Cited by 138Neurotransmitter Receptor Influence on BehaviorPsychopathy, Forensic Psychiatry, Sexual OffendingNeuroendocrine regulation and behavior

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The role of monoamine oxidase A in the neurobiology of aggressive, antisocial, and violent behavior: A tale of mice and men

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Kolla, Nathan J., Bortolato, Marco·2020·Progress in Neurobiology

DOI 10.1016/j.pneurobio.2020.101875PMC PMC7609507

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Abstract

Over the past two decades, research has revealed that genetic factors shape the propensity for aggressive, antisocial, and violent behavior. The best-documented gene implicated in aggression is MAOA (Monoamine oxidase A), which encodes the key enzyme for the degradation of serotonin and catecholamines. Congenital MAOA deficiency, as well as low-activity MAOA variants, has been associated with a higher risk for antisocial behavior (ASB) and violence, particularly in males with a history of child maltreatment. Indeed, the interplay between low MAOA genetic variants and early-life adversity is the best-documented gene × environment (G × E) interaction in the pathophysiology of aggression and ASB. Additional evidence indicates that low MAOA activity in the brain is strongly associated with a higher propensity for aggression; furthermore, MAOA inhibition may be one of the primary mechanisms whereby prenatal smoke exposure increases the risk of ASB. Complementary to these lines of evidence, mouse models of Maoa deficiency and G × E interactions exhibit striking similarities with clinical phenotypes, proving to be valuable tools to investigate the neurobiological mechanisms underlying antisocial and aggressive behavior. Here, we provide a comprehensive overview of the current state of the knowledge on the involvement of MAOA in aggression, as defined by preclinical and clinical evidence. In particular, we show how the convergence of human and animal research is proving helpful to our understanding of how MAOA influences antisocial and violent behavior and how it may assist in the development of preventative and therapeutic strategies for aggressive manifestations.

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The Evolution of Dopamine Systems in Chordates
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Psychopathy/Antisocial Personality Disorder Conundrum
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Genetic variation in MAOA modulates ventromedial prefrontal circuitry mediating individual differences in human personality
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The activation of 5‐HT2A receptors in prefrontal cortex enhances dopaminergic activity
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Interaction between a functional MAOA locus and childhood sexual abuse predicts alcoholism and antisocial personality disorder in adult women
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Understanding Genetic Risk for Aggression: Clues From the Brain’s Response to Social Exclusion
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Meta-analysis of gene–environment interactions in developmental psychopathology
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Genetic background of extreme violent behavior
Tiihonen, J., Rautiainen, M.-R., Ollila, H. M., Repo‐Tiihonen, E., Virkkunen, M. E., Palotie, A. V., Pietiläinen, O. P. H., Kristiansson, K., Joukamaa, M. I., Lauerma, H., et al. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.130 · Cited by 220
Early Language Impairment and Young Adult Delinquent and Aggressive Behavior
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Distribution of Monoamine Oxidase Proteins in Human Brain: Implications for Brain Imaging Studies
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Genetics of human aggressive behaviour
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Maternal Smoking During Pregnancy and Risk of Criminal Behavior Among Adult Male Offspring in the Northern Finland 1966 Birth Cohort
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The Covalently‐Bound Flavin of Hepatic Monoamine Oxidase
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Developmental consequences of prenatal tobacco exposure
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Early Trauma and Increased Risk for Physical Aggression during Adulthood: The Moderating Role of MAOA Genotype
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Diathesis-stress models.
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The Social Psychology of Aggression
Krahé, B. (2020) · Routledge eBooks · doi:10.4324/9780429466496 · Cited by 203
Estrogen increases the density of 5-Hydroxytryptamine2A receptors in cerebral cortex and nucleus accumbens in the female rat
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Association between monoamine oxidase A activity in human male skin fibroblasts and genotype of the MAOA promoter-associated variable number tandem repeat
Denney, R. M., Koch, H., & Craig, I. (1999) · Human Genetics · doi:10.1007/s004399900183 · Cited by 201
Human monoamine oxidase A and B genes map to xp11.23 and are deleted in a patient with norrie disease
Lan, N. C., Heinzmann, C., Gal, A., Klisak, I. J., Orth, U., Lai, E., Grimsby, J. S., Sparkes, R. S., Mohandas, T. K., & Shih, J. C. (1989) · Genomics · doi:10.1016/0888-7543(89)90279-6 · Cited by 200
CRF receptor 1 regulates anxiety behavior via sensitization of 5-HT2 receptor signaling
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Thalamic axons confer a blueprint of the sensory periphery onto the developing rat somatosensory cortex
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Association of a regulatory polymorphism in the promoter region of the monoamine oxidase A gene with antisocial alcoholism
Samochowiec, J., Lesch, K., Rottmann, M., Smolka, M. N., Syagailo, Y. V., Okladnova, O., Rommelspacher, H., Winterer, G., Schmidt, L. G., & Sander, T. (1999) · Psychiatry Research · doi:10.1016/s0165-1781(99)00020-7 · Cited by 190
MAOA Genotype, Maltreatment, and Aggressive Behavior: The Changing Impact of Genotype at Varying Levels of Trauma
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Childhood Maltreatment, Subsequent Antisocial Behavior, and the Role of Monoamine Oxidase A Genotype
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Glial GABA, synthesized by monoamine oxidase B, mediates tonic inhibition
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Candidate Genes for Aggression and Antisocial Behavior: A Meta-analysis of Association Studies of the 5HTTLPR and MAOA-uVNTR
Ficks, C. A., & Waldman, I. D. (2014) · Behavior Genetics · doi:10.1007/s10519-014-9661-y · Cited by 182
The neurobiological basis of human aggression: A review on genetic and epigenetic mechanisms
Waltes, R., Chiocchetti, A. G., & Freitag, C. M. (2016) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32388 · Cited by 182
Violent evil and the General Aggression Model.
Anderson, C. A., & Carnagey, N. L. (2004) · Cited by 180
The impact of selective amygdala, orbital frontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta).
Machado, C. J., & Bachevalier, J. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.4.761 · Cited by 178
Laboratory Induced Aggression: A Positron Emission Tomography Study of Aggressive Individuals with Borderline Personality Disorder
New, A. S., Hazlett, E. A., Newmark, R. E., Zhang, J., Triebwasser, J., Meyerson, D. A., Lazarus, S. A., Trisdorfer, R., Goldstein, K. E., Goodman, M. S., et al. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.07.015 · Cited by 176
The VNTR 2 repeat in MAOA and delinquent behavior in adolescence and young adulthood: associations and MAOA promoter activity
Guo, G., Ou, X., Roettger, M. E., & Shih, J. C. (2008) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201999 · Cited by 174
The epidemiology of antisocial personality disorder
Moran, P. (1999) · Social Psychiatry and Psychiatric Epidemiology · doi:10.1007/s001270050138 · Cited by 166
Glucocorticoid and Androgen Activation of Monoamine Oxidase A Is Regulated Differently by R1 and Sp1
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Reduced amygdala–orbitofrontal connectivity during moral judgments in youths with disruptive behavior disorders and psychopathic traits
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Investigation of the functional effect of monoamine oxidase polymorphisms in human brain
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Dopamine and serotonin signaling during two sensitive developmental periods differentially impact adult aggressive and affective behaviors in mice
Yu, Q., Teixeira, C. M., Mahadevia, D., Huang, Y., Balsam, D., Mann, J. J., Gingrich, J. A., & Ansorge, M. S. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.10 · Cited by 158
Monoamine oxidase A genotype is associated with gang membership and weapon use
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A Theory of How Columns in the Neocortex Enable Learning the Structure of the World
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“Cortical columns are posited to integrate input over time and space and are, therefore, essential for integrating environmental information (Hawkins et al., 2017).”
Background
A Non-Additive Interaction of a Functional MAO-A VNTR and Testosterone Predicts Antisocial Behavior
Sjöberg, R. L., Ducci, F., Barr, C. S., Newman, T. K., Dell’Osso, L., Virkkunen, M. E., & Goldman, D. A. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301417 · Cited by 148
Genetics of aggressive behavior: An overview
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MAOA, abuse exposure and antisocial behaviour: 30-year longitudinal study
Fergusson, D. M., Boden, J. M., Horwood, L. J., Miller, A. L., & Kennedy, M. A. (2011) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.110.086991 · Cited by 147
The effects of child maltreatment on early signs of antisocial behavior: Genetic moderation by tryptophan hydroxylase, serotonin transporter, and monoamine oxidase A genes
Cicchetti, D., Rogosch, F. A., & Thibodeau, E. L. (2012) · Development and Psychopathology · doi:10.1017/s0954579412000442 · Cited by 146
A Spontaneous Point Mutation Produces Monoamine Oxidase A/B Knock-out Mice with Greatly Elevated Monoamines and Anxiety-like Behavior*♦
Chen, K., Holschneider, D., Wu, W., Rebrin, I., & Shih, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405550200 · Cited by 144
The Social Psychology of Aggression
Krahé, B. (2013) · Psychology Press eBooks · doi:10.4324/9780203082171 · Cited by 144
Behavioral outcomes of monoamine oxidase deficiency: preclinical and clinical evidence
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Self-citation
Adolescent girls and criminal activity: Role of MAOA-LPR genotype and psychosocial factors
Sjöberg, R. L., Nilsson, K. W., Wargelius, H., Leppert, J., Lindström, L., & Oreland, L. (2007) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30360 · Cited by 143
Association of the Serotonin Transporter and Receptor Gene Polymorphisms in Neuropsychiatric Symptoms in Alzheimer Disease
Assal, F., Alarcón, M., Solomon, E., Masterman, D. L., Geschwind, D. H., & Cummings, J. L. (2004) · Archives of Neurology · doi:10.1001/archneur.61.8.1249 · Cited by 142
Promoter organization and activity of human monoamine oxidase (MAO) A and B genes
Zhu, Q., Grimsby, J. S., Chen, K., & Shih, J. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-11-04437.1992 · Cited by 140
The Appetitive Aggression Scale—development of an instrument for the assessment of human's attraction to violence.
Weierstall, R., & Elbert, T. R. (2011) · European Journal of Psychotraumatology · doi:10.3402/ejpt.v2i0.8430 · Cited by 140
Influence of cage enrichment on aggressive behaviour and physiological parameters in male mice
Loo, P. L. P. V., Kruitwagen, C. L. J. J., Koolhaas, J. M., de Weerd, H. A. V., van Zutphen, L. F. M., & Baumans, V. (2002) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(01)00200-3 · Cited by 140
Fascination violence: on mind and brain of man hunters
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Genetics of Aggression
Anholt, R. R. H., & Mackay, T. F. C. (2012) · Annual Review of Genetics · doi:10.1146/annurev-genet-110711-155514 · Cited by 139
Maltreatment, MAOA, and Delinquency: Sex Differences in Gene–Environment Interaction in a Large Population-Based Cohort of Adolescents
Åslund, C., Nordquist, N., Comasco, E., Leppert, J., Oreland, L., & Nilsson, K. W. (2010) · Behavior Genetics · doi:10.1007/s10519-010-9356-y · Cited by 135
Presynaptic serotonin 2A receptors modulate thalamocortical plasticity and associative learning
Barre, A., Berthoux, C., De Bundel, D., Valjent, E., Bockaert, J., Marin, P., & Bécamel, C. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1525586113 · Cited by 135
Interaction of prenatal exposure to cigarettes and MAOA genotype in pathways to youth antisocial behavior
Wakschlag, L. S., Kistner, E. O., Pine, D. S., Biesecker, G., Pickett, K. E., Skol, A. D., Dukić, V., Blair, J., LEVENTHAL, B. L., Cox, N. J., et al. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.22 · Cited by 133
The Psychopharmacology of Aggressive Behavior
Comai, S., Tau, M., & Gobbi, G. (2011) · Journal of Clinical Psychopharmacology · doi:10.1097/jcp.0b013e31823f8770 · Cited by 132
Novel monoamine oxidase A knock out mice with human-like spontaneous mutation
Scott, A. L., Bortolato, M., Chen, K., & Shih, J. C. (2008) · Neuroreport · doi:10.1097/wnr.0b013e3282fd6e88 · Cited by 130
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A promoter polymorphism in the monoamine oxidase A gene and its relationships to monoamine metabolite concentrations in CSF of healthy volunteers
Jönsson, E. G., Norton, N., Gustavsson, P. J., Oreland, L., Owen, M. J., & Sedvall, G. C. (2000) · Journal of Psychiatric Research · doi:10.1016/s0022-3956(00)00013-3 · Cited by 128
The nature of human aggression
Archer, J. E. (2009) · International Journal of Law and Psychiatry · doi:10.1016/j.ijlp.2009.04.001 · Cited by 126
HEART RATE AND ANTISOCIAL BEHAVIOR: THE MEDIATING ROLE OF IMPULSIVE SENSATION SEEKING
Portnoy, J., Raine, A., Chen, F. R., Pardini, D. A., Loeber, R., & Jennings, J. R. (2014) · Criminology · doi:10.1111/1745-9125.12038 · Cited by 126
Basal and dynamic relationships between implicit power motivation and estradiol in women
Stanton, S. J., & Schultheiss, O. C. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.07.002 · Cited by 125
Dinucleotide repeat polymorphism at the MAOA locus
BIack, G. C. M., Chen, Z., Craig, I., & Powell, J. F. (1991) · Nucleic Acids Research · doi:10.1093/nar/19.3.689-a · Cited by 124
Monoamine oxidase A and A/B knockout mice display autistic-like features
Bortolato, M., Godar, S. C., Alzghoul, L., Zhang, J., Darling, R. D., Simpson, K. L., Bini, V., Chen, K., Wellman, C. L., Lin, R. C. S., et al. (2012) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145712000715 · Cited by 124
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Differential Functional Variability of Serotonin Transporter and Monoamine Oxidase A Genes in Macaque Species Displaying Contrasting Levels of Aggression-Related Behavior
Wendland, J. R., Lesch, K., Newman, T. K., Timme, A., Gachot‐Neveu, H., Thierry, B., & Suomi, S. J. (2005) · Behavior Genetics · doi:10.1007/s10519-005-9017-8 · Cited by 124
Identifying persistently antisocial offenders using the Hare Psychopathy Checklist and DSM antisocial personality disorder criteria.
Skilling, T. A., Harris, G. T., Rice, M., & Quinsey, V. L. (2002) · Psychological Assessment · doi:10.1037/1040-3590.14.1.27 · Cited by 124
The role of monoamine oxidase A in aggression: Current translational developments and future challenges
Godar, S. C., Fite, P. J., McFarlin, K. M., & Bortolato, M. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.01.001 · Cited by 124
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Environmental enrichment and mouse models: Current perspectives
Bayne, K. A. L. (2018) · Animal Models and Experimental Medicine · doi:10.1002/ame2.12015 · Cited by 124
The Epidemiology of Antisocial Personality Disorder
Howard, R., & Duggan, C. F. (2022) · Cambridge University Press eBooks · doi:10.1017/9781911623892.006 · Cited by 124
Multimethod assessment of psychopathy in relation to factors of internalizing and externalizing from the Personality Assessment Inventory: The impact of method variance and suppressor effects.
Blonigen, D. M., Patrick, C. J., Douglas, K. S., Poythress, N. G., Skeem, J. L., Lilienfeld, S. O., Edens, J. F., & Krueger, R. F. (2010) · Psychological Assessment · doi:10.1037/a0017240 · Cited by 121
Violence and psychiatric morbidity in the national household population of Britain: public health implications
Coid, J., Yang, M., Roberts, A., Ullrich, S., Moran, P., Bebbington, P., Brugha, T., Jenkins, R., Farrell, M., Lewis, G., et al. (2006) · British Journal of Psychiatry · doi:10.1192/bjp.189.1.12 · Cited by 121
Evidence that the methylation state of the monoamine oxidase A (MAOA) gene predicts brain activity of MAO A enzyme in healthy men
Shumay, E., Logan, J., Volkow, N. D., & Fowler, J. S. (2012) · Epigenetics · doi:10.4161/epi.21976 · Cited by 120
The Relationship Between Adult Reactive and Proactive Aggression, Hostile Interpretation Bias, and Antisocial Personality Disorder
Lobbestael, J., Cima, M., & Arntz, A. R. (2013) · Journal of Personality Disorders · doi:10.1521/pedi.2013.27.1.53 · Cited by 117
CURRENT CONCEPTIONS OF PSYCHOPATHIC PERSONALITY
Partridge, G. E. (1930) · American Journal of Psychiatry · doi:10.1176/ajp.87.1.53 · Cited by 116
Identifying persistently antisocial offenders using the Hare Psychopathy Checklist and DSM antisocial personality disorder criteria.
Skilling, T. A., Harris, G. T., Rice, M. E., & Quinsey, V. L. (2002) · Psychological Assessment · doi:10.1037//1040-3590.14.1.27 · Cited by 116
Aggressive behavior as a reinforcer in mice: activation by allopregnanolone
Fish, E. W., Bold, J. F. D., & Miczek, K. A. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1211-2 · Cited by 115
Serotonin depresses excitatory synaptic transmission and depolarization-evoked Ca2+influx in rat basolateral amygdala via 5-HT1Areceptors
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Susceptibility of brain to AMPA induced excitotoxicity transiently peaks during early postnatal development
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Monoamine oxidase a gene promoter methylation and transcriptional downregulation in an offender population with antisocial personality disorder
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Evidence That Brain MAO A Activity Does Not Correspond to MAO A Genotype in Healthy Male Subjects
Fowler, J. S., Alia‐Klein, N., Kriplani, A., Logan, J., Williams, B. S., Zhu, W., Craig, I., Telang, F., Goldstein, R. Z., Volkow, N. D., et al. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.08.038 · Cited by 112
MAOA‐uVNTR polymorphism in a Brazilian sample: Further support for the association with impulsive behaviors and alcohol dependence
Contini, V., Marques, F. Z., Garcia, C. E. D., Hutz, M. H., & Bau, C. H. D. (2006) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30290 · Cited by 110
Regulation of monoamine oxidase A by the SRY gene on the Y chromosome
Wu, J. B., Chen, K., Li, Y., Lau, Y. C., & Shih, J. C. (2009) · The FASEB Journal · doi:10.1096/fj.09-139097 · Cited by 110
Testosterone induces molecular changes in dopamine signaling pathway molecules in the adolescent male rat nigrostriatal pathway
Purves-Tyson, T. D., Owens, S. J., Double, K. L., Desai, R., Handelsman, D. J., & Weickert, C. S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091151 · Cited by 109 · cited 1×
“Ample evidence has shown that, by acting on androgen receptors, this hormone increases the synthesis of both MAOA as well as tyrosine hydroxylase (TH), the rate-limiting enzyme for dopamine synthesis (Goldstein et al., 1992; Purves-Tyson et al., 2014).”
Background
Effects of Gestational Exposure to Monoamine Oxidase Inhibitors in Rats: Preliminary Behavioral and Neurochemical Studies
Whitaker‐Azmitia, P. M., Zhang, X., & Clarke, C. (1994) · Neuropsychopharmacology · doi:10.1038/npp.1994.42 · Cited by 109
Structural Features of Human Monoamine Oxidase A Elucidated from cDNA and Peptide Sequences
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Early life stress, MAOA, and gene‐environment interactions predict behavioral disinhibition in children
Enoch, M., Steer, C. D., Newman, T. K., Gibson, N. P. S. J., & Goldman, D. A. (2009) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2009.00535.x · Cited by 107
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Self-citation

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Authors: Kolla, N. J., & Bortolato, M.
Affiliations: Centre for Addiction and Mental Health (CA)
University of Utah (US)
Corresponding author: Kolla, Nathan J.
Bortolato, Marco
ORCID: Kolla, Nathan J.
Bortolato, Marco
Venue: Progress in Neurobiology
Publisher: Elsevier BV
Published: 2020-11
Volume: 194
Pages: 101875
ISSN: 0301-0082 (ISSN-L)
DOI: 10.1016/j.pneurobio.2020.101875
PMC: PMC7609507
OpenAlex: W3036818139
Cited by: 138
References: 400
Citations by year: 2026: 18 · 2025: 25 · 2024: 29 · 2023: 42 · 2022: 11 · 2021: 12 · 2020: 1
FWCI: 2.28
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Progress in Neurobiology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Social Sciences › Psychology › Clinical Psychology › Psychopathy, Forensic Psychiatry, Sexual Offending
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
Keywords: monoamine oxidase A, aggression, antisocial behavior, violent behavior, gene-environment interaction, child abuse, prenatal tobacco exposure, serotonin, catecholamines, neurobiology of aggression
MeSH terms: Aggression, Animals, Antisocial Personality Disorder, Behavior, Animal, Humans, Monoamine Oxidase, Social Behavior, Violence, Gene-Environment Interaction

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The role of monoamine oxidase A in the neurobiology of aggressive, antisocial, and violent behavior: A tale of mice and men

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