Scholar
  13. Bernstein IS, Rose RM, Gordon TP (1977) Behavioural and hormonal responses of male rhesus monkeys introduced to females in the breeding and non-breeding seasons. Anim Behav 25:609–614PubMedCrossRefGoogle Scholar
  14. Bernstein IS, Rose RM, Gordon TP et al. (1979) Agonistic rank, aggression, social context, and testosterone in male pigtailed monkeys. Aggress Behav 5:329–339CrossRefGoogle Scholar
  15. Bertilsson L, Tybring G, Braithwaite R et al. (1982) Urinary excretion of 5-hydroxyindoleacetic acid – no relationship to the level in cerebrospinal fluid. Acta Psychiatr Scand 66:190–198PubMedCrossRefGoogle Scholar
  16. Bolig R, Price CS, O’Neill PL et al. (1992) Subjective assessment of reactivity level and personality traits of rhesus monkeys. Int J Primatol 13:287–306CrossRefGoogle Scholar
  17. Booth A, Shelley G, Mazur A et al. (1989) Testosterone, and winning and losing in human competition. Horm Behav 23:556–571PubMedCrossRefGoogle Scholar
  18. Botchin MB, Kaplan JR, Manuck SB et al. (1993) Low versus high prolactin responders to fenfluramine challenge: Marker of behavioral differences in adult male cynomolgus macaques. Neuropsychopharmacology 9:93–99PubMedCrossRefGoogle Scholar
  19. Brown GL, Ebert MH, Goyer PF et al. (1982a) Aggression, suicide, and serotonin: Relationships to CSF amine metabolites. Am J Psychiatry 139:741–746PubMedGoogle Scholar
  20. Brown GL, Goodwin FK, Ballenger JC et al. (1979) Aggression in humans correlates with cerebrospinal fluid amine metabolites. Psychiatry Res 1:131–139PubMedCrossRefGoogle Scholar
  21. Brown GL, Goodwin FK, Bunney WEJ (1982b) Human aggression and suicide: Their relationship to neuropsychiatric diagnoses and serotonin metabolism. Adv Biochem Psychopharmacol 34:287–307PubMedGoogle Scholar
  22. Buchanan CM, Eccles JS, Becker JB (1992) Are adolescents the victims of raging hormones: Evidence for activational effects of hormones on moods and behavior at adolescence. Psychol Bull 111:62–107PubMedCrossRefGoogle Scholar
  23. 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
  24. Capitanio JP, Abel K, Mendoza SP 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 Behav Immun 22:679–689Google Scholar
  25. Capitanio JP, Widaman KF (2005) Confirmatory factor analysis of personality structure in adult male rhesus monkeys (Macaca mulatta). Am J Primatol 65:289–294PubMedCrossRefGoogle Scholar
  26. Caramaschi D, de Boer SF, Koolhaas JM (2007) Differential role of the 5-HT1A receptor in aggressive and non-aggressive mice: An across-strain comparison. Physiol Behav 90:590–601PubMedCrossRefGoogle Scholar
  27. Caspi A, McClay J, Moffitt TE et al. (2002) Role of genotype in the cycle of violence in maltreated children. Science 297:851–854PubMedCrossRefGoogle Scholar
  28. Caspi A, Sugden D, Moffitt TE et al. (2003) Influence of life stress on depression: Moderation by a polymorphism in the 5-HTT gene. Science 301:386–389PubMedCrossRefGoogle Scholar
  29. Chamberlain B, Ervin FR, Pihl RO et al. (1987) The effect of raising or lowering tryptophan levels on aggression in vervet monkeys. Pharmacol Biochem Behav 28:503–510PubMedCrossRefGoogle Scholar
  30. Chamove AS, Eysenck HJ, Harlow HF (1972) Personality in monkeys: Factor analyses of rhesus social behaviour. Q J Exp Psychol 24:496–504PubMedCrossRefGoogle Scholar
  31. Champoux M, Bennett A, Shannon C et al. (2002) Serotonin transporter gene polymorphism, differential early rearing, and behavior in rhesus monkey neonates. Mol Psychiatry 7:1058–1063PubMedCrossRefGoogle Scholar
  32. Champoux M, Higley JD, Suomi SJ (1997) Behavioral and physiological characteristics of Indian and Chinese-Indian hybrid rhesus macaque infants. Dev Psychobiol 31:49–63PubMedCrossRefGoogle Scholar
  33. 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
  34. Chapais B (1983) Matriline membership and male rhesus reaching high ranks in the natal troop. In: Hinde RA (ed) Primate social relationships: An integrated approach. Sinauer Associates, Inc., SunderlandGoogle Scholar
  35. Chapais B (1986) Why do male and female rhesus monkeys affiliate during the birth season? In: Rawlins RG, Kessler M (eds) The Cayo Santiago macaques. SUNY Press, ChicagoGoogle Scholar
  36. Chapais B (1988) Rank maintenance in female Japanese macaques: Experimental evidence for social dependency. Behaviour 102:41–59CrossRefGoogle Scholar
  37. Christiansen K, Knussmann R (1987a) Androgen levels and components of aggressive behavior in men. Horm Behav 21:170–180PubMedCrossRefGoogle Scholar
  38. Christiansen K, Knussmann R (1987b) Sex hormones and cognitive functioning in men. Neuropsychobiology 18:27–36PubMedCrossRefGoogle Scholar
  39. Cleveland A, Westergaard GC, Trenkle MK et al. (2004) Physiological predictors of reproductive outcome and mother-infant behaviors in captive rhesus macaque females (Macaca mulatta). Neuropsychopharmacology 29:901–910PubMedCrossRefGoogle Scholar
  40. Cloninger CR (1986) A unified biosocial theory of personality and its role in the development of anxiety states. Psychiatr Dev 4:167–226PubMedGoogle Scholar
  41. Critchley HD, Simmons A, Daly EM et al. (2000) Prefrontal and medial temporal correlates of repetitive violence to self and others. Biol Psychiatry 47:928–934PubMedCrossRefGoogle Scholar
  42. Crockett CM, Pope T (1988) Inferring patterns of aggression from red howler monkey injuries. Am J Primatol 15:289–308CrossRefGoogle Scholar
  43. Dabbs JMJ, Frady RL, Carr TS et al. (1987) Saliva testosterone and criminal violence in young adult prison inmates. Psychosom Med 49:174–182PubMedGoogle Scholar
  44. Eaton GG, Resko JA (1974) Plasma testosterone and male dominance in a Japanese macaque (Macaca fuscata) troop compared with repeated measures of testosterone in laboratory males. Horm Behav 5:251–259PubMedCrossRefGoogle Scholar
  45. Eberhart JA, Yodyingyuad U, Keverne EB (1985) Subordination in male talapoin monkeys lowers sexual behaviour in the absence of dominants. Physiol Behav 35:673–677PubMedCrossRefGoogle Scholar
  46. Ehrenkranz J, Bliss E, Sheard MH (1974) Plasma testosterone: Correlation with aggressive behavior and social dominance in man. Psychosom Med 36:469–475PubMedGoogle Scholar
  47. 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
  48. Eysenck SB, Eysenck HJ (1971) A comparative study of criminals and matched controls on three dimensions of personality. Br J Soc Clin Psychol 10:362–366PubMedCrossRefGoogle Scholar
  49. Fairbanks LA, Fontenot MB, Phillips-Conroy JE et al. (1999) CSF monoamines, age and impulsivity in wild grivet monkeys (Cercopithecus aethiops aethiops). Brain Behav Evol 53:305–312PubMedCrossRefGoogle Scholar
  50. Fairbanks LA and Jorgensen MJ (2011) Objective behavioral tests of temperament in nonhuman primates. In: Weiss A, King JE, Murray L (eds) Personality and temperament in nonhuman primates. Springer, New YorkGoogle Scholar
  51. Fairbanks LA, Melega WP, Jorgensen MJ et al. (2001) Social impulsivity inversely associated with CSF 5-HIAA and fluoxetine exposure in vervet monkeys. Neuropsychopharmacology 24:370–378PubMedCrossRefGoogle Scholar
  52. Ferrari PF, Palanza P, Parmigiani S et al. (2005) Serotonin and aggressive behavior in rodents and nonhuman primates: Predispositions and plasticity. Eur J Pharmacol 526:259–273PubMedCrossRefGoogle Scholar
  53. Gibbs RA, Rogers J, Katze MG et al. (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science 316:222–234PubMedCrossRefGoogle Scholar
  54. Gill K, Amit Z (1989) Serotonin uptake blockers and voluntary alcohol consumption. A review of recent studies. Recent Dev Alcohol 7:225–248PubMedGoogle Scholar
  55. Gleeson S, Ahlers ST, Mansbach RS et al. (1989) Behavioral studies with anxiolytic drugs. VI. Effects on punished responding of drugs interacting with serotonin receptor subtypes. J Pharmacol Exp Ther 250:809–817PubMedGoogle Scholar
  56. Gordon TP, Bernstein IS, Rose RM (1978) Social and seasonal influences on testosterone secretion in the male rhesus monkey. Physiol Behav 21:623–637PubMedCrossRefGoogle Scholar
  57. Gordon TP, Rose RM, Bernstein IS (1976) Seasonal rhythm in plasma testosterone levels in the rhesus monkey (Macaca mulatta): A three year study. Horm Behav 7:229–243PubMedCrossRefGoogle Scholar
  58. Harlow HF (2008) The monkey as a psychological subject. Integr Psychol Behav Sci 42:336–347PubMedCrossRefGoogle Scholar
  59. Harris RA, Rogers J, Milosavljevic A (2007) Human-specific changes of genome structure detected by genomic triangulation. Science 316:235–237PubMedCrossRefGoogle Scholar
  60. Higley JD (2003) Aggression in Old World primates: Causes, cures, and functions. In: Maestripieri D (ed) Primate psychology. The mind and behavior of human and nonhuman primates. Harvard University Press, CambridgeGoogle Scholar
  61. Higley JD, Barr CS (2008) Neurochemistry and behavior. In: Burbacher TM, Sackett GP, Grant KS (eds) Nonhuman primate models of children’s health and developmental disabilities. Academic, New YorkCrossRefGoogle Scholar
  62. Higley JD, Hasert MF, Dodson A et al. (1992a) Treatment of excessive alcohol consumption using the serotonin reuptake inhibitor Sertraline in a nonhuman primate model of alcohol abuse. Paper presented at the meeting of the Research Society on Alcoholism, San Diego, June 13–18Google Scholar
  63. Higley JD, Hasert MF, Suomi SJ et al. (1998) The serotonin reuptake inhibitor sertraline reduces excessive alcohol consumption in nonhuman primates: Effect of stress. Neuropsychopharma­cology 18:431–443PubMedCrossRefGoogle Scholar
  64. Higley JD, King ST, Hasert MF et al. (1996a) Stability of interindividual differences in serotonin function and its relationship to severe aggression and competent social behavior in rhesus macaque females. Neuropsychopharmacology 14:67–76PubMedCrossRefGoogle Scholar
  65. 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
  66. Higley JD, Mehlman PT, Higley SB et al. (1996b) Excessive mortality in young free-ranging male nonhuman primates with low cerebrospinal fluid 5-hydroxyindoleacetic acid concentrations. Arch Gen Psychiatry 53:537–543PubMedCrossRefGoogle Scholar
  67. Higley JD, Mehlman PT, Poland RE et al. (1996c) CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors. Biol Psychiatry 40:1067–1082PubMedCrossRefGoogle Scholar
  68. 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 49:436–441PubMedCrossRefGoogle Scholar
  69. Higley JD, Suomi SJ (1989) Temperamental reactivity in non-human primates. In: Kohnstamm GA, Bates JE, Rothbart MK (eds) Temperament in childhood. Wiley, New YorkGoogle Scholar
  70. Higley JD, Suomi SJ (1996) Effect of reactivity and social competence on individual responses to severe stress in children: Investigations using nonhuman primates. In: Pfeffer CR (ed) Intense stress and mental disturbance in children. American Psychiatric Press, Inc., WashingtonGoogle Scholar
  71. Higley JD, Suomi SJ, 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 103:551–556CrossRefGoogle Scholar
  72. Higley JD, Suomi SJ, Linnoila M (1992c) A longitudinal assessment of CSF monoamine metabolite and plasma cortisol concentrations in young rhesus monkeys. Biol Psychiatry 32:127–145PubMedCrossRefGoogle Scholar
  73. Higley JD, Suomi SJ, Linnoila M (1996d) 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 20:643–650PubMedCrossRefGoogle Scholar
  74. Higley JD, Suomi SJ, Linnoila M (1996e) 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 20:629–642PubMedCrossRefGoogle Scholar
  75. 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 50:615–623PubMedCrossRefGoogle Scholar
  76. Hirsch RM, Higley JD, Suomi SJ (1986) Growing-up without adults: The effect of peer-only rearing on daily behaviors in rhesus monkeys. Paper presented at the meeting of the International Society for Developmental Psychobiology, Annapolis, MDGoogle Scholar
  77. Howell S, Westergaard G, Hoos B et al. (2007) Serotonergic influences on life-history outcomes in free-ranging male rhesus macaques. Am J Primatol 69:851–865PubMedCrossRefGoogle Scholar
  78. Izquierdo A, Newman TK, Higley JD et al. (2007) Genetic modulation of cognitive flexibility and socioemotional behavior in rhesus monkeys. Proc Natl Acad Sci USA 104:14128–14133PubMedCrossRefGoogle Scholar
  79. 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 93:807–819PubMedCrossRefGoogle Scholar
  80. 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
  81. Kaufman JH (1967) Social relations of adult males in a free-ranging band of rhesus monkeys. In: Altmann SA (ed) Social communication among primates. University of Chicago Press, ChicagoGoogle Scholar
  82. Keverne EB, Eberhart JA, Meller RE (1983) Plasma testosterone, sexual and aggressive behavior in social groups of talapoin monkeys. In: Steklis HD, King AS (eds) Hormones, drugs and social behavior in primates. Spectrum, New YorkGoogle Scholar
  83. 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 2:175–189PubMedCrossRefGoogle Scholar
  84. Kruesi MJ, Rapoport JL, Hamburger S et al. (1990) Cerebrospinal fluid monoamine metabolites, aggression, and impulsivity in disruptive behavior disorders of children and adolescents. Arch Gen Psychiatry 47:419–426PubMedCrossRefGoogle Scholar
  85. Kuester J, Paul A (1992) Influence of male competition and female mate choice on male mating success in Barbary macaques (Macaca sylvanus). Behaviour 120:192–217CrossRefGoogle Scholar
  86. Kyes RC, Botchin MB, Kaplan JR et al. (1995) Aggression and brain serotonergic responsivity: Response to slides in male macaques. Physiol Behav 57:205–208PubMedCrossRefGoogle Scholar
  87. 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 17:1127–1136PubMedCrossRefGoogle Scholar
  88. Lesch KP (2007) Linking emotion to the social brain. The role of the serotonin transporter in human social behaviour. EMBO Rep 8 Spec No:S24–S29Google Scholar
  89. Lidberg L, Tuck JR, Åsberg M et al. (1985) Homicide, suicide and CSF 5-HIAA. Acta Psychiatr Scand 71:230–236PubMedCrossRefGoogle Scholar
  90. Limson R, Goldman D, Roy A et al. (1991) Personality and cerebrospinal fluid monoamine metabolites in alcoholics and controls. Arch Gen Psychiatry 48:437–441PubMedCrossRefGoogle Scholar
  91. Lindman R, Järvinen P, Vidjeskog J (1987) Verbal interactions of aggressively and nonaggressively predisposed males in a drinking situation. Aggress Behav 13:187–196CrossRefGoogle Scholar
  92. Linnoila M, Virkkunen M, George T et al. (1993) Impulse control disorders. Int Clin Psycho­pharmacol 8, Supplement 1:53–56PubMedCrossRefGoogle Scholar
  93. Linnoila M, Virkkunen M, Scheinin M et al. (1983) Low cerebrospinal fluid 5-hydroxyindoleacetic acid concentration differentiates impulsive from nonimpulsive violent behavior. Life Sci 33:2609–2614PubMedCrossRefGoogle Scholar
  94. Linsky AS, Colby JP, Jr., Straus MA (1986) Drinking norms and alcohol-related problems in the United States. J Stud Alcohol 47:384–393PubMedGoogle Scholar
  95. Lorenz JG, Long JC, Linnoila M et al. (2006) Genetic and other contributions to alcohol intake in rhesus macaques (Macaca mulatta). Alcohol Clin Exp Res 30:389–398PubMedCrossRefGoogle Scholar
  96. Mandell W, Eaton WW, Anthony JC et al. (1992) Alcoholism and occupations: A review and analysis of 104 occupations. Alcohol Clin Exp Res 16:734–746PubMedCrossRefGoogle Scholar
  97. Manuck SB, Flory JD, Ferrell RE et al. (2000) A regulatory polymorphism of the monoamine oxidase-A gene may be associated with variability in aggression, impulsivity, and central nervous system serotonergic responsivity. Psychiatry Res 95:9–23PubMedCrossRefGoogle Scholar
  98. Manuck SB, Kaplan JR, Rymeski BA et al. (2003) Approach to a social stranger is associated with low central nervous system serotonergic responsivity in female cynomolgus monkeys (Macaca fascicularis). Am J Primatol 61:187–194PubMedCrossRefGoogle Scholar
  99. Martensz ND, Vellucci SV, Fuller LM et al. (1987) Relation between aggressive behaviour and circadian rhythms in cortisol and testosterone in social groups of talapoin monkeys. J Endocrinol 115:107–120PubMedCrossRefGoogle Scholar
  100. Mattsson A, Schalling D, Olweus D et al. (1980) Plasma testosterone, aggressive behavior, and personality dimensions in young male delinquents. J Am Acad Child Psychiatry 19:476–490PubMedCrossRefGoogle Scholar
  101. Mazur A (1983) Hormones, aggression, and dominance in humans. In: Svare BB (ed) Hormones and aggressive behavior. Plenum Press, New YorkCrossRefGoogle Scholar
  102. McBride WJ, Murphy JM, Lumeng L et al. (1989) Serotonin and ethanol preference. Recent Dev Alcohol 7:187–209PubMedGoogle Scholar
  103. 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 55:538–547PubMedCrossRefGoogle Scholar
  104. McGuire MT, Raleigh MJ, Pollack DB (1994) Personality factors in vervet monkeys: The effects of sex, age, social status, and group composition. Am J Primatol 33:1–13CrossRefGoogle Scholar
  105. Mehlman PT, Higley JD, Faucher I et al. (1994) Low CSF 5-HIAA concentrations and severe aggression and impaired impulse control in nonhuman primates. Am J Psychiatry 151:1485–1491PubMedGoogle Scholar
  106. Mehlman PT, Higley JD, 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 152:907–913PubMedGoogle Scholar
  107. Mehlman PT, Higley JD, Fernald BJ et al. (1997) CSF 5-HIAA, testosterone, and sociosexual behaviors in free-ranging male rhesus macaques in the mating season. Psychiatry Res 72:89–102PubMedCrossRefGoogle Scholar
  108. Mehlman PT, Westergaard GC, Hoos BJ et al. (2000) CSF 5-HIAA and nighttime activity in free-ranging primates. Neuropsychopharmacology 22:210–218PubMedCrossRefGoogle Scholar
  109. Miczek KA, Donat P (1990) Brain 5-HT system and inhibition of aggressive behavior. In: Archer T, Bevan P, Cools A (eds) Behavioral pharmacology of 5-HT. Lawrence Erlbaum Associates, Inc., HillsdaleGoogle Scholar
  110. Miczek KA, Mos J, Olivier B (1989) Brain 5-HT and inhibition of aggressive behavior in animals: 5-HIAA and receptor subtypes. Psychopharmacol Bull 25:399–403PubMedGoogle Scholar
  111. Miller-Butterworth CM, Kaplan JR, Barmada MM et al. (2007) The serotonin transporter: Sequence variation in Macaca fascicularis and its relationship to dominance. Behav Genet 37:678–696PubMedCrossRefGoogle Scholar
  112. Mischel W (1968) Personality and assessment. Wiley, New YorkGoogle Scholar
  113. Namboodiri MA, Sugden D, Klein DC et al. (1985) Serum melatonin and pineal indoleamine metabolism in a species with a small day/night N-acetyltransferase rhythm. Comp Biochem Physiol B Comp Biochem 80:731–736CrossRefGoogle Scholar
  114. Newman ME, Shapira B, Lerer B (1998) Evaluation of central serotonergic function in affective and related disorders by the fenfluramine challenge test: A critical review. Int J Neuropsychopharmacol 1:49–69PubMedCrossRefGoogle Scholar
  115. 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 57:167–172PubMedCrossRefGoogle Scholar
  116. Nikulina EM, Avgustinovich DF, Popova NK (1992) Role of 5HT1A receptors in a variety of kinds of aggressive behavior in wild rats and counterparts selected for low defensiveness to man. Aggress Behav 18:357–364CrossRefGoogle Scholar
  117. Olivier B, Mos J (1990) Serenics, serotonin and aggression. Prog Clin Biol Res 361:203–230PubMedGoogle Scholar
  118. Olivier B, Mos J, Tulp M et al. (1990) Modulatory action of serotonin in aggressive behavior. In: Archer T, Bevan P, Cools A (eds) Behavioral pharmacology of 5-HT. Lawrence Erlbaum Associates, Inc., HillsdaleGoogle Scholar
  119. Olweus D, Mattsson A, Schalling D et al. (1980) Testosterone, aggression, physical, and personality dimensions in normal adolescent males. Psychosom Med 42:253–269PubMedGoogle Scholar
  120. Olweus D, Mattsson A, Schalling D et al. (1988) Circulating testosterone levels and aggression in adolescent males: A causal analysis. Psychosom Med 50:261–272PubMedGoogle Scholar
  121. Packer C (1979) Male dominance and reproductive activity in Papio anubis. Anim Behav 27:37–45PubMedCrossRefGoogle Scholar
  122. Paul A (1989) Determinants of male mating success in a large group of Barbary macaques (Macaca sylvanus) at Affenberg Salem. Primates 30:344–349CrossRefGoogle Scholar
  123. Popova NK (2006) From genes to aggressive behavior: The role of serotonergic system. Bioessays 28:495–503PubMedCrossRefGoogle Scholar
  124. 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 17:207–213CrossRefGoogle Scholar
  125. 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 40:751–756PubMedCrossRefGoogle Scholar
  126. Raleigh MJ, Brammer GL, McGuire MT (1983) Male dominance, serotonergic systems, and the behavioral and physiological effects of drugs in vervet monkeys (Cercopithecus aethiops sabaeus). In: Miczek KA (ed) Ethopharmacology: Primate models of neuropsychiatric disorders. Alan R. Liss, New YorkGoogle Scholar
  127. Raleigh MJ, Brammer GL, McGuire MT et al. (1992) Individual differences in basal cisternal cerebrospinal fluid 5-HIAA and HVA in monkeys. The effects of gender, age, physical characteristics, and matrilineal influences. Neuropsychopharmacology 7:295–304PubMedGoogle Scholar
  128. Raleigh MJ, Brammer GL, McGuire MT et al. (1985) Dominant social status facilitates the behavioral effects of serotonergic agonists. Brain Res 348:274–282PubMedCrossRefGoogle Scholar
  129. Raleigh MJ, Brammer GL, Ritvo ER et al. (1986) Effects of chronic fenfluramine on blood serotonin, cerebrospinal fluid metabolites, and behavior in monkeys. Psychopharmacology 90:503–508CrossRefGoogle Scholar
  130. Raleigh MJ, Brammer GL, Yuwiler A et al. (1980) Serotonergic influences on the social behavior of vervet monkeys (Cercopithecus aethiops sabaeus). Exp Neurol 68:322–334PubMedCrossRefGoogle Scholar
  131. Raleigh MJ, McGuire MT (1986) Animal analogues of ostracism: Biological mechanisms and social consequences. Ethology and Sociobiology 7:53–66CrossRefGoogle Scholar
  132. Raleigh MJ, McGuire MT (1990) Social influences on endocrine function in male vervet monkeys. In: Ziegler TE, Bercovitch FB (eds) Socioendocrinology of primate reproduction. Wiley-Liss, New YorkGoogle Scholar
  133. Raleigh MJ, McGuire MT (1991) Bidirectional relationships between tryptophan and social behavior in vervet monkeys. Adv Exp Med Biol 294:289–298PubMedCrossRefGoogle Scholar
  134. Raleigh MJ, McGuire MT (1994) Serotonin, aggression, and violence in vervet monkeys. In: Masters RD, McGuire MT (eds) The neurotransmitter revolution. Southern Illinois University Press, CarbondaleGoogle Scholar
  135. Raleigh MJ, McGuire MT, Brammer GL (1989) Subjective assessment of behavioral style: Links to overt behavior and physiology in vervet monkeys. Am J Primatol 18:161–162Google Scholar
  136. Raleigh MJ, McGuire MT, Brammer GL et al. (1991) Serotonergic mechanisms promote dominance acquisition in adult male vervet monkeys. Brain Res 559:181–190PubMedCrossRefGoogle Scholar
  137. Rejeski WJ, Brubaker PH, Herb RA et al. (1988) The role of anabolic steroids on baseline and stress heart rate in cynomolgus monkeys. Health Psychol 7:299–307PubMedCrossRefGoogle Scholar
  138. Rejeski WJ, Gregg E, Kaplan JR et al. (1990) Anabolic–androgenic steroids: Effects on social behavior and baseline heart rate. Health Psychol 9:774–791PubMedCrossRefGoogle Scholar
  139. Riddle MA, Anderson GM, McIntosh S et al. (1986) Cerebrospinal fluid monoamine precursor and metabolite levels in children treated for leukemia: Age and sex effects and individual variability. Biol Psychiatry 21:69–83PubMedCrossRefGoogle Scholar
  140. Rose RM, Bernstein IS, Gordon TP (1975) Consequences of social conflict on plasma testosterone levels in rhesus monkeys. Psychosom Med 37:50–61PubMedGoogle Scholar
  141. Rose RM, Gordon TP, Bernstein IS (1972) Plasma testosterone levels in the male rhesus: Influences of sexual and social stimuli. Science 178:643–645PubMedCrossRefGoogle Scholar
  142. Rose RM, Gordon TP, Bernstein IS (1978) Diurnal variation in plasma testosterone and cortisol in rhesus monkeys living in social groups. J Endocrinol 76:67–74PubMedCrossRefGoogle Scholar
  143. Rose RM, Holaday JW, Bernstein IS (1971) Plasma testosterone, dominance rank and aggressive behaviour in male rhesus monkeys. Nature 231:366–368PubMedCrossRefGoogle Scholar
  144. Roy A, Virkkunen M, Linnoila M (1988) Monoamines, glucose metabolism, aggression towards self and others. Int J Neurosci 41:261–264PubMedCrossRefGoogle Scholar
  145. Sapolsky RM (1983) Individual differences in cortisol secretory patterns in the wild baboon: Role of negative feedback sensitivity. Endocrinology 113:2263–2267PubMedCrossRefGoogle Scholar
  146. Sapolsky RM (1992) Stress, the aging brain, and the mechanisms of neuron death. MIT Press, CambridgeGoogle Scholar
  147. Scaramella TJ, Brown WA (1978) Serum testosterone and aggressiveness in hockey players. Psychosom Med 40:262–265PubMedGoogle Scholar
  148. 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 162:1658–1664PubMedCrossRefGoogle Scholar
  149. Shively CA, Fontenot MB, Kaplan JR (1995) Social status, behavior, and central serotonergic responsivity in female cynomolgus monkeys. Am J Primatol 37:333–340CrossRefGoogle Scholar
  150. Smuts BB (1987) Gender, aggression and influence. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, ChicagoGoogle Scholar
  151. Soubrié P (1986) Reconciling the role of central serotonin neurons in human and animal behavior. Behav Brain Sci 9:319–364CrossRefGoogle Scholar
  152. Steklis HD, Brammer GL, Raleigh MJ et al. (1985) Serum testosterone, male dominance, and aggression in captive groups of vervet monkeys (Cercopithecus aethiops sabaeus). Horm Behav 19:154–163PubMedCrossRefGoogle Scholar
  153. Suomi SJ (1982) Abnormal behavior and primate models of psychopathology. In: Fobes JL, King JE (eds) Primate behavior. Academic, New YorkGoogle Scholar
  154. Suomi SJ (2006) Risk, resilience, and gene × environment interactions in rhesus monkeys. Ann N Y Acad Sci 1994:52–62CrossRefGoogle Scholar
  155. Suomi SJ, Ripp C (1983) A history of mother-less mother monkey mothering at the university of wisconsin primate laboratory. In: Reite M, Caine N (eds) Child abuse: The nonhuman primate data. Alan R. Liss, New YorkGoogle Scholar
  156. Träskman-Bendz L, Åsberg M, Bertilsson L et al. (1984) CSF monoamine metabolites of depressed patients during illness and after recovery. Acta Psychiatr Scand 69(Supplementum):333–342Google Scholar
  157. Trefilov A, Berard J, Krawczak M et al. (2000) Natal dispersal in rhesus macaques is related to serotonin transporter gene promoter variation. Behav Genet 30:295–301PubMedCrossRefGoogle Scholar
  158. Virkkunen M, De Jong J, Bartko J et al. (1989) Relationship of psychobiological variables to recidivism in violent offenders and impulsive fire setters. A follow-up study. Arch Gen Psychiatry 46:600–603PubMedCrossRefGoogle Scholar
  159. Virkkunen M, Nuutila A, Goodwin FK et al. (1987) Cerebrospinal fluid monoamine metabolite levels in male arsonists. Arch Gen Psychiatry 44:241–217PubMedCrossRefGoogle Scholar
  160. Walters JR, Seyfarth RM (1987) Conflict and cooperation. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, ChicagoGoogle Scholar
  161. Wendland JR, Hampe M, Newman TK et al. (2006a) Structural variation of the monoamine oxidase A gene promoter repeat polymorphism in nonhuman primates. Genes Brain Behav 5:40–45CrossRefGoogle Scholar
  162. Wendland JR, Lesch KP, Newman TK et al. (2006b) Differential functional variability of serotonin transporter and monoamine oxidase A genes in macaque species displaying contrasting levels of aggression-related behavior. Behav Genet 36:163–172PubMedCrossRefGoogle Scholar
  163. Westergaard GC, Cleveland A, Trenkle MK et al. (2003a) CSF 5-HIAA concentration as an early screening tool for predicting significant life history outcomes in female specific-pathogen-free (SPF) rhesus macaques (Macaca mulatta) maintained in captive breeding groups. J Med Primatol 32:95–104PubMedCrossRefGoogle Scholar
  164. 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 49:339–347PubMedCrossRefGoogle Scholar
  165. Westergaard GC, Suomi SJ, Chavanne TJ et al. (2003b) Physiological correlates of aggression and impulsivity in free-ranging female primates. Neuropsychopharmacology 28:1045–1055PubMedGoogle Scholar
  166. Westergaard GC, Suomi SJ, Higley JD et al. (1999b) CSF 5-HIAA and aggression in female macaque monkeys: Species and interindividual differences. Psychopharmacology 146:440–446CrossRefGoogle Scholar
  167. Wickings EJ, Dixson AF (1992) Testicular function, secondary sexual development, and social status in male mandrills (Mandrillus sphinx). Physiol Behav 52:909–916PubMedCrossRefGoogle Scholar
  168. Woermann FG, van Elst LT, Koepp MJ et al. (2000) Reduction of frontal neocortical grey matter associated with affective aggression in patients with temporal lobe epilepsy: an objective voxel by voxel analysis of automatically segmented MRI. J Neurol Neurosurg Psychiatry 68:162–169PubMedCrossRefGoogle Scholar
  169. Yodyingyuad U, Eberhart JA, Keverne EB (1982) Effects of rank and novel females on behaviour and hormones in male talapoin monkeys. Physiol Behav 28:995–1005PubMedCrossRefGoogle Scholar
  170. Zajicek KB, Higley JD, Suomi SJ et al. (1997) Rhesus macaques with high CSF 5-HIAA concentrations exhibit early sleep onset. Psychiatry Res 73:15–25PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

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

Personalised recommendations