Evidence for a Sex-Dependent MAOA× Childhood Stress Interaction in the Neural Circuitry of Aggression

Cerebral Cortex

Volumn 26, Issue 3, 2016, Pages 904-914

  Holz, Nathalie ^a   Boecker, Regina ^a   Buchmann, Arlette F ^a   Blomeyer, Dorothea ^a   Baumeister, Sarah ^a   Hohmann, Sarah ^a   Jennen Steinmetz, Christine ^b   Wolf, Isabella ^a,b   Rietschel, Marcella ^b   Witt, Stephanie H ^b   Plichta, Michael M ^a   Meyer Lindenberg, Andreas ^a   Schmidt, Martin H ^a   Esser, Gunter ^c   Banaschewski, Tobias ^a   Brandeis, Daniel ^a,d   Laucht, Manfred ^a,c  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b Department of Biostatistics ^*  (Germany)

^c UNIVERSITY OF POTSDAM   (Germany)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Aggression; amygdala; fMRI; life stress; MAOA

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; AMINE OXIDASE (FLAVIN CONTAINING); MONOAMINE OXIDASE A, HUMAN;

ADULT; AGGRESSION; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; CHILD; EARLY LIFE STRESS; EMOTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENOTYPE ENVIRONMENT INTERACTION; HIGH RISK POPULATION; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; MALE; NERVE CELL; NORMAL HUMAN; PRIORITY JOURNAL; PSYCHOLOGIC ASSESSMENT; SEX DIFFERENCE; TASK PERFORMANCE; VARIABLE NUMBER OF TANDEM REPEAT; BRAIN; BRAIN MAPPING; FACIAL RECOGNITION; GENETICS; GENOTYPING TECHNIQUE; GROWTH, DEVELOPMENT AND AGING; MENTAL STRESS; NERVE TRACT; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PRESCHOOL CHILD; SEXUAL DEVELOPMENT;

ADULT; AGGRESSION; BRAIN; BRAIN MAPPING; CHILD; CHILD, PRESCHOOL; FACIAL RECOGNITION; FEMALE; GENOTYPING TECHNIQUES; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MONOAMINE OXIDASE; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL;

EID: 84961282234     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu249     Document Type: Article

References (123)

1. Achenbach TM. 1991a. Manual for the Youth Self-Report and 1991 Profile. Burlington: University of Vermont, Department of Psychiatry.
2. Achenbach TM. 1991b. Young Adult Self Report. Burlington: University of Vermont, Department of Psychiatry.
3. Adamec RE. 1990. Role of the amygdala and medial hypothalamus in spontaneous feline aggression and defense. Aggress Behav. 16:207-222.
4. Adleman NE, Menon V, Blasey CM, White CD, Warsofsky IS, Glover GH, Reiss AL. 2002. A developmental fMRI study of the Stroop color-word task. Neuroimage. 16:61-75.
5. Alia-Klein N, Goldstein RZ, Tomasi D, Woicik PA, Moeller SJ, Williams B, Craig IW, Telang F, Biegon A, Wang GJ, et al. 2009. Neural mechanisms of anger regulation as a function of genetic risk for violence. Emotion. 9:385-396.
6. Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hof P. 2001. The anterior cingulate cortex. The evolution of an interface between emotion and cognition. Ann N Y Acad Sci. 935:107-117.
7. Andersen SL, Tomada A, Vincow ES, Valente E, Polcari A, Teicher MH. 2008. Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. J Neuropsychiatry Clin Neurosci. 20:292-301.
8. Aslund C, Nordquist N, Comasco E, Leppert J, Oreland L, Nilsson KW. 2011. Maltreatment, MAOA, and delinquency: sex differences in gene-environment interaction in a large population-based cohort of adolescents. Behav Genet. 41:262-272.
9. Audero E, Mlinar B, Baccini G, Skachokova ZK, Corradetti R, Gross C. 2013. Suppression of serotonin neuron firing increases aggression in mice. J Neurosci. 33:8678-8688.
10. Baird AA, Silver SH, Veague HB. 2010. Cognitive control reduces sensitivity to relational aggression among adolescent girls. Soc Neurosci. 5:519-532.
11. Baker LM, Williams LM, Korgaonkar MS, Cohen RA, Heaps JM, Paul RH. 2013. Impact of early vs. late childhood early life stress on brain morphometrics. Brain Imaging Behav. 7:196-203.
12. Barratt ES, Felthous AR. 2003. Impulsive versus premeditated aggression: implications for mens rea decisions. Behav Sci Law. 21:619-630.
13. Baumeister S, Hohmann S, Wolf I, Plichta MM, Rechtsteiner S, Zangl M, Ruf M, Holz N, Boecker R, Meyer-Lindenberg A, et al. 2014. Sequential inhibitory control processes assessed through simultaneous EEG-fMRI. Neuroimage. 94:349-359.
14. Berumen LC, Rodriguez A, Miledi R, Garcia-Alcocer G. 2012. Serotonin receptors in hippocampus. ScientificWorldJournal. 2012:823493.
15. Birbaumer N, Veit R, LotzeM, Erb M, Hermann C, GroddW, Flor H. 2005. Deficient fear conditioning in psychopathy: a functional magnetic resonance imaging study. Arch Gen Psychiatry. 62:799-805.
16. Blair RJ. 2013. The neurobiology of psychopathic traits in youths. Nat Rev Neurosci. 14:786-799.
17. Blair RJ. 2010. Neuroimaging of psychopathy and antisocial behavior: a targeted review. Curr Psychiatry Rep. 12:76-82.
18. Blasi G, Goldberg TE, Weickert T, Das S, Kohn P, Zoltick B, Bertolino A, Callicott JH, Weinberger DR, Mattay VS. 2006. Brain regions underlying response inhibition and interference monitoring and suppression. Eur J Neurosci. 23:1658-1664.
19. Bouma EM, Riese H, Doornbos B, Ormel J, Oldehinkel AJ. 2012. Genetically based reducedMAOAand COMTfunctioning is associated with the cortisol stress response: a replication study. Mol Psychiatry. 17:119-121.
20. Brown GL, Ebert MH, Goyer PF, Jimerson DC, Klein WJ, Bunney WE, Goodwin FK. 1982. Aggression, suicide, and serotonin: relationships to CSF amine metabolites. Am J Psychiatry. 139:741-746.
21. Buitelaar JK, Smeets KC, Herpers P, Scheepers F, Glennon J, Rommelse NN. 2013. Conduct disorders. Eur Child Adolesc Psychiatry. 22(Suppl 1):S49-S54.
22. Bush G, Luu P, Posner MI. 2000. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci. 4:215-222.
23. Byrd AL, Manuck SB. 2014. MAOA, childhood maltreatment, and antisocial behavior: meta-analysis of a gene-environment interaction. Biol Psychiatry. 75:9-17.
24. Carrel L, Willard HF. 2005. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature. 434:400-404.
25. Caspi A, McClay J, Moffitt TE, Mill J, Martin J, Craig IW, Taylor A, Poulton R. 2002. Role of genotype in the cycle of violence in maltreated children. Science. 297:851-854.
26. Cicchetti D, Rogosch FA, Sturge-Apple ML. 2007. Interactions of child maltreatment and serotonin transporter and monoamine oxidase A polymorphisms: depressive symptomatology among adolescents from low socioeconomic status backgrounds. Dev Psychopathol. 19:1161-1180.
27. Clemens B, Voß B, Pawliczek C, Mingoia G, Weyer D, Repple J, Eggermann T, Zerres K, Reetz K, Habel U. 2015. Effect of MAOA genotype on resting-state networks in healthy participants. Cereb Cortex. 25:1771-1781.
28. Coccaro EF. 1989. Central serotonin and impulsive aggression. Br J Psychiatry Suppl. 155 (Suppl 8):52-62.
29. Coccaro EF, Astill JL. 1990. Central serotonergic function in parasuicide. Prog Neuropsychopharmacol Biol Psychiatry. 14:663-674.
30. Coccaro EF, McCloskey MS, Fitzgerald DA, Phan KL. 2007. Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biol Psychiatry. 62:168-178.
31. Cunningham MG, Bhattacharyya S, Benes FM. 2002. Amygdalocortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence. J Comp Neurol. 453:116-130.
32. Deakin JF, Pennell I, Upadhyaya AJ, Lofthouse R. 1990. A neuroendocrine study of 5HT function in depression: evidence for biological mechanisms of endogenous and psychosocial causation. Psychopharmacology (Berl). 101:85-92.
33. de Boer SF, Lesourd M, Mocaer E, Koolhaas JM. 1999. Selective antiaggressive effects of alnespirone in resident-intruder test are mediated via 5-hydroxytryptamine1A receptors: a comparative pharmacological study with 8-hydroxy-2-dipropylaminotetralin, ipsapirone, buspirone, eltoprazine, and WAY-100635. J Pharmacol Exp Ther. 288:1125-1133.
34. Deckert J, Catalano M, Syagailo YV, Bosi M, Okladnova O, Di BD, Nothen MM, Maffei P, Franke P, Fritze J, et al. 1999. Excess of high activity monoamine oxidase A gene promoter alleles in female patients with panic disorder. Hum Mol Genet. 8:621-624.
35. Denson TF, Pedersen WC, Ronquillo J, Nandy AS. 2009. The angry brain: neural correlates of anger, angry rumination, and aggressive personality. J Cogn Neurosci. 21:734-744.
36. de Quervain DJ, Kolassa IT, Ackermann S, Aerni A, Boesiger P, Demougin P, Elbert T, Ertl V, Gschwind L, Hadziselimovic N, et al. 2012. PKCalpha is genetically linked to memory capacity in healthy subjects and to risk for posttraumatic stress disorder in genocide survivors. Proc Natl Acad Sci USA. 109:8746-8751.
37. 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. 40:639-648.
38. Devinsky O, Morrell MJ, Vogt BA. 1995. Contributions of anterior cingulate cortex to behaviour. Brain. 118(Pt 1):279-306.
39. Dodge KA. 1991. The structure and function of reactive and proactive aggression. In: Pepler DJ, Rubin KH, editors. The development and treatment of childhood aggression. Hilldale (NJ): Erlbaum. p. 201-218.
40. Domschke K, Tidow N, Kuithan H, Schwarte K, Klauke B, Ambree O, Reif A, Schmidt H, Arolt V, Kersting A, et al. 2012. Monoamine oxidase A gene DNA hypomethylation-A risk factor for panic disorder? Int J Neuropsychopharmacol. 15: 1217-1228.
41. Ducharme S, Hudziak JJ, Botteron KN, Ganjavi H, Lepage C, Collins DL, Albaugh MD, Evans AC, Karama S, Brain Development Cooperative G. 2011. Right anterior cingulate cortical thickness and bilateral striatal volume correlate with child behavior checklist aggressive behavior scores in healthy children. Biol Psychiatry. 70:283-290.
42. Edmiston EK, Blackford JU. 2013. Childhood maltreatment and response to novel face stimuli presented during functional magnetic resonance imaging in adults. Psychiatry Res. 212: 36-42.
43. Ekman P, FriesenW. 1979. Pictures of Facial Affect. San Francisco: Consulting Psychologist Press.
44. Esslinger C, Walter H, Kirsch P, Erk S, Schnell K, Arnold C, Haddad L, Mier D, Opitz vB, Raab K, et al. 2009. Neural mechanisms of a genome-wide supported psychosis variant. Science. 324:605.
45. 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. 100:7406-7411.
46. Fish EW, Faccidomo S, Miczek KA. 1999. Aggression heightened by alcohol or social instigation in mice: reduction by the 5-HT(1B) receptor agonist CP-94,253. Psychopharmacology (Berl). 146:391-399.
47. Fox SE, Levitt P, Nelson CA III. 2010. Howthe timing and quality of early experiences influence the development of brain architecture. Child Develop. 81:28-40.
48. Frazzetto G, Di Lorenzo G, Carola V, Proietti L, Sokolowska E, Siracusano A, Gross C, Troisi A. 2007. Early trauma and increased risk for physical aggression during adulthood: the moderating role of MAOA genotype. PLoS ONE. 2:e486.
49. Frings L, Wagner K, Unterrainer J, Spreer J, Halsband U, Schulze-Bonhage A. 2006. Gender-related differences in lateralization of hippocampal activation and cognitive strategy. Neuroreport. 17:417-421.
50. Fumagalli F, Molteni R, Racagni G, Riva MA. 2007. Stress during development: impact on neuroplasticity and relevance to psychopathology. Prog Neurobiol. 81:197-217.
51. Gallardo-Pujol D, Andres-Pueyo A, Maydeu-Olivares A. 2013. MAOA genotype, social exclusion and aggression: an experimental test of a gene-environment interaction. Genes Brain Behav. 12:140-145.
52. Giedd JN. 2004. Structural magnetic resonance imaging of the adolescent brain. Ann N Y Acad Sci. 1021:77-85.
53. Hariri AR, Tessitore A, Mattay VS, Fera F, Weinberger DR. 2002.The amygdala response to emotional stimuli: a comparison of faces and scenes. Neuroimage. 17:317-323.
54. Herman JP, Cullinan WE. 1997. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci. 20:78-84.
55. Herman JP, Prewitt CM, Cullinan WE. 1996. Neuronal circuit regulation of the hypothalamo-pituitary-adrenocortical stress axis. Crit Rev Neurobiol. 10:371-394.
56. Hill J, Breen G, Quinn J, Tibu F, Sharp H, Pickles A. 2013. Evidence for interplay between genes and maternal stress in utero: monoamine oxidase A polymorphism moderates effects of life events during pregnancy on infant negative emotionality at 5 weeks. Genes Brain Behav. 12:388-396.
57. Holz NE, Boecker R, Baumeister S, Hohm E, Zohsel K, Buchmann AF, Blomeyer D, Jennen-Steinmetz C, Hohmann S, Wolf I, et al. 2014. Effect of prenatal exposure to tobacco smoke on inhibitory control: neuroimaging results from a 25-year prospective study. JAMA Psychiatry. doi:10.1001/jamapsychiatry.2014.343.
58. Holz NE, Buchmann AF, Boecker R, Blomeyer D, Baumeister S, Wolf I, Rietschel M, Witt SH, Plichta MM, Meyer-Lindenberg A, et al. 2014. Role of FKBP5 in emotion processing: results on amygdala activity, connectivity and volume. Brain Struct Funct. doi:10.1007/s00429-014-0729-5.
59. Jabbi M, Korf J, Kema IP, Hartman C, van der PG, Minderaa RB, Ormel J, den Boer JA. 2007. Convergent genetic modulation of the endocrine stress response involves polymorphic variations of 5-HTT, COMT and MAOA. Mol Psychiatry. 12:483-490.
60. Jones AP, Laurens KR, Herba CM, Barker GJ, Viding E. 2009. Amygdala hypoactivity to fearful faces in boys with conduct problems and callous-unemotional traits. Am J Psychiatry. 166:95-102.
61. Kempes M, Matthys W, Maassen G, van Goozen S, van Engeland H. 2006. A parent questionnaire for distinguishing between reactive and proactive aggression in children. Eur Child Adolesc Psychiatry. 15:38-45.
62. Kiehl KA. 2006.A cognitive neuroscience perspective on psychopathy: evidence for paralimbic system dysfunction. Psychiatry Res. 142:107-128.
63. Kiehl KA, Smith AM, Hare RD, Mendrek A, Forster BB, Brink J, Liddle PF. 2001. Limbic abnormalities in affective processing by criminal psychopaths as revealed by functional magnetic resonance imaging. Biol Psychiatry. 50:677-684.
64. Kim-Cohen J, Caspi A, Taylor A, Williams B, Newcombe R, Craig IW, Moffitt TE. 2006. MAOA, maltreatment, and geneenvironment interaction predicting children's mental health: new evidence and a meta-analysis. Mol Psychiatry. 11:903-913.
65. Klur S, Muller C, Pereira de Vasconcelos A, Ballard T, Lopez J, Galani R, Certa U, Cassel JC. 2009. Hippocampal-dependent spatial memory functions might be lateralized in rats: an approach combining gene expression profiling and reversible inactivation. Hippocampus. 19:800-816.
66. Kudielka BM, Kirschbaum C. 2005. Sex differences in HPA axis responses to stress: a review. Biol Psychiatry. 69:113-132.
67. Laucht M, Brandeis D, Zohsel K. 2013. Gene-environment interactions in the etiology of human violence. In: Miczek KA, Meyer-Lindenberg A, editors. Neuroscience of aggression: preclinical and clinical research. Berlin (DE): Springer.
68. Laucht M, Esser G, Baving L, Gerhold M, Hoesch I, Ihle W, Steigleider P, Stock B, Stoehr RM, Weindrich D, et al. 2000. Behavioral sequelae of perinatal insults and early family adversity at 8 years of age. J Am Acad Child Adolesc Psychiatry. 39:1229-1237.
69. Laucht M, Esser G, Schmidt MH. 1997. Developmental outcome of infants born with biological and psychosocial risks. J Child Psychol Psychiatry. 38:843-853.
70. Lee BT, Ham BJ. 2008. Monoamine oxidase A-uVNTR genotype affects limbic brain activity in response to affective facial stimuli. Neuroreport. 19:515-519.
71. Lenroot RK, Giedd JN. 2011. Annual research review: developmental considerations of gene by environment interactions. J Child Psychol Psychiatry. 52:429-441.
72. Linnoila VM, Virkkunen M. 1992. Aggression, suicidality, and serotonin. J Clin Psychiatry. 53(Suppl):46-51.
73. Lupien SJ, McEwen BS, Gunnar MR, Heim C. 2009. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci. 10:434-445.
74. MacLusky NJ, Clark AS, Naftolin F, Goldman-Rakic PS. 1987. Estrogen formation in the mammalian brain: possible role of aromatase in sexual differentiation of the hippocampus and neocortex. Steroids. 50:459-474.
75. MacLusky NJ, Naftolin F, Goldman-Rakic PS. 1986. Estrogen formation and binding in the cerebral cortex of the developing rhesus monkey. Proc Natl Acad Sci USA. 83:513-516.
76. Maheu FS, Dozier M, Guyer AE, Mandell D, Peloso E, Poeth K, Jenness J, Lau JY, Ackerman JP, Pine DS, et al. 2010. A preliminary study of medial temporal lobe function in youths with a history of caregiver deprivation and emotional neglect. Cogn Affect Behav Neurosci. 10:34-49.
77. Maier-Diewald W, Wittchen H-U, Hecht H, Werner-Eilert K. 1983. [Munich Interview for the Assessment of Life Events and Conditions-Manual]. Munich (DE): Max Planck Institute of Psychiatry.
78. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH. 2003. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage. 19:1233-1239.
79. 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. 95:9-23.
80. Maron E, Lang A, Tasa G, Liivlaid L, Toru I, Must A, Vasar V, Shlik J. 2005. Associations between serotonin-related gene polymorphisms and panic disorder. Int J Neuropsychopharmacol. 8:261-266.
81. Marsh AA, Finger EC, Mitchell DG, Reid ME, Sims C, Kosson DS, Towbin KE, Leibenluft E, Pine DS, Blair RJ. 2008. Reduced amygdala response to fearful expressions in children and adolescents with callous-unemotional traits and disruptive behavior disorders. Am J Psychiatry. 165:712-720.
82. Meloy JR. 2006. Empirical basis and forensic application of affective and predatory violence. Aust N Z J Psychiatry. 40:539-547.
83. Meyer-Lindenberg A, Buckholtz JW, Kolachana B, Hariri R, Pezawas L, Blasi G, Wabnitz A, Honea R, Verchinski B, Callicott JH, et al. 2006. Neural mechanisms of genetic risk for impulsivity and violence in humans. Proc Natl Acad Sci USA. 103:6269-6274.
84. Meyer-Lindenberg A, Weinberger DR. 2006. Intermediate phenotypes and genetic mechanisms of psychiatric disorders. Nat Rev Neurosci. 7:818-827.
85. Mier D, Kirsch P, Meyer-Lindenberg A. 2010. Neural substrates of pleiotropic action of genetic variation in COMT: a meta-analysis. Mol Psychiatry. 15:918-927.
86. Migeon B. 2014. Females Are Mosaics: X Inactivation and Sex Differences in Disease. Oxford (GB): University Press.
87. Molodtsova GF, Il'iuchenok RI. 1990. [Role of serotonin receptors in the amygdaloid complex and central gray substance in conditioned passive avoidance reaction in rats]. Biull Eksp Biol Med. 109:3-5.
88. Mos J, Olivier B, Poth M, Van OR, Van AH. 1993. The effects of dorsal raphe administration of eltoprazine, TFMPP and 8-OHDPAT on resident intruder aggression in the rat. Eur J Pharmacol. 238:411-415.
89. Neumann ID, Veenema AH, Beiderbeck DI. 2010. Aggression and anxiety: social context and neurobiological links. Front Behav Neurosci. 4:12.
90. Olivier B, Mos J, Van OR, Hen R. 1995. Serotonin receptors and animal models of aggressive behavior. Pharmacopsychiatry. 28 (Suppl 2):80-90.
91. Passamonti L, Cerasa A, Gioia MC, Magariello A, Muglia M, Quattrone A, Fera F. 2008. Genetically dependent modulation of serotonergic inactivation in the human prefrontal cortex. Neuroimage. 40:1264-1273.
92. Passamonti L, Fairchild G, Goodyer IM, Hurford G, Hagan CC, Rowe JB, Calder AJ. 2010. Neural abnormalities in early-onset and adolescence-onset conduct disorder. Arch Gen Psychiatry. 67:729-738.
93. Passamonti L, Fera F, Magariello A, Cerasa A, Gioia MC, Muglia M, Nicoletti G, Gallo O, Provinciali L, Quattrone A. 2006. Monoamine oxidase-A genetic variations influence brain activity associated with inhibitory control: newinsight into the neural correlates of impulsivity. Biol Psychiatry. 59:334-340.
94. Pawliczek CM, Derntl B, Kellermann T, Gur RC, Schneider F, Habel U. 2013. Anger under control: neural correlates of frustration as a function of trait aggression. PLoS ONE. 8:e78503.
95. Pezawas L, Meyer-Lindenberg A, Drabant EM, Verchinski BA, Munoz KE, Kolachana BS, Egan MF, Mattay VS, Hariri AR, Weinberger DR. 2005. 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat Neurosci. 8:828-834.
96. Philibert RA, Gunter TD, Beach SR, Brody GH, Madan A. 2008. MAOA methylation is associated with nicotine and alcohol dependence in women. Am J Med Genet B Neuropsychiatr Genet. 147B:565-570.
97. Price LH, Malison RT, McDougle CJ, Pelton GH, Heninger GR. 1998. The neurobiology of tryptophan depletion in depression: effects of intravenous tryptophan infusion. Biol Psychiatry. 43:339-347.
98. Reif A, Weber H, Domschke K, Klauke B, Baumann C, Jacob CP, Strohle A, Gerlach AL, Alpers GW, Pauli P, et al. 2012. Metaanalysis argues for a female-specific role of MAOA-uVNTR in panic disorder in four European populations. Am J Med Genet B Neuropsychiatr Genet. 159B:786-793.
99. Sabol SZ, Hu S, Hamer D. 1998. A functional polymorphism in the monoamine oxidase A gene promoter. Hum Genet. 103: 273-279.
100. Samochowiec J, Hajduk A, Samochowiec A, Horodnicki J, Stepien G, Grzywacz A, Kucharska-Mazur J. 2004. Association studies of MAO-A, COMT, and 5-HTT genes polymorphisms in patients with anxiety disorders of the phobic spectrum. Psychiatry Res. 128:21-26.
101. Schneider S, Peters J, Bromberg U, Brassen S, Menz MM, Miedl SF, Loth E, Banaschewski T, Barbot A, Barker G, et al. 2011. Boys do it the right way: sex-dependent amygdala lateralization during face processing in adolescents. Neuroimage. 56: 1847-1853.
102. Shaikh MB, Steinberg A, Siegel A. 1993. Evidence that substance P is utilized in medial amygdaloid facilitation of defensive rage behavior in the cat. Brain Res. 625:283-294.
103. Siever LJ. 2008. Neurobiology of aggression and violence. Am J Psychiatry. 165:429-442.
104. Simons RL, Lei MK, Beach SR, Brody GH, Philibert RA, Gibbons FX. 2011. Social environmental variation, plasticity genes, and aggression: evidence for the differential susceptibility hypothesis. Am Sociol Rev. 76:833-912.
105. Soloff P, Nutche J, Goradia D, Diwadkar V. 2008. Structural brain abnormalities in borderline personality disorder: a voxelbased morphometry study. Psychiatry Res. 164:223-236.
106. Squire LR. 1986. Mechanisms of memory. Science. 232:1612-1619.
107. Stephenson Z, Woodhams J, Cooke C. 2013. Sex differences in predictors of violent and non-violent juvenile offending. Aggress Behav. 40:165-177.
108. Suzuki M, Hagino H, Nohara S, Zhou SY, Kawasaki Y, Takahashi T, Matsui M, Seto H, Ono T, Kurachi M. 2005. Male-specific volume expansion of the human hippocampus during adolescence. Cereb Cortex. 15:187-193.
109. Teicher MH, Andersen SL, Polcari A, Anderson CM, Navalta CP, Kim DM. 2003. The neurobiological consequences of early stress and childhood maltreatment. Neurosci Biobehav Rev. 27:33-44.
110. Tottenham N, Sheridan MA. 2010. A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing. Front Hum Neurosci. 3:1-18.
111. van Bogaert P, Wikler D, Damhaut P, Szliwowski HB, Goldman S. 1998. Regional changes in glucose metabolism during brain development from the age of 6 years. Neuroimage. 8:62-68.
112. van der Vegt BJ, Lieuwes N, van deWall EH, Kato K, Moya-Albiol L, Martinez-Sanchis S, de Boer SF, Koolhaas JM. 2003. Activation of serotonergic neurotransmission during the performance of aggressive behavior in rats. Behav Neurosci. 117:667-674.
113. Varnas K, Halldin C, Hall H. 2004. Autoradiographic distribution of serotonin transporters and receptor subtypes in human brain. Hum Brain Mapp. 22:246-260.
114. Verhoeven FE, Booij L, Kruijt AW, Cerit H, Antypa N, Does W. 2012. The effects of MAOA genotype, childhood trauma, and sex on trait and state-dependent aggression. Brain Behav. 2:806-813.
115. Virkkunen M, Rawlings R, Tokola R, Poland RE, Guidotti A, Nemeroff C, Bissette G, Kalogeras K, Karonen SL, Linnoila M. 1994. CSF biochemistries, glucose metabolism, and diurnal activity rhythms in alcoholic, violent offenders, fire setters, and healthy volunteers. Arch Gen Psychiatry. 51:20-27.
116. Vogt BA, Finch DM, Olson CR. 1992. Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb Cortex. 2:435-443.
117. Vrticka P, Sander D, Vuilleumier P. 2012. Lateralized interactive social content and valence processing within the human amygdala. Front Hum Neurosci. 6:358.
118. Wakschlag LS, Kistner EO, Pine DS, Biesecker G, Pickett KE, Skol AD, Dukic V, Blair RJ, Leventhal BL, Cox NJ Jr, et al. 2010. Interaction of prenatal exposure to cigarettes and MAOA genotype in pathways to youth antisocial behavior. Mol Psychiatry. 15:928-937.
119. Widom CS, Brzustowicz LM. 2006. MAOA and the "cycle of violence": childhood abuse and neglect, MAOA genotype, and risk for violent and antisocial behavior. Biol Psychiatry. 60:684-689.
120. Wittchen HU, Essau CA, Hecht H, Teder W, Pfister H. 1989. Reliability of life event assessments: test-retest reliability and fall-off effects of the Munich Interview for the Assessment of Life Events and Conditions. J Affect Disord. 16:77-91.
121. Wittchen HU, Zaudig M, Fydrich T. 1997. [Structured clinical interview for DSM-IV Axis I and II-SCID]. Göttingen (DE): Hogrefe.
122. Wong CC, Caspi A, Williams B, Craig IW, Houts R, Ambler A, Moffitt TE, Mill J. 2010. A longitudinal study of epigenetic variation in twins. Epigenetics. 5:516-526.
123. Yang Y, Raine A. 2009. Prefrontal structural and functional brain imaging findings in antisocial, violent, and psychopathic individuals: a meta-analysis. Psychiatry Res. 174:81-88.