Neurobiological Mechanisms for Impulsive-Aggression: The Role of MAOA

  • Hayley M. Dorfman
  • Andreas Meyer-Lindenberg
  • Joshua W. Buckholtz
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 17)

Abstract

Aggression may be present across a large part of the spectrum of psychopathology, and underlies costly criminal antisocial behaviors. Human aggression is a complex and underspecified construct, confounding scientific discovery. Nevertheless, some biologically tractable subtypes are apparent, and one in particular—impulsive (reactive) aggression—appears to account for many facets of aggression-related dysfunction in psychiatric illness. Impulsive-aggression is significantly heritable, suggesting genetic transmission. However, the specific neurobiological mechanisms that mediate genetic risk for impulsive-aggression remain unclear. Here, we review extant data on the genetics and neurobiology of individual differences in impulsive-aggression, with particular attention to the role of genetic variation in Monoamine Oxidase A (MAOA) and its impact on serotonergic signaling within corticolimbic circuitry.

Keywords

Aggression Violence Corticolimbic Amygdala Genetic MAOA Prefrontal 

References

  1. af Klinteberg B, Schalling D, Edman G, Oreland L, Asberg M (1987) Personality correlates of platelet monoamine oxidase (MAO) activity in female and male subjects. Neuropsychobiology 18:89–96Google Scholar
  2. Alia-Klein N et al (2008) Brain monoamine oxidase A activity predicts trait aggression. J Neurosci 28:5099–5104PubMedCentralPubMedGoogle Scholar
  3. Alia-Klein N et al (2011) Gene x disease interaction on orbitofrontal gray matter in cocaine addiction. Arch Gen Psychiatry 68:283–294PubMedCentralPubMedGoogle Scholar
  4. Amaral DG, Price JL (1984) Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 230:465–496PubMedGoogle Scholar
  5. Anderson SW, Bechara A, Damasio H, Tranel D, Damasio AR (1999) Impairment of social and moral behavior related to early damage in human prefrontal cortex. Nat Neurosci 2:1032–1037PubMedGoogle Scholar
  6. Ansorge MS, Hen R, Gingrich JA (2007) Neurodevelopmental origins of depressive disorders. Curr Opin Pharmacol 7:8–17PubMedGoogle Scholar
  7. Ansorge MS, Zhou M, Lira A, Hen R, Gingrich JA (2004) Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science 306:879–881PubMedGoogle Scholar
  8. Arai R et al (2002) Differential subcellular location of mitochondria in rat serotonergic neurons depends on the presence and the absence of monoamine oxidase type B. Neuroscience 114:825–835PubMedGoogle Scholar
  9. Baker LA, Jacobson KC, Raine A, Lozano DI, Bezdjian S (2007) Genetic and environmental bases of childhood antisocial behavior: a multi-informant twin study. J Abnorm Psychol 116:219–235PubMedCentralPubMedGoogle Scholar
  10. Baker LA, Raine A, Liu J, Jacobson KC (2008) Differential genetic and environmental influences on reactive and proactive aggression in children. J Abnorm Child Psychol 36:1265–1278PubMedCentralPubMedGoogle Scholar
  11. Balciuniene J, Emilsson L, Oreland L, Pettersson U, Jazin E (2002) Investigation of the functional effect of monoamine oxidase polymorphisms in human brain. Hum Genet 110:1–7PubMedGoogle Scholar
  12. Baltic S (2011) Crime in the United States 2011—Google booksGoogle Scholar
  13. Beitchman JH, Mik HM, Ehtesham S, Douglas L, Kennedy JL (2004) MAOA and persistent, pervasive childhood aggression. Mol Psychiatry 9:546–547PubMedGoogle Scholar
  14. Belfrage H, Lidberg L, Oreland L (1992) Platelet monoamine oxidase activity in mentally disordered violent offenders. Acta Psychiatr Scand 85:218–221PubMedGoogle Scholar
  15. Best M, Williams JM, Coccaro EF (2002) Evidence for a dysfunctional prefrontal circuit in patients with an impulsive aggressive disorder. Proc Natl Acad Sci USA 99:8448–8453PubMedCentralPubMedGoogle Scholar
  16. Blair RJ, Cipolotti L (2000) Impaired social response reversal. A case of ‘acquired sociopathy’. Brain 123(Pt 6):1122–1141PubMedGoogle Scholar
  17. Bortolato M et al (2011) Social deficits and perseverative behaviors, but not overt aggression, in MAO-A hypomorphic mice. Neuropsychopharmacology 36:2674–2688PubMedCentralPubMedGoogle Scholar
  18. Brunner HG et al (1993b) X-linked borderline mental retardation with prominent behavioral disturbance: phenotype, genetic localization, and evidence for disturbed monoamine metabolism. Am J Hum Genet 52:1032–1039PubMedCentralPubMedGoogle Scholar
  19. Brunner HG, Nelen M, Breakefield XO, Ropers HH, van Oost BA (1993a) Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science 262:578–580PubMedGoogle Scholar
  20. Buckholtz JW, Meyer-Lindenberg A (2008) MAOA and the neurogenetic architecture of human aggression. Trends Neurosci 31:120–129PubMedGoogle Scholar
  21. Buckholtz JW, Meyer-Lindenberg A (2012) Psychopathology and the human: toward a transdiagnostic model of risk for mental illness. Neuron 74:990–1004PubMedGoogle Scholar
  22. Butter CM, Snyder DR (1972) Alterations in aversive and aggressive behaviors following orbital frontal lesions in rhesus monkeys. Acta Neurobiol Exp (Wars) 32:525–565Google Scholar
  23. Button TMM, Scourfield J, Martin N, McGuffin P (2004) Do aggressive and non-aggressive antisocial behaviors in adolescents result from the same genetic and environmental effects? Am J Med Genet B Neuropsychiatr Genet 129B:59–63PubMedGoogle Scholar
  24. Carmichael ST, Price JL (1995) Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 363:615–641PubMedGoogle Scholar
  25. Carmichael ST, Price JL (1996) Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 371:179–207PubMedGoogle Scholar
  26. Cases O et al (1995) Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 268:1763–1766PubMedCentralPubMedGoogle Scholar
  27. Cases O et al (1996) Lack of barrels in the somatosensory cortex of monoamine oxidase A-deficient mice: role of a serotonin excess during the critical period. Neuron 16:297–307PubMedGoogle Scholar
  28. Caspi A et al (2002) Role of genotype in the cycle of violence in maltreated children. Science 297:851–854PubMedGoogle Scholar
  29. Cavada C, Compañy T, Tejedor J, Cruz-Rizzolo RJ, Reinoso-Suárez F (2000) The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb Cortex 10:220–242PubMedGoogle Scholar
  30. Cerasa A et al (2010) Morphological correlates of MAO A VNTR polymorphism: new evidence from cortical thickness measurement. Behav Brain Res 211:118–124PubMedGoogle Scholar
  31. Cirulli ET, Goldstein DB (2007) In vitro assays fail to predict in vivo effects of regulatory polymorphisms. Hum Mol Genet 16:1931–1939PubMedGoogle Scholar
  32. Clark L, Manes F (2004) Social and emotional decision-making following frontal lobe injury. Neurocase 10:398–403PubMedGoogle Scholar
  33. Coccaro EF, Kavoussi RJ, Cooper TB, Hauger RL (1997) Central serotonin activity and aggression: inverse relationship with prolactin response to d-fenfluramine, but not CSF 5-HIAA concentration, in human subjects. Am J Psychiatry 154:1430–1435PubMedGoogle Scholar
  34. Coccaro EF, McCloskey MS, Fitzgerald DA, Phan KL (2007) Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biol Psychiatry 62:168–178PubMedGoogle Scholar
  35. Coccaro EF, Sripada CS, Yanowitch RN, Phan KL (2011) Corticolimbic function in impulsive aggressive behavior. Biol Psychiatry 69:1153–1159PubMedGoogle Scholar
  36. Contini V, Marques FZC, Garcia CED, Hutz MH, Bau CHD (2006) MAOA-uVNTR polymorphism in a Brazilian sample: further support for the association with impulsive behaviors and alcohol dependence. Am J Med Genet B Neuropsychiatr Genet 141B:305–308PubMedGoogle Scholar
  37. Dannlowski U et al (2009) Reduced amygdala-prefrontal coupling in major depression: association with MAOA genotype and illness severity. Int J Neuropsychopharmacol 12:11–22PubMedGoogle Scholar
  38. Daruna JH, Kent EW (1976) Comparison of regional serotonin levels and turnover in the brain of naturally high and low aggressive rats. Brain Res 101:489–501PubMedGoogle Scholar
  39. Davis BA, Yu PH, Boulton AA, Wormith JS, Addington D (1983) Correlative relationship between biochemical activity and aggressive behaviour. Prog Neuropsychopharmacol Biol Psychiatry 7:529–535PubMedGoogle Scholar
  40. de Boer SF, Caramaschi D, Natarajan D, Koolhaas JM (2009) The vicious cycle towards violence: focus on the negative feedback mechanisms of brain serotonin neurotransmission. Front Behav Neurosci 3:52PubMedCentralPubMedGoogle Scholar
  41. Derringer J, Krueger RF, Irons DE, Iacono WG (2010) Harsh discipline, childhood sexual assault, and MAOA genotype: an investigation of main and interactive effects on diverse clinical externalizing outcomes. Behav Genet 40:639–648PubMedCentralPubMedGoogle Scholar
  42. Doudet D et al (1995) Cerebral glucose metabolism, CSF 5-HIAA levels, and aggressive behavior in rhesus monkeys. Am J Psychiatry 152:1782–1787PubMedGoogle Scholar
  43. Ducci F et al (2006) A functional polymorphism in the MAOA gene promoter (MAOA-LPR) predicts central dopamine function and body mass index. Mol Psychiatry 11:858–866PubMedGoogle Scholar
  44. Ducci F et al (2008) Interaction between a functional MAOA locus and childhood sexual abuse predicts alcoholism and antisocial personality disorder in adult women. Mol Psychiatry 13:334–347PubMedGoogle Scholar
  45. Edwards AC et al (2010) MAOA-uVNTR and early physical discipline interact to influence delinquent behavior. J Child Psychol Psychiatry 51:679–687PubMedCentralPubMedGoogle Scholar
  46. Eklund J, Alm PO, af Klinteberg B (2005) Monoamine oxidase activity and tri-iodothyronine level in violent offenders with early behavioural problems. Neuropsychobiology 52:122–129Google Scholar
  47. Eley TC, Lichtenstein P, Moffitt TE (2003) A longitudinal behavioral genetic analysis of the etiology of aggressive and nonaggressive antisocial behavior. Dev Psychopathol 15:383–402PubMedGoogle Scholar
  48. Enoch M-A, Steer CD, Newman TK, Gibson N, Goldman D (2010) Early life stress, MAOA, and gene-environment interactions predict behavioral disinhibition in children. Genes Brain Behav 9:65–74PubMedCentralPubMedGoogle Scholar
  49. Fairbanks LA et al (2004) Genetic contributions to social impulsivity and aggressiveness in vervet monkeys. Biol Psychiatry 55:642–647PubMedGoogle Scholar
  50. Fan J, Fossella J, Sommer T, Wu Y, Posner MI (2003) Mapping the genetic variation of executive attention onto brain activity. Proc Natl Acad Sci USA 100:7406–7411PubMedCentralPubMedGoogle Scholar
  51. Farrington DP, Jolliffe D, Loeber R, Stouthamer-Loeber M, Kalb LM (2001) The concentration of offenders in families, and family criminality in the prediction of boys’ delinquency. J Adolesc 24:579–596PubMedGoogle Scholar
  52. Fergusson DM, Boden JM, Horwood LJ, Miller AL, Kennedy MA (2011) MAOA, abuse exposure and antisocial behaviour: 30-year longitudinal study. Br J Psychiatry 198:457–463PubMedCentralPubMedGoogle Scholar
  53. Ferris CF (2005) Vasopressin/oxytocin and aggression. Novartis Found. Symp 268:190–8– discussion 198–200– 242–53Google Scholar
  54. Foley DL et al (2004) Childhood adversity, monoamine oxidase a genotype, and risk for conduct disorder. Arch Gen Psychiatry 61:738–744PubMedGoogle Scholar
  55. Fowler JS et al (1997) Age-related increases in brain monoamine oxidase B in living healthy human subjects. Neurobiol Aging 18:431–435PubMedGoogle Scholar
  56. Frazzetto G et al (2007) Early trauma and increased risk for physical aggression during adulthood: the moderating role of MAOA genotype. PLoS ONE 2:e486PubMedCentralPubMedGoogle Scholar
  57. Gallardo-Pujol D, Andrés-Pueyo A, Maydeu-Olivares A (2013) MAOA genotype, social exclusion and aggression: an experimental test of a gene-environment interaction. Genes Brain Behav 12:140–145PubMedGoogle Scholar
  58. Garpenstrand H, Annas P, Ekblom J, Oreland L, Fredrikson M (2001) Human fear conditioning is related to dopaminergic and serotonergic biological markers. Behav Neurosci 115:358–364PubMedGoogle Scholar
  59. Gelhorn HL et al (2005) Genetic and environmental influences on conduct disorder: symptom, domain and full-scale analyses. J Child Psychol Psychiatry 46:580–591PubMedGoogle Scholar
  60. Gelhorn HL et al (2006) Common and specific genetic influences on aggressive and nonaggressive conduct disorder domains. J Am Acad Child Adolesc Psychiatry 45:570–577PubMedGoogle Scholar
  61. Ghashghaei HT, Barbas H (2002) Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115:1261–1279PubMedGoogle Scholar
  62. Ghashghaei HT, Hilgetag CC, Barbas H (2007) Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. NeuroImage 34:905–923PubMedCentralPubMedGoogle Scholar
  63. Gingrich JA, Ansorge MS, Merker R, Weisstaub N, Zhou M (2003) New lessons from knockout mice: the role of serotonin during development and its possible contribution to the origins of neuropsychiatric disorders. CNS Spectr 8:572–577PubMedGoogle Scholar
  64. Godar SC et al (2010) Maladaptive defensive behaviours in monoamine oxidase A-deficient mice. Int J Neuropsychopharmacol 14:1195–1207PubMedCentralPubMedGoogle Scholar
  65. Good CD (2003) Dosage-sensitive X-linked locus influences the development of amygdala and orbitofrontal cortex, and fear recognition in humans. Brain 126:2431–2446PubMedGoogle Scholar
  66. Goursaud A-PS, Bachevalier J (2007) Social attachment in juvenile monkeys with neonatal lesion of the hippocampus, amygdala and orbital frontal cortex. Behav Brain Res 176:75–93PubMedGoogle Scholar
  67. Grimsby J, Chen K, Wang LJ, Lan NC, Shih JC (1991) Human monoamine oxidase A and B genes exhibit identical exon-intron organizationGoogle Scholar
  68. Gross C, Hen R (2004) Genetic and environmental factors interact to influence anxiety. Neurotox Res 6:493–501PubMedGoogle Scholar
  69. Haberstick BC et al (2013) MAOA genotype, childhood maltreatment, and their interaction in the etiology of adult antisocial behaviors. Biol Psychiatry. doi:10.1016/j.biopsych.2013.03.028 PubMedGoogle Scholar
  70. Heinrichs M, Domes G (2008) Neuropeptides and social behaviour: effects of oxytocin and vasopressin in humans. Prog Brain Res 170:337–350PubMedGoogle Scholar
  71. Huang Y–Y et al (2004) An association between a functional polymorphism in the monoamine oxidase a gene promoter, impulsive traits and early abuse experiences. Neuropsychopharmacology 29:1498–1505PubMedGoogle Scholar
  72. Hudziak JJ et al (2003) Individual differences in aggression: genetic analyses by age, gender, and informant in 3-, 7-, and 10-year-old Dutch twins. Behav Genet 33:575–589PubMedGoogle Scholar
  73. Jacob CP et al (2005) Cluster B personality disorders are associated with allelic variation of monoamine oxidase A activity. Neuropsychopharmacology 30:1711–1718PubMedGoogle Scholar
  74. Jahng JW et al (1997) Localization of monoamine oxidase A and B mRNA in the rat brain by in situ hybridization. Synapse 25:30–36PubMedGoogle Scholar
  75. Jönsson EG et al (2000) A promoter polymorphism in the monoamine oxidase A gene and its relationships to monoamine metabolite concentrations in CSF of healthy volunteers. J Psychiatr Res 34:239–244PubMedGoogle Scholar
  76. Kalin NH et al (2008) The serotonin transporter genotype is associated with intermediate brain phenotypes that depend on the context of eliciting stressor. Mol Psychiatry 13:1021–1027PubMedCentralPubMedGoogle Scholar
  77. Kim-Cohen J et al (2006) MAOA, maltreatment, and gene-environment interaction predicting children’s mental health: new evidence and a meta-analysis. Mol Psychiatry 11:903–913PubMedGoogle Scholar
  78. Kinnally EL et al (2009) Parental care moderates the influence of MAOA-uVNTR genotype and childhood stressors on trait impulsivity and aggression in adult women. Psychiatr Genet 19:126–133PubMedCentralPubMedGoogle Scholar
  79. Krueger RF, South SC (2009) Externalizing disorders: cluster 5 of the proposed meta-structure for DSM-V and ICD-11. Psychol Med 39:2061–2070PubMedGoogle Scholar
  80. Kuepper Y, Grant P, Wielpuetz C, Hennig J (2013) MAOA-uVNTR genotype predicts interindividual differences in experimental aggressiveness as a function of the degree of provocation. Behav Brain Res 247:73–78PubMedGoogle Scholar
  81. Levitt P, Pintar JE, Breakefield XO (1982) Immunocytochemical demonstration of monoamine oxidase B in brain astrocytes and serotonergic neurons. Proc Natl Acad Sci USA 79:6385–6389PubMedCentralPubMedGoogle Scholar
  82. Machado CJ, Bachevalier J (2006) The impact of selective amygdala, orbital frontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta). Behav Neurosci 120:761–786PubMedGoogle Scholar
  83. Manuck SB, Flory JD, Ferrell RE, Mann JJ, Muldoon MF (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 95:9–23PubMedGoogle Scholar
  84. Manuck SB, Flory JD, Muldoon MF, Ferrell RE (2002) Central nervous system serotonergic responsivity and aggressive disposition in men. Physiol Behav 77:705–709PubMedGoogle Scholar
  85. Márquez C et al (2013) Peripuberty stress leads to abnormal aggression, altered amygdala and orbitofrontal reactivity and increased prefrontal MAOA gene expression. Transl Psychiatry 3:e216PubMedCentralPubMedGoogle Scholar
  86. McDermott R, Tingley D, Cowden J, Frazzetto G, Johnson DDP (2009) Monoamine oxidase A gene (MAOA) predicts behavioral aggression following provocation. Proc Nat Acad Sci 106:2118–2123PubMedCentralPubMedGoogle Scholar
  87. Mertins V, Schote AB, Hoffeld W, Griessmair M, Meyer J (2011) Genetic susceptibility for individual cooperation preferences: the role of monoamine oxidase A gene (MAOA) in the voluntary provision of public goods. PLoS ONE 6:e20959PubMedCentralPubMedGoogle Scholar
  88. Meyer-Lindenberg A et al (2006) Neural mechanisms of genetic risk for impulsivity and violence in humans. Proc Natl Acad Sci USA 103:6269–6274PubMedCentralPubMedGoogle Scholar
  89. Meyer-Lindenberg A et al (2009) Genetic variants in AVPR1A linked to autism predict amygdala activation and personality traits in healthy humans. Mol Psychiatry 14:968–975PubMedCentralPubMedGoogle Scholar
  90. Miczek KA, Maxson SC, Fish EW, Faccidomo S (2001) Aggressive behavioral phenotypes in mice. Behav Brain Res 125:167–181PubMedGoogle Scholar
  91. Mukasa H, Nakamura J, Yamada S, Inoue M, Nakazawa Y (1990) Platelet monoamine oxidase activity and personality traits in alcoholics and methamphetamine dependents. Drug Alcohol Depend 26:251–254PubMedGoogle Scholar
  92. Nicotra A, Pierucci F, Parvez H, Senatori O (2004) Monoamine oxidase expression during development and aging. Neurotoxicology 25:155–165PubMedGoogle Scholar
  93. Nilsson KW et al (2006) Role of monoamine oxidase A genotype and psychosocial factors in male adolescent criminal activity. Biol Psychiatry 59:121–127PubMedGoogle Scholar
  94. Nymberg C et al (2013) Neural mechanisms of attention-deficit/hyperactivity disorder symptoms are stratified by MAOA genotype. Biol Psychiatry. doi:10.1016/j.biopsych.2013.03.027 PubMedGoogle Scholar
  95. Ongür D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10:206–219PubMedGoogle Scholar
  96. Parsian A, Cloninger CR, Sinha R, Zhang ZH (2003) Functional variation in promoter region of monoamine oxidase A and subtypes of alcoholism: haplotype analysis. Am J Med Genet B Neuropsychiatr Genet 117B:46–50PubMedGoogle Scholar
  97. Passamonti L et al (2008) Genetically dependent modulation of serotonergic inactivation in the human prefrontal cortex. NeuroImage 40:1264–1273PubMedGoogle Scholar
  98. Perris C, Eisemann M, Knorring von L, Oreland L, Perris H (1984) Personality traits and monoamine oxidase activity in platelets in depressed patients. Neuropsychobiology 12:201–205Google Scholar
  99. Popova NK et al (2001) Behavioral characteristics of mice with genetic knockout of monoamine oxidase type A. Neurosci Behav Physiol 31:597–602PubMedGoogle Scholar
  100. Prochazka H, Anderberg UM, Oreland L, Knorring LV, Agren H (2003) Self-rated aggression related to serum testosterone and platelet MAO activity in female patients with the fibromyalgia syndrome. World J Biol Psychiatry 4:35–41PubMedGoogle Scholar
  101. Raine A et al (1994) Selective reductions in prefrontal glucose metabolism in murderers. Biol Psychiatry 36:365–373PubMedGoogle Scholar
  102. Raine A 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
  103. Raine A, Buchsbaum M, LaCasse L (1997) Brain abnormalities in murderers indicated by positron emission tomography. Biol Psychiatry 42:495–508PubMedGoogle Scholar
  104. Rebsam A, Seif I, Gaspar P (2002) Refinement of thalamocortical arbors and emergence of barrel domains in the primary somatosensory cortex: a study of normal and monoamine oxidase a knock-out mice. J Neurosci 22:8541–8552PubMedGoogle Scholar
  105. Reif A et al (2007) Nature and nurture predispose to violent behavior: serotonergic genes and adverse childhood environment. Neuropsychopharmacology 32:2375–2383PubMedGoogle Scholar
  106. Reti IM et al (2011) Monoamine oxidase A regulates antisocial personality in whites with no history of physical abuse. Compr Psychiatry 52:188–194PubMedCentralPubMedGoogle Scholar
  107. Roiser JP et al (2009) A genetically mediated bias in decision making driven by failure of amygdala control. J Neurosci 29:5985–5991PubMedCentralPubMedGoogle Scholar
  108. Sabol S, Hamer D (1998) A functional polymorphism in the monoamine oxidase A gene promoterGoogle Scholar
  109. Saito T et al (2002) Analysis of monoamine oxidase A (MAOA) promoter polymorphism in Finnish male alcoholics. Psychiatry Res 109:113–119PubMedGoogle Scholar
  110. Salichon N et al (2001) Excessive activation of serotonin (5-HT) 1B receptors disrupts the formation of sensory maps in monoamine oxidase a and 5-ht transporter knock-out mice. J Neurosci 21:884–896PubMedGoogle Scholar
  111. Saura J et al (1996a) Localization of monoamine oxidases in human peripheral tissues. Life Sci 59:1341–1349PubMedGoogle Scholar
  112. Saura J et al (1996b) Molecular neuroanatomy of human monoamine oxidases A and B revealed by quantitative enzyme radioautography and in situ hybridization histochemistry. Neuroscience 70:755–774PubMedGoogle Scholar
  113. Scott AL, Bortolato M, Chen K, Shih JC (2008) Novel monoamine oxidase A knock out mice with human-like spontaneous mutation. NeuroReport 19:739–743PubMedCentralPubMedGoogle Scholar
  114. Shih J, Thompson R (1999) Monoamine oxidase in neuropsychiatry and behavior. Am J Hum Genet 65:593–598PubMedCentralPubMedGoogle Scholar
  115. Shih JC, Chen K (1999) MAO-A and -B gene knock-out mice exhibit distinctly different behavior. Neurobiology (Bp) 7:235–246Google Scholar
  116. Sjöberg RL et al (2008) A non-additive interaction of a functional MAO-A VNTR and testosterone predicts antisocial behavior. Neuropsychopharmacology 33:425–430PubMedCentralPubMedGoogle Scholar
  117. Skondras M, Markianos M, Botsis A, Bistolaki E, Christodoulou G (2004) Platelet monoamine oxidase activity and psychometric correlates in male violent offenders imprisoned for homicide or other violent acts. Eur Arch Psychiatry Clin Neurosci 254:380–386PubMedGoogle Scholar
  118. Stadler C et al (2007) Reduced anterior cingulate activation in aggressive children and adolescents during affective stimulation: association with temperament traits. J Psychiatr Res 41:410–417PubMedGoogle Scholar
  119. Stark P, Fuller RW, Wong DT (1985) The pharmacologic profile of fluoxetine. J Clin Psychiatry 46:7–13PubMedGoogle Scholar
  120. Stefanacci L, Amaral DG (2002) Some observations on cortical inputs to the macaque monkey amygdala: an anterograde tracing study. J Comp Neurol 451:301–323PubMedGoogle Scholar
  121. Sterzer P, Stadler C, Krebs A, Kleinschmidt A, Poustka F (2005) Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder. Biol Psychiatry 57:7–15PubMedGoogle Scholar
  122. Strolin Benedetti M, Dostert P, Tipton KF (1992) Developmental aspects of the monoamine-degrading enzyme monoamine oxidase. Dev Pharmacol Ther 18:191–200PubMedGoogle Scholar
  123. Suomi SJ (2003) Gene-environment interactions and the neurobiology of social conflict. Ann N Y Acad Sci 1008:132–139PubMedGoogle Scholar
  124. Syagailo YV et al (2001) Association analysis of the functional monoamine oxidase A gene promoter polymorphism in psychiatric disorders. Am J Med Genet 105:168–171PubMedGoogle Scholar
  125. Tost H et al (2010) A common allele in the oxytocin receptor gene (OXTR) impacts prosocial temperament and human hypothalamic-limbic structure and function. Proc Nat Acad Sci 107:13936–13941PubMedCentralPubMedGoogle Scholar
  126. Tsang D, Ho KP, Wen HL (1986) Ontogenesis of multiple forms of monoamine oxidase in rat brain regions and liver. Dev Neurosci 8:243–250PubMedGoogle Scholar
  127. Valzelli L, Bernasconi S (1979) Aggressiveness by isolation and brain serotonin turnover changes in different strains of mice. Neuropsychobiology 5:129–135PubMedGoogle Scholar
  128. Valzelli L, Bernasconi S, Dalessandro M (1981b) Effect of tryptophan administration on spontaneous and P-CPA-induced muricidal aggression in laboratory rats. Pharmacol Res Commun 13:891–897PubMedGoogle Scholar
  129. Valzelli L, Garattini S, Bernasconi S, Sala A (1981a) Neurochemical correlates of muricidal behavior in rats. Neuropsychobiology 7:172–178PubMedGoogle Scholar
  130. van Beijsterveldt CEM, Verhulst FC, Molenaar PCM, Boomsma DI (2004) The genetic basis of problem behavior in 5-year-old Dutch twin pairs. Behav Genet 34:229–242PubMedGoogle Scholar
  131. Verdejo-García A et al (2013) Article in press. Drug Alcohol Depend 1–4. doi:10.1016/j.drugalcdep.2013.04.031
  132. Vergnes M, Kempf E (1981) Tryptophan deprivation: effects on mouse-killing and reactivity in the rat. Pharmacol Biochem Behav 14(Suppl 1):19–23PubMedGoogle Scholar
  133. Wakschlag LS et al (2010) Interaction of prenatal exposure to cigarettes and MAOA genotype in pathways to youth antisocial behavior. Mol Psychiatry 15:928–937PubMedCentralPubMedGoogle Scholar
  134. Waters H, Hyder AA, Rajkotia Y, Basu S, Rehwinkel JA (2004) The economic dimensions of interpersonal violence/editorial committee: Hugh Waters…[et al.]Google Scholar
  135. Weder N et al (2013) MAOA genotype, maltreatment, and aggressive behavior: the changing impact of genotype at varying levels of trauma. Biol Psychiatry 65:417–424Google Scholar
  136. Westlund KN, Denney RM, Kochersperger LM, Rose RM, Abell CW (1985) Distinct monoamine oxidase A and B populations in primate brain. Science 230:181–183PubMedGoogle Scholar
  137. Westlund KN, Denney RM, Rose RM, Abell CW (1988) Localization of distinct monoamine oxidase A and monoamine oxidase B cell populations in human brainstem. Neuroscience 25:439–456PubMedGoogle Scholar
  138. Westlund KN, Krakower TJ, Kwan SW, Abell CW (1993) Intracellular distribution of monoamine oxidase A in selected regions of rat and monkey brain and spinal cord. Brain Res 612:221–230PubMedGoogle Scholar
  139. Widom CS, Brzustowicz LM (2006) MAOA and the ‘cycle of violence:’ childhood abuse and neglect, MAOA genotype, and risk for violent and antisocial behavior. BPS 60:684–689Google Scholar
  140. Williams LM et al (2009) A polymorphism of the MAOA gene is associated with emotional brain markers and personality traits on an antisocial index. Neuropsychopharmacology 34:1797–1809PubMedGoogle Scholar
  141. Willoughby J et al (1988) Monoamine oxidase activity and distribution in marmoset brain: implications for MPTP toxicity. Neurosci Lett 90:100–106PubMedGoogle Scholar
  142. Yeh MT, Coccaro EF, Jacobson KC (2010) Multivariate behavior genetic analyses of aggressive behavior subtypes. Behav Genet 40:603–617PubMedCentralPubMedGoogle Scholar
  143. Ziermans T et al (2012) Working memory brain activity and capacity link MAOA polymorphism to aggressive behavior during development. Transl Psychiatry 2:e85PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Hayley M. Dorfman
    • 1
  • Andreas Meyer-Lindenberg
    • 2
  • Joshua W. Buckholtz
    • 1
    • 3
  1. 1.Department of PsychologyHarvard UniversityCambridgeUSA
  2. 2.Central Institute of Mental HealthMannheimGermany
  3. 3.Center for Brain ScienceHarvard UniversityCambridgeUSA

Personalised recommendations