Cognitive and neurobiological mechanisms of alcohol-related aggression

Key Points

  • Alcohol use is implicated in approximately 50% of all violent crimes and sexual assaults in industrialized nations.

  • Both acute and chronic alcohol intake increase the risk for alcohol-associated aggression.

  • Only a subset of individuals who drink alcohol become aggressive, and psychological studies have identified several gender and individual differences that confer risk for alcohol-related aggression.

  • Twin and adoption studies have shown a significant disposition towards violent behaviour only in association with an increased risk to develop alcohol dependence.

  • Animal experiments and a limited number of studies in humans show that alcohol-related aggression is found in a subset of individuals who were exposed to social adversity and carry certain risk genotypes.

  • Genetic and environmental factors are associated with aggressive behaviour: findings point to an important role of the serotonin system and its interactions with GABAergic neurotransmission in determining vulnerability to alcohol-associated aggression.

  • Chronic alcohol intake impairs serotonergic neurotransmission, which (according to studies in healthy controls but not yet in patients who are alcohol dependent) modulates limbic processing of aversive stimuli and prefrontal functions associated with behavioural control.

  • We suggest that acute alcohol intake facilitates aggression in vulnerable individuals because it impairs prefrontal executive functions, disinhibits limbic processing of threatening stimuli and elicits expectancies for alcohol-associated aggression.

Abstract

Alcohol-related violence is a serious and common social problem. Moreover, violent behaviour is much more common in alcohol-dependent individuals. Animal experiments and human studies have provided insights into the acute effect of alcohol on aggressive behaviour and into common factors underlying acute and chronic alcohol intake and aggression. These studies have shown that environmental factors, such as early-life stress, interact with genetic variations in serotonin-related genes that affect serotonergic and GABAergic neurotransmission. This leads to increased amygdala activity and impaired prefrontal function that, together, predispose to both increased alcohol intake and impulsive aggression. In addition, acute and chronic alcohol intake can further impair executive control and thereby facilitate aggressive behaviour.

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Figure 1: A neurobiological model for alcohol-associated aggression.
Figure 2: Functional and structural neural correlates of aggressive behaviour and genetic risk towards violence.

References

  1. 1

    World Health Organization. World health organization expert committee on problems related to alcohol consumption. (WHO, Geneva, 2007).

  2. 2

    Murdoch, D., Pihl, R. O. & Ross, D. Alcohol and crimes of violence: present issues. Int. J. Addict. 25, 1065–1081 (1990).

    CAS  Article  PubMed  Google Scholar 

  3. 3

    Collins, J. J. & Messerschmidt, P. M. Epidemiology of alcohol-related violence. Alcohol Health Res. World 17, 93–100 (1993).

    Google Scholar 

  4. 4

    Foran, H. M. & O'Leary, K. D. Alcohol and intimate partner violence: a meta-analytic review. Clin. Psychol. Rev. 28, 1222–1234 (2008).

    Article  PubMed  Google Scholar 

  5. 5

    Spunt, B., Brownstein, H., Goldstein, P., Fendrich, M. & Liberty, H. J. Drug-use by homicide offenders. J. Psychoactive Drugs 27, 125–134 (1995).

    CAS  Article  PubMed  Google Scholar 

  6. 6

    Jaffe, J. H., Babor, T. F. & Fishbein, D. H. Alcoholics, aggression and antisocial personality. J. Stud. Alcohol 49, 211–218 (1988).

    CAS  Article  PubMed  Google Scholar 

  7. 7

    Mayfield, D. Alcoholism, alcohol, intoxication and assaultive behavior. Dis. Nerv. Syst. 37, 288–291 (1976).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. 8

    Nicol, A. R., Gunn, J. C., Gristwoo, J., Foggitt, R. H. & Watson, J. P. Relationship of alcoholism to violent behavior resulting in long-term imprisonment. Br. J. Psychiatry 123, 47–51 (1973).

    CAS  Article  PubMed  Google Scholar 

  9. 9

    Schuckit, M. A. & Russell, J. W. An evaluation of primary alcoholics with histories of violence. J. Clin. Psychiatry 45, 3–6 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    Arseneault, L., Moffitt, T. E., Caspi, A., Taylor, P. J. & Silva, P. A. Mental disorders and violence in a total birth cohort: results from the Dunedin study. Arch. Gen. Psychiatry 57, 979–986 (2000).

    CAS  Article  PubMed  Google Scholar 

  11. 11

    Swanson, J. W., Holzer, C. E., Ganju, V. K. & Jono, R. T. Violence and psychiatric-disorder in the community: evidence from the epidemiologic catchment-area surveys. Hosp. Community Psychiatry 41, 761–770 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 12

    Lipsey, M. W., Wilson D. B., Cohen, M. A. & Derzon, J. H. Is there a causal relationship between alcohol use and violence? A synthesis of evidence. Recent Dev. Alcohol. 13, 245–282 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13

    O'Farrell, T. J., Fals-Stewart, W., Murphy, M. & Murphy, C. M. Partner violence before and after individually based alcoholism treatment for male alcoholic patients. J. Consult. Clin. Psychol. 71, 92–102 (2003).

    Article  PubMed  Google Scholar 

  14. 14

    Coid, J. et al. Violence and psychiatric morbidity in the national household population of Britain: public health implications. Br. J. Psychiatry 189, 12–19 (2006).

    Article  PubMed  Google Scholar 

  15. 15

    Chermack, S. T. & Blow, F. C. Violence among individuals in substance abuse treatment: the role of alcohol and cocaine consumption. Drug Alcohol Depend. 66, 29–37 (2002).

    Article  PubMed  Google Scholar 

  16. 16

    Murphy, C. M., Winters, J., O'Farrell, T. J., Fals-Stewart, W. & Murphy, M. Alcohol consumption and intimate partner violence by alcoholic men: comparing violent and nonviolent conflicts. Psychol. Addict. Behav. 19, 35–42 (2005).

    Article  PubMed  Google Scholar 

  17. 17

    Takahashi, A., Kwa, C., Debold, J. F. & Miczek, K. A. GABAA receptors in the dorsal raphe, nucleus of mice: escalation of aggression after alcohol consumption. Psychopharmacology 211, 467–477 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. 18

    Weerts, E. M., Tornatzky, W. & Miczek, K. A. Prevention of the pro-aggressive effects of alcohol in rats and squirrel-monkeys by benzodiazepine receptor antagonists. Psychopharmacology 111, 144–152 (1993).

    CAS  Article  PubMed  Google Scholar 

  19. 19

    Miczek, K. A., Weerts, E. M. & Debold, J. F. Alcohol, benzodiazepine-GABAA receptor complex and aggression: ethological analysis of individual differences in rodents and primates. J. Stud. Alcohol 11 (Suppl. 11), 170–179 (1993).

    CAS  Article  Google Scholar 

  20. 20

    Higley, J. D. Individual differences in alcohol-induced aggression. A nonhuman-primate model. Alcohol Res. Health 25, 12–19 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21

    Taylor, S. P. Experimental investigation of alcohol-induced aggression in humans. Alcohol Health Res. World 17, 108–112 (1993).

    Google Scholar 

  22. 22

    Buss, A. H. The Psychology of Aggression. (Wiley, New York, 1961).

    Google Scholar 

  23. 23

    Cherek, D. R. Effects of smoking different doses of nicotine on human aggressive-behavior. Psychopharmacology 75, 339–345 (1981).

    CAS  Article  PubMed  Google Scholar 

  24. 24

    Graham, K. Theories of intoxicated aggression. Can. J. Behav. Sci. 12, 141–158 (1980).

    Article  Google Scholar 

  25. 25

    Bushman, B. J. & Cooper, H. M. Effects of alcohol on human aggression: an integrative research review. Psychol. Bull. 107, 341–354 (1990). Performed over 20 years ago, this seminal meta-analysis was among the first to establish that alcohol causes aggressive behaviour in humans.

    CAS  Article  PubMed  Google Scholar 

  26. 26

    Chermack, S. T. & Giancola, P. R. The relation between alcohol and aggression: an integrated biopsychosocial conceptualization. Clin. Psychol. Rev. 17, 621–649 (1997).

    CAS  Article  PubMed  Google Scholar 

  27. 27

    Giancola, P. R. Executive functioning: a conceptual framework for alcohol-related aggression. Exp. Clin. Psychopharmacol. 8, 576–597 (2000). This conceptual paper is one of the first attempts to provide an integrative framework for the role of multiple prefrontal cognitive abilities in alcohol-related aggression. More specifically, the model proposes that alcohol-induced disruption of executive functioning mediates the relationship between alcohol consumption and aggressive behaviour and that individual differences in sober-state executive functioning moderate the strength of this relationship.

    CAS  Article  PubMed  Google Scholar 

  28. 28

    Ito, T. A., Miller, N. & Pollock, V. E. Alcohol and aggression: a meta-analysis on the moderating effects of inhibitory cues, triggering events, and self-focused attention. Psychol. Bull. 120, 60–82 (1996).

    CAS  Article  PubMed  Google Scholar 

  29. 29

    Diana, M., Gessa, G. L. & Rossetti, Z. L. Lack of tolerance to ethanol-induced stimulation of mesolimbic dopamine system. Alcohol Alcohol. 27, 329–333 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 30

    Puglisiallegra, S., Imperato, A., Angelucci, L. & Cabib, S. Acute stress induces time-dependent responses in dopamine mesolimbic system. Brain Res. 554, 217–222 (1991).

    CAS  Article  Google Scholar 

  31. 31

    Mathews, T. A., John, C. E., Lapa, G. B., Budygin, E. A. & Jones, S. R. No role of the dopamine transporter in acute ethanol effects on striatal dopamine dynamics. Synapse 60, 288–294 (2006).

    CAS  Article  PubMed  Google Scholar 

  32. 32

    Tsai, G. C., Gastfriend, D. R. & Coyle, J. T. The glutamatergic basis of human alcoholism. Am. J. Psychiatry 152, 332–340 (1995).

    CAS  Article  PubMed  Google Scholar 

  33. 33

    DiChiara, G., Acquas, E. & Tanda, G. Ethanol as a neurochemical surrogate of conventional reinforcers: the dopamine-opioid link. Alcohol 13, 13–17 (1996).

    CAS  Article  Google Scholar 

  34. 34

    Heinz, A., Beck, A., Grusser, S. M., Grace, A. A. & Wrase, J. Identifying the neural circuitry of alcohol craving and relapse vulnerability. Addict. Biol. 14, 108–118 (2009).

    CAS  Article  PubMed  Google Scholar 

  35. 35

    Bradberry, C. W. Dose-dependent effect of ethanol on extracellular dopamine in mesolimbic striatum of awake rhesus monkeys: comparison with cocaine across individuals. Psychopharmacology 165, 67–76 (2002).

    CAS  Article  PubMed  Google Scholar 

  36. 36

    Dazzi, L. et al. Progesterone enhances ethanol-induced modulation of mesocortical dopamine neurons: antagonism by finasteride. J. Neurochem. 83, 1103–1109 (2002).

    CAS  Article  PubMed  Google Scholar 

  37. 37

    Engleman, E. A., Ingraham, C. M., McBride, W. J., Lumeng, L. & Murphy, J. M. Extracellular dopamine levels are lower in the medial prefrontal cortex of alcohol-preferring rats compared to Wistar rats. Alcohol 38, 5–12 (2006).

    CAS  Article  PubMed  Google Scholar 

  38. 38

    Miczek, K. A., Covington, H. E., Nikulina, E. A. & Hammer, R. P. Aggression and defeat: persistent effects on cocaine self-administration and gene expression in peptidergic and aminergic mesocorticolimbic circuits. Neurosci. Biobehav. Rev. 27, 787–802 (2004).

    CAS  Article  PubMed  Google Scholar 

  39. 39

    Nader, M. A. & Czoty, P. W. PET imaging of dopamine D2 receptors in monkey models of cocaine abuse: genetic predisposition versus environmental modulation. Am. J. Psychiatry 162, 1473–1482 (2005).

    Article  PubMed  Google Scholar 

  40. 40

    de Almeida, R. M. M., Ferrari, P. F., Parmigiani, S. & Miczek, K. A. Escalated aggressive behavior: dopamine, serotonin and GABA. Eur. J. Pharmacol. 526, 51–64 (2005).

    CAS  Article  PubMed  Google Scholar 

  41. 41

    McBride, W. J. Central nucleus of the amygdala and the effects of alcohol and alcohol-drinking behavior in rodents. Pharmacol. Biochem. Behav. 71, 509–515 (2002).

    CAS  Article  PubMed  Google Scholar 

  42. 42

    Yokoyama, M. et al. Amygdalic levels of doparnine and serotonin rise upon exposure to conditioned fear stress without elevation of glutamate. Neurosci. Lett. 379, 37–41 (2005).

    CAS  Article  PubMed  Google Scholar 

  43. 43

    Kienast, T. et al. Dopamine in amygdala gates limbic processing of aversive stimuli in humans. Nature Neurosci. 11, 1381–1382 (2008).

    CAS  Article  PubMed  Google Scholar 

  44. 44

    Kringelbach, M. L. The human orbitofrontal cortex: linking reward to hedonic experience. Nature Rev. Neurosci. 6, 691–702 (2005).

    CAS  Article  Google Scholar 

  45. 45

    Adolphs, R. The social brain: neural basis of social knowledge. Annu. Rev. Psychol. 60, 693–716 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  46. 46

    Peterson, J. B., Rothfleisch, J., Zelazo, P. D. & Pihl, R. O. Acute alcohol-intoxication and cognitive-functioning. J. Stud. Alcohol 51, 114–122 (1990).

    CAS  Article  PubMed  Google Scholar 

  47. 47

    Easdon, C. M. & Vogel-Sprott, M. Alcohol and behavioral control: impaired response inhibition and flexibility in social drinkers. Exp. Clin. Psychopharmacol. 8, 387–394 (2000).

    CAS  Article  PubMed  Google Scholar 

  48. 48

    Finn, P. R., Justus, A., Mazas, C. & Steinmetz, J. E. Working memory, executive processes and the effects of alcohol on Go/No-Go learning: testing a model of behavioral regulation and impulsivity. Psychopharmacology 146, 465–472 (1999).

    CAS  Article  PubMed  Google Scholar 

  49. 49

    Mulvihill, L. E., Skilling, T. A. & VogelSprott, M. Alcohol and the ability to inhibit behavior in men and women. J. Stud. Alcohol 58, 600–605 (1997).

    CAS  Article  PubMed  Google Scholar 

  50. 50

    Schweizer, T. A. et al. Neuropsychological profile of acute alcohol intoxication during ascending and descending blood alcohol concentrations. Neuropsychopharmacology 31, 1301–1309 (2006).

    CAS  Article  PubMed  Google Scholar 

  51. 51

    Schreckenberger, M. et al. Acute alcohol effects on neuronal and attentional processing: striatal reward system and inhibitory sensory interactions under acute ethanol challenge. Neuropsychopharmacology 29, 1527–1537 (2004).

    CAS  Article  PubMed  Google Scholar 

  52. 52

    Guillot, C. R., Fanning, J. R., Bullock, J. S., McCloskey, M. S. & Berman, M. E. Effects of alcohol on tests of executive functioning in men and women: a dose response examination. Exp. Clin. Psychopharmacol. 18, 409–417 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  53. 53

    Lyvers, M. F. & Maltzman, I. Selective effects of alcohol on wisconsin card sorting test-performance. Br. J. Addict. 86, 399–407 (1991).

    CAS  Article  PubMed  Google Scholar 

  54. 54

    Ridderinkhof, K. R. et al. Alcohol consumption impairs detection of performance errors in mediofrontal cortex. Science 298, 2209–2211 (2002).

    CAS  Article  PubMed  Google Scholar 

  55. 55

    Hawkins, K. A. & Trobst, K. K. Frontal lobe dysfunction and aggression: conceptual issues and research findings. Aggress. Violent Behav. 5, 147–157 (2000).

    Article  Google Scholar 

  56. 56

    Barbas, H. Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices. Brain Res. Bull. 52, 319–330 (2000).

    CAS  Article  PubMed  Google Scholar 

  57. 57

    Amaral, D. G. & Price, J. L. Amygdalo-cortical projections in the monkey (macaca-fascicularis). J. Comp. Neurol. 230, 465–496 (1984).

    CAS  Article  PubMed  Google Scholar 

  58. 58

    Ochsner, K. N. & Gross, J. J. The cognitive control of emotion. Trends Cogn. Sci. 9, 242–249 (2005).

    Article  PubMed  Google Scholar 

  59. 59

    Birbaumer, N. et al. Deficient fear conditioning in psychopathy: a functional magnetic resonance imaging study. Arch. Gen. Psychiatry 62, 799–805 (2005).

    Article  PubMed  Google Scholar 

  60. 60

    Jones, A. P., Laurens, K. R., Herba, C. M., Barker, G. J. & Viding, E. Amygdala hypoactivity to fearful faces in boys with conduct problems and callous-unemotional traits. Am. J. Psychiatry 166, 95–102 (2009).

    Article  PubMed  Google Scholar 

  61. 61

    Marsh, A. A. et al. Reduced amygdala response to fearful expressions in children and adolescents with callous-unemotional traits and disruptive behavior disorders. Am. J. Psychiatry 165, 712–720 (2008).

    Article  PubMed  Google Scholar 

  62. 62

    Coccaro, E. F., McCloskey, M. S., Fitzgerald, D. A. & Phan, K. L. Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biol. Psychiatry 62, 168–178 (2007). This study used fMRI to show that amygdala responses to social threat cues are increased in individuals exhibiting impulsive aggression, whereas orbitofrontal cortex resonses are reduced, providing evidence for a link between a dysfunctional corticolimbic network and aggressive behaviour.

    Article  PubMed  Google Scholar 

  63. 63

    Lee, T. M. C., Chan, S. C. & Raine, A. Strong limbic and weak frontal activation to aggressive stimuli in spouse abusers. Mol. Psychiatry 13, 655–656 (2008).

    CAS  Article  PubMed  Google Scholar 

  64. 64

    Sterzer, P., Stadler, C., Krebs, A., Kleinschmidt, A. & Poustka, F. Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder. Biol. Psychiatry 57, 7–15 (2005).

    Article  PubMed  Google Scholar 

  65. 65

    Sterzer, P. & Stadler, C. Neuroimaging of aggressive and violent behaviour in children and adolescents. Front. Behav. Neurosci. 3, 35 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  66. 66

    Davidson, R. J., Putnam, K. M. & Larson, C. L. Dysfunction in the neural circuitry of emotion regulation — a possible prelude to violence. Science 289, 591–594 (2000).

    CAS  Article  PubMed  Google Scholar 

  67. 67

    Muehlberger, C. W. Medicolegal aspects of alcohol intoxication. Michigan State Bar J. 35, 38–42 (1956).

    Google Scholar 

  68. 68

    Chiavegatto, S., Quadros, I. M. H., Ambar, G. & Miczek, K. A. Individual vulnerability to escalated aggressive behavior by a low dose of alcohol: decreased serotonin receptor mRNA in the prefrontal cortex of male mice. Genes Brain Behav. 9, 110–119 (2010).

    CAS  Article  PubMed  Google Scholar 

  69. 69

    Giancola, P. R. et al. Men and women, alcohol and aggression. Exp. Clin. Psychopharmacol. 17, 154–164 (2009).

    Article  PubMed  Google Scholar 

  70. 70

    Giancola, P. R. & Zeichner, A. An investigation of gender differences in alcohol-related aggression. J. Stud. Alcohol 56, 573–579 (1995).

    CAS  Article  PubMed  Google Scholar 

  71. 71

    Giancola, P. R. Executive functioning and alcohol-related aggression. J. Abnorm. Psychol. 113, 541–555 (2004).

    Article  PubMed  Google Scholar 

  72. 72

    Parrott, D. J. & Zeichner, A. Effects of alcohol and trait anger on physical aggression in men. J. Stud. Alcohol 63, 196–204 (2002).

    Article  PubMed  Google Scholar 

  73. 73

    Cheong, J. & Nagoshi, C. T. Effects of sensation seeking, instruction set, and alcohol/placebo administration on aggressive behavior. Alcohol 17, 81–86 (1999).

    CAS  Article  PubMed  Google Scholar 

  74. 74

    Giancola, P. R. Difficult temperament, acute alcohol intoxication, and aggressive behavior. Drug Alcohol Depend. 74, 135–145 (2004).

    Article  PubMed  Google Scholar 

  75. 75

    Parrott, D. J. & Giancola, P. R. A further examination of the relation between trait anger and alcohol-related aggression: the role of anger control. Alcohol. Clin. Exp. Res. 28, 855–864 (2004).

    Article  PubMed  Google Scholar 

  76. 76

    Godlaski, A. J. & Giancola, P. R. Executive functioning, irritability, and alcohol-related aggression. Psychol. Addict. Behav. 23, 391–403 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  77. 77

    Giancola, P. R. The moderating effects of dispositional empathy on alcohol-related aggression in men and women. J. Abnorm. Psychol. 112, 275–281 (2003).

    Article  PubMed  Google Scholar 

  78. 78

    Mihic, L., Wells, S., Graham, K., Tremblay, P. F. & Demers, A. Situational and respondent-level motives for drinking and alcohol-related aggression: a multilevel analysis of drinking events in a sample of Canadian University students. Addict. Behav. 34, 264–269 (2009).

    Article  PubMed  Google Scholar 

  79. 79

    Levinson, C. A. & Giancola, P. R. Beliefs about aggression moderate alcohol's effects on aggression. Exp. Clin. Psychopharmacol. 19, 64–74 (2011).

    Article  PubMed  Google Scholar 

  80. 80

    Chermack, S. T. & Taylor, S. P. Alcohol and human physical aggression — pharmacological, versus expectancy effects. J. Stud. Alcohol 56, 449–456 (1995).

    CAS  Article  PubMed  Google Scholar 

  81. 81

    Rohsenow, D. J. & Bachorowski, J. A. Effects of alcohol and expectancies on verbal aggression in men and women. J. Abnorm. Psychol. 93, 418–432 (1984).

    CAS  Article  PubMed  Google Scholar 

  82. 82

    Giancola, P. R. et al. The effects of alcohol and provocation on aggressive behavior in men and women. J. Stud. Alcohol 63, 64–73 (2002).

    Article  PubMed  Google Scholar 

  83. 83

    Taylor, S. P., Schmutte, G. T., Leonard, K. E. & Cranston, J. W. The effects of alcohol and extreme provocation on the use of a highly noxious electric shock. Motiv. Emot. 3, 73–81 (1979).

    CAS  Article  Google Scholar 

  84. 84

    Taylor, S. P., Gammon, C. B. & Capasso, D. R. Aggression as a function of interaction of alcohol and threat. J. Pers. Soc. Psychol. 34, 938–941 (1976).

    CAS  Article  PubMed  Google Scholar 

  85. 85

    Taylor, S. P. & Sears, J. D. The effects of alcohol and persuasive social pressure on human physical aggression. Aggress. Behav. 14, 237–243 (1988).

    Article  Google Scholar 

  86. 86

    Wells, S. & Graham, K. Aggression involving alcohol: relationship to drinking patterns and social context. Addiction 98, 33–42 (2003).

    Article  PubMed  Google Scholar 

  87. 87

    Salomon, R. M., Mazure, C. M., Delgado, P. L., Mendia, P. & Charney, D. S. Serotonin function in aggression — the effect of acute plasma tryptophan depletion in aggressive patients. Biol. Psychiatry 35, 570–572 (1994).

    CAS  Article  PubMed  Google Scholar 

  88. 88

    Dougherty, D. M., Moeller, F. G., Bjork, J. M. & Marsh, D. M. Plasma L-tryptophan depletion and aggression. Adv. Exp. Med. Biol. 467, 57–65 (1999).

    CAS  Article  PubMed  Google Scholar 

  89. 89

    Delgado, P. L. et al. Serotonin and the neurobiology of depression — effects of tryptophan depletion in drug-free depressed-patients. Arch. Gen. Psychiatry 51, 865–874 (1994).

    CAS  Article  PubMed  Google Scholar 

  90. 90

    Cloninger, C. R. Neurogenetic adaptive-mechanisms in alcoholism. Science 236, 410–416 (1987).

    CAS  Article  PubMed  Google Scholar 

  91. 91

    Bohman, M., Cloninger, R., Sigvardsson, S. & Vonknorring, A. L. The genetics of alcoholisms and related disorders. J. Psychiatr. Res. 21, 447–452 (1987).

    CAS  Article  PubMed  Google Scholar 

  92. 92

    Cosgrove, K. P. et al. Dopamine and serotonin transporter availability during acute alcohol withdrawal: effects of comorbid tobacco smoking. Neuropsychopharmacology 34, 2218–2226 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  93. 93

    Heinz, A. et al. A relationship between serotonin transporter genotype and in vivo protein expression and alcohol neurotoxicity. Biol. Psychiatry 47, 643–649 (2000).

    CAS  Article  PubMed  Google Scholar 

  94. 94

    Clarke, H. F., Dalley, J. W., Crofts, H. S., Robbins, T. W. & Roberts, A. C. Cognitive inflexibility after prefrontal serotonin depletion. Science 304, 878–880 (2004).

    CAS  Article  PubMed  Google Scholar 

  95. 95

    Chamberlain, S. R. et al. Neurochemical modulation of response inhibition and probabilistic learning in humans. Science 311, 861–863 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  96. 96

    George, D. T. et al. Fluoxetine treatment of alcoholic perpetrators of domestic violence: a 12-week, double-blind, randomized, placebo-controlled intervention study. J. Clin. Psychiatry 72, 60–65 (2011).

    CAS  Article  PubMed  Google Scholar 

  97. 97

    Dalley, J. W. et al. Nucleus Accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science 315, 1267–1270 (2007).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  98. 98

    van Erp, A. M. M. & Miczek, K. A. Increased accumbal dopamine during daily alcohol consumption and subsequent aggressive behavior in rats. Psychopharmacology 191, 679–688 (2007).

    Article  CAS  PubMed  Google Scholar 

  99. 99

    van Erp, A. M. M. & Miczek, K. A. Aggressive behavior, increased accumbal dopamine, and decreased cortical serotonin in rats. J. Neurosci. 20, 9320–9325 (2000).

    CAS  Article  PubMed  Google Scholar 

  100. 100

    Takahashi, A., Shimamoto, A., Boyson, C. O., Debold, J. F. & Miczek, K. A. GABA(B) receptor modulation of serotonin neurons in the dorsal raphe nucleus and escalation of aggression in mice. J. Neurosci. 30, 11771–11780 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  101. 101

    Faccidomo, S., Bannai, M. & Miczek, K. A. Escalated aggression after alcohol drinking in male mice: dorsal raphe and prefrontal cortex serotonin and 5-HT1B receptors. Neuropsychopharmacology 33, 2888–2899 (2008). A landmark paper that describes a blunted prefrontal serotonin release following 5-HT 1B receptor stimulation in rodents with alcohol-heightened aggression.

  102. 102

    Fish, E. W., McKenzie-Quirk, S. D., Bannai, M. & Miczek, K. A. 5-HT1B receptor inhibition of alcohol-heightened aggression in mice: comparison to drinking and running. Psychopharmacology 197, 145–156 (2008).

    CAS  Article  PubMed  Google Scholar 

  103. 103

    Fink, K. B. & Gothert, M. 5-HT receptor regulation of neurotransmitter release. Pharmacol. Rev. 59, 360–417 (2007).

    CAS  Article  PubMed  Google Scholar 

  104. 104

    Cai, X., Flores-Hernandez, J., Feng, J. & Yan, Z. Activity-dependent bidirectional regulation of GABA(A) receptor channels by the 5-HT4 receptor-mediated signalling in rat prefrontal cortical pyramidal neurons. J. Physiol. 540, 743–759 (2002).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  105. 105

    Clarke, A. S. et al. Rearing experience and biogenic amine activity in infant rhesus monkeys. Biol. Psychiatry 40, 338–352 (1996).

    CAS  Article  PubMed  Google Scholar 

  106. 106

    Jones, G. H., Hernandez, T. D., Kendall, D. A., Marsden, C. A. & Robbins, T. W. Dopaminergic and serotonergic function following isolation rearing in rats: study of behavioral responses and postmortem and in vivo neurochemistry. Pharmacol. Biochem. Behav. 43, 17–35 (1992).

    CAS  Article  PubMed  Google Scholar 

  107. 107

    Higley, J. D., Suomi, S. J. & Linnoila, M. 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, 629–642 (1996).

    CAS  Article  PubMed  Google Scholar 

  108. 108

    Higley, J. D., Suomi, S. J. & Linnoila, M. 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, 643–650 (1996).

    CAS  Article  PubMed  Google Scholar 

  109. 109

    Barr, C. S. et al. Interaction between serotonin transporter gene variation and rearing condition in alcohol preference and consumption in female primates. Arch. Gen. Psychiatry 61, 1146–1152 (2004).

    CAS  Article  PubMed  Google Scholar 

  110. 110

    Heinz, A. et al. In vivo association between alcohol intoxication, aggression, and serotonin transporter availability in nonhuman primates. Am. J. Psychiatry 155, 1023–1028 (1998).

    CAS  Article  PubMed  Google Scholar 

  111. 111

    Lesch, K. P. et al. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274, 1527–1531 (1996).

    CAS  Article  PubMed  Google Scholar 

  112. 112

    Bennett, A. J. et al. Early experience and serotonin transporter gene variation interact to influence primate CNS function. Mol. Psychiatry 7, 118–122 (2002).

    CAS  Article  PubMed  Google Scholar 

  113. 113

    Heinz, A. et al. Depletion and restoration of endogenous monoamines affects beta-CIT binding to serotonin but not dopamine transporters in non-human primates. J. Neural Transm. 29–38 (2004).

  114. 114

    Ichise, M. et al. Effects of early life stress on [C-11] DASB positron emission tomography imaging of serotonin transporters in adolescent peer- and mother-reared rhesus monkeys. J. Neurosci. 26, 4638–4643 (2006).

    CAS  Article  PubMed  Google Scholar 

  115. 115

    Hummerich, R. et al. DASB - in vitro binding characteristics on human recombinant monoamine transporters with regard to its potential as positron emission tomography (PET) tracer. J. Neurochem. 90, 1218–1226 (2004).

    CAS  Article  PubMed  Google Scholar 

  116. 116

    Doudet, D. et al. Cerebral glucose-metabolism, Csf 5-hiaa levels, and aggressive behavior in rhesus monkeys. Am. J. Psychiatry 152, 1782–1787 (1995).

    CAS  Article  PubMed  Google Scholar 

  117. 117

    Heinz, A., Mann, K., Weinberger, D. R. & Goldman, D. Serotonergic dysfunction, negative mood states, and response to alcohol. Alcohol. Clin. Exp. Res. 25, 487–495 (2001).

    CAS  Article  PubMed  Google Scholar 

  118. 118

    Schuckit, M. A. Low level of response to alcohol as a predictor of future alcoholism. Am. J. Psychiatry 151, 184–189 (1994).

    CAS  Article  PubMed  Google Scholar 

  119. 119

    Hinckers, A. S. et al. Low level of response to alcohol as associated with serotonin transporter genotype and high alcohol intake in adolescents. Biol. Psychiatry 60, 282–287 (2006).

    CAS  Article  PubMed  Google Scholar 

  120. 120

    Heinz, A. et al. Serotonin transporter availability correlates with alcohol intake in non-human primates. Mol. Psychiatry 8, 231–234 (2003).

    CAS  Article  PubMed  Google Scholar 

  121. 121

    Johnson, E. O., vandenBree, M. B. M. & Pickens, R. W. Subtypes of alcohol-dependent men: A typology based on relative genetic and environmental loading. Alcohol. Clin. Exp. Res. 20, 1472–1480 (1996).

    CAS  Article  PubMed  Google Scholar 

  122. 122

    Higley, J. D., Suomi, S. J. & Linnoila, M. 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, 551–556 (1991).

    CAS  Article  PubMed  Google Scholar 

  123. 123

    Higley, J. D. et al. Paternal and maternal genetic and environmental contributions to cerebrospinal-fluid monoamine metabolites in rhesus monkeys (Macaca mulatta). Arch. Gen. Psychiatry 50, 615–623 (1993).

    CAS  Article  PubMed  Google Scholar 

  124. 124

    Oxenstierna, G. et al. Concentrations of monoamine metabolites in the cerebrospinal-fluid of twins and unrelated individuals — a genetic-study. J. Psychiatric Res. 20, 19–29 (1986).

    CAS  Article  Google Scholar 

  125. 125

    Virkkunen, M. et al. Personality profiles and state aggressiveness in finnish alcoholic, violent offenders, fire setters, and healthy volunteers. Arch. Gen. Psychiatry 51, 28–33 (1994).

    CAS  Article  PubMed  Google Scholar 

  126. 126

    Bohman, M., Cloninger, C. R., Sigvardsson, S. & Vonknorring, A. L. Predisposition to petty criminality in Swedish adoptees. I. Genetic and environmental heterogeneity. Arch. Gen. Psychiatry 39, 1233–1241 (1982).

    CAS  Article  PubMed  Google Scholar 

  127. 127

    Carey, G. Aggression and Violence: Genetic, Neurobiological, and Biosocial Perspectives. (eds Stoff, D. M. & Cairns, R. B.) 3–21 (Lawrence Earlbaum Associates, New Jersey, 1996).

    Google Scholar 

  128. 128

    Gray, J. A. The neuropsychology of Anxiety. An Inquiry into the Function of the Septo-hippocampal System. (Oxford University Press, New York, 1982).

    Google Scholar 

  129. 129

    Mann, J. J. et al. Attempted suicide characteristics and cerebrospinal fluid amine metabolites in depressed inpatients. Neuropsychopharmacology 15, 576–586 (1996).

    CAS  Article  PubMed  Google Scholar 

  130. 130

    Kruesi, M. J. P. et al. Cerebrospinal fluid monoamine metabolites, aggression, and impulsivity in disruptive behavior disorders of children and adolescents. Arch. Gen. Psychiatry 47, 419–426 (1990).

    CAS  Article  PubMed  Google Scholar 

  131. 131

    Linnoila, M. et al. Low Cerebrospinal fluid 5-hydroxyindoleacetic acid concentration differentiates impulsive from nonimpulsive violent behavior. Life Sciences 33, 2609–2614 (1983).

    CAS  Article  PubMed  Google Scholar 

  132. 132

    Brunner, H. G., Nelen, M., Breakefield, X. O., Ropers, H. H. & Vanoost, B. A. Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science 262, 578–580 (1993).

    CAS  Article  PubMed  Google Scholar 

  133. 133

    Saraceno, L., Munafo, M., Heron, J., Craddock, N. & van den Bree, M. B. M. Genetic and non-genetic influences on the development of co-occurring alcohol problem use and internalizing symptomatology in adolescence: a review. Addiction 104, 1100–1121 (2009).

    Article  PubMed  Google Scholar 

  134. 134

    Lu, R. B., Lin, W. W., Lee, J. F., Ko, H. C. & Shih, J. C. Neither antisocial personality disorder nor antisocial alcoholism is associated with the MAO-A gene in Han Chinese males. Alcohol. Clin. Exp. Res. 27, 889–893 (2003).

    CAS  Article  PubMed  Google Scholar 

  135. 135

    Sabol, S. Z., Hu, S. & Hamer, D. A functional polymorphism in the monoamine oxidase A gene promoter. Hum. Genet. 103, 273–279 (1998).

    CAS  Article  PubMed  Google Scholar 

  136. 136

    Raine, A. From genes to brain to antisocial behavior. Curr. Dir. Psychol. Sci. 17, 323–328 (2008).

    Article  Google Scholar 

  137. 137

    Eisenberger, N. I., Way, B. M., Taylor, S. E., Welch, W. T. & Lieberman, M. D. Understanding genetic risk for aggression: clues from the brain's response to social exclusion. Biol. Psychiatry 61, 1100–1108 (2007).

    Article  PubMed  Google Scholar 

  138. 138

    Meyer-Lindenberg, A. et al. Neural mechanisms of genetic risk for impulsivity and violence in humans. Proc. Natl Acad. Sci. USA 103, 6269–6274 (2006). This study investigated the effect of the MAOA genetic polymorphism on brain structure and functions, and found differences in limbic circuitry for emotion regulation and cognitive control that may be involved in the association of MAOA with impulsive aggression.

    CAS  Article  PubMed  Google Scholar 

  139. 139

    Buckholtz, J. W. et al. Genetic variation in MAOA modulates ventromedial prefrontal circuitry mediating individual differences in human personality. Mol. Psychiatry 13, 313–324 (2008).

    CAS  Article  PubMed  Google Scholar 

  140. 140

    Caspi, A. et al. Role of genotype in the cycle of violence in maltreated children. Science 297, 851–854 (2002). A landmark study providing evidence for a gene–environment interaction in humans that is linked to violence in the MAOA VNTR genetic polymorphism.

    CAS  Article  PubMed  Google Scholar 

  141. 141

    Kim-Cohen, J. et al. MAOA, maltreatment, and gene–environment interaction predicting children's mental health: new evidence and a meta-analysis. Mol. Psychiatry 11, 903–913 (2006).

    CAS  Article  PubMed  Google Scholar 

  142. 142

    Reif, A. et al. Nature and nurture predispose to violent behavior: serotonergic genes and adverse childhood environment. Neuropsychopharmacology 32, 2375–2383 (2007).

    CAS  Article  PubMed  Google Scholar 

  143. 143

    Pezawas, L. et al. 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nature Neurosci. 8, 828–834 (2005).

    CAS  Article  PubMed  Google Scholar 

  144. 144

    Heinz, A. et al. Amygdala-prefrontal coupling depends on a genetic variation of the serotonin transporter. Nature Neurosci. 8, 20–21 (2005).

    CAS  Article  PubMed  Google Scholar 

  145. 145

    Schwandt, M. L. et al. Gene–environment interactions and response to social intrusion in male and female rhesus macaques. Biol. Psychiatry 67, 323–330 (2010). A non-human primate study showing a genotype–environment interaction. Increased aggressiveness was found in male rhesus monkeys that were exposed to early social adversity and carry a serotonin transporter loss-of-function allele ( 5-HTTLPR S allele).

    Article  PubMed  Google Scholar 

  146. 146

    Freedman, N. M. T. et al. In vivo measurement of brain monoamine oxidase B occupancy by rasagiline, using C-11-L-deprenyl and PET. J. Nucl. Med. 46, 1618–1624 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  147. 147

    Bevilacqua, L. et al. A population-specific HTR2B stop codon predisposes to severe impulsivity. Nature 468, 1061–1066 (2010). This study shows that in rodents, knockout of the 5-HT 2B gene is associated with increased impulsivity. In humans, a 5-HT 2B stop codon was associated with high impulsivity in Finnish violent offenders who mainly acted out when alcohol-intoxicated.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  148. 148

    Schuckit, M. A. et al. Selective genotyping for the role of 5-HT2A, 5-HT2C, and GABA(alpha 6) receptors and the serotonin transporter in the level of response to alcohol: a pilot study. Biol. Psychiatry 45, 647–651 (1999).

    CAS  Article  PubMed  Google Scholar 

  149. 149

    Moeller, F. G., Barratt, E. S., Dougherty, D. M., Schmitz, J. M. & Swann, A. C. Psychiatric aspects of impulsivity. Am. J. Psychiatry 158, 1783–1793 (2001).

    CAS  Article  PubMed  Google Scholar 

  150. 150

    Bechara, A. Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nature Neurosci. 8, 1458–1463 (2005).

    CAS  Article  PubMed  Google Scholar 

  151. 151

    Rubio, G. et al. The role of behavioral impulsivity in the development of alcohol dependence: a 4-year follow-up study. Alcohol. Clin. Exp. Res., 32, 1681–1687 (2008).

    Article  PubMed  Google Scholar 

  152. 152

    Dom, G., D'Haene, P., Hulstijn, W. & Sabbe, B. Impulsivity in abstinent early- and late-onset alcoholics: differences in self-report measures and a discounting task. Addiction 101, 50–59 (2006).

    CAS  Article  PubMed  Google Scholar 

  153. 153

    Lejoyeux, M., Feuche, N., Loi, S., Solomon, J. & Ades, J. Impulse-control disorders in alcoholics are related to sensation seeking and not to impulsivity. Psychiatry Res. 81, 149–155 (1998).

    CAS  Article  PubMed  Google Scholar 

  154. 154

    Volkow, N. D. et al. Decreases in dopamine receptors but not in dopamine transporters in alcoholics. Alcohol. Clin. Exp. Res. 20, 1594–1598 (1996).

    CAS  Article  PubMed  Google Scholar 

  155. 155

    Heinz, A. et al. Psychopathological and behavioral correlates of dopaminergic sensitivity in alcohol-dependent patients. Arch. Gen. Psychiatry 53, 1123–1128 (1996).

    CAS  Article  PubMed  Google Scholar 

  156. 156

    Heinz, A. et al. Correlation between dopamine D(2) receptors in the ventral striatum and central processing of alcohol cues and craving. Am. J. Psychiatry 161, 1783–1789 (2004).

    Article  PubMed  Google Scholar 

  157. 157

    Rommelspacher, H., Raeder, C., Kaulen, P. & Bruning, G. Adaptive changes of dopamine-D(2) receptors in rat brain following ethanol withdrawal: a quantitative autoradiographic investigation. Alcohol 9, 355–362 (1992).

    CAS  Article  PubMed  Google Scholar 

  158. 158

    Beck, A. et al. Ventral striatal activation during reward anticipation correlates with impulsivity in alcoholics. Biol. Psychiatry 66, 734–742 (2009). This study in human patients with alcohol dependence and healthy controls shows that neuronal activation elicited by reward anticipation in the ventral striatum is blunted in detoxified patients. Low ventral striatal activation was associated with increased impulsivity in both patients and controls.

    CAS  Article  PubMed  Google Scholar 

  159. 159

    Hariri, A. R. et al. Preference for immediate over delayed rewards is associated with magnitude of ventral striatal activity. J. Neurosci. 26, 13213–13217 (2006).

    CAS  Article  PubMed  Google Scholar 

  160. 160

    Corte, C. M. & Sommers, M. S. Alcohol and risky behaviors. Annu. Rev. Nurs. Res. 23, 327–360 (2005).

    Article  PubMed  Google Scholar 

  161. 161

    Park, S. Q. et al. Prefrontal cortex fails to learn. from reward prediction errors in alcohol dependence. J. Neurosci. 30, 7749–7753 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  162. 162

    Edwards, D. W., Scott, C. L., Yarvis, R. M., Paizis, C. L. & Panizzon, M. S. Impulsiveness, impulsive aggression, personality disorder, and spousal violence. Violence Vict. 18, 3–14 (2003).

    Article  PubMed  Google Scholar 

  163. 163

    McCloskey, M. S., Lee, R., Berman, M. E., Noblett, K. L. & Coccaro, E. F. The relationship between impulsive verbal aggression and intermittent explosive disorder. Aggress. Behav. 34, 51–60 (2008).

    Article  PubMed  Google Scholar 

  164. 164

    Barratt, E. S. Impulsivity, behavioral dyscontrol, and conscious awareness. Behav. Mot. Contr. Psychiatr. Disord. S04, 217 (1982).

    Google Scholar 

  165. 165

    Dougherty, D. M., Marsh-Richard, D. M., Hatzis, E. S., Nouvion, S. O. & Mathias, C. W. A test of alcohol dose effects on multiple behavioral measures of impulsivity. Drug Alcohol Depend. 96, 111–120 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  166. 166

    Marczinski, C. A., Combs, S. W. & Fillmore, M. T. Increased sensitivity to the disinhibiting effects of alcohol in binge drinkers. Psychol. Addict. Behav. 21, 346–354 (2007).

    Article  PubMed  Google Scholar 

  167. 167

    Higley, J. D. & Linnoila, M. Low central nervous system serotonergic activity is traitlike and correlates with impulsive behavior. A nonhuman primate model investigating genetic and environmental influences on neurotransmission. Ann. NY Acad. Sci. 836, 39–56 (1997).

    CAS  Article  PubMed  Google Scholar 

  168. 168

    Lemarquand, D., Pihl, R. O. & Benkelfat, C. Serotonin and alcohol intake, abuse, and dependence: findings of animal studies. Biol. Psychiatry 36, 395–421 (1994).

    CAS  Article  PubMed  Google Scholar 

  169. 169

    Giancola, P. R. & Moselhy, H. F. Executive cognitive functioning in alcohol use disorders. Recent Dev. Alcohol. 14, 227–251 (1998).

    CAS  Article  PubMed  Google Scholar 

  170. 170

    Loeber, S. et al. Effects of repeated withdrawal from alcohol on recovery of cognitive impairment under abstinence and rate of relapse. Alcohol Alcohol. 45, 541–547 (2010).

    CAS  Article  PubMed  Google Scholar 

  171. 171

    Ratti, M. T., Bo, P., Giardini, A. & Soragna, D. Chronic alcoholism and the frontal lobe: which executive functions are impaired? Acta Neurol. Scand. 105, 276–281 (2002).

    CAS  Article  PubMed  Google Scholar 

  172. 172

    Sullivan, E. V., Rosenbloom, M. J. & Pfefferbaum, A. Pattern of motor and cognitive deficits in detoxified alcoholic men. Alcohol. Clin. Exp. Res. 24, 611–621 (2000).

    CAS  Article  PubMed  Google Scholar 

  173. 173

    Moselhy, H. F., Georgiou, G. & Kahn, A. Frontal lobe changes in alcoholism: a review of the literature. Alcohol Alcohol. 36, 357–368 (2001).

    CAS  Article  PubMed  Google Scholar 

  174. 174

    Siever, L. J. et al. d,l-fenfluramine response in impulsive personality disorder assessed with [F-18]fluorodeoxyglucose positron emission tomography. Neuropsychopharmacology 20, 413–423 (1999).

    CAS  Article  PubMed  Google Scholar 

  175. 175

    Raine, A. et al. Reduced prefrontal and increased subcortical brain functioning assessed using positron emission tomography in predatory and affective murderers. Behav. Sci. Law 16, 319–332 (1998).

    CAS  Article  PubMed  Google Scholar 

  176. 176

    Heinz, A. et al. Reduced central serotonin transporters in alcoholism. Am. J. Psychiatry 155, 1544–1549 (1998).

    CAS  Article  PubMed  Google Scholar 

  177. 177

    Anderson, G. M. et al. Time course of the effects of the serotonin-selective reuptake inhibitor sertraline on central and peripheral serotonin neurochemistry in the rhesus monkey. Psychopharmacology 178, 339–346 (2005).

    CAS  Article  PubMed  Google Scholar 

  178. 178

    Knutson, B. et al. Selective alteration of personality and social behavior by serotonergic intervention. Am. J. Psychiatry 155, 373–379 (1998).

    CAS  Article  PubMed  Google Scholar 

  179. 179

    Knutson, B., Panksepp, J. & Pruitt, D. Effects of fluoxetine on play dominance in juvenile rats. Aggress. Behav. 22, 297–307 (1996).

    CAS  Article  Google Scholar 

  180. 180

    Raleigh, M. A. & McGuire, M. T. Kynurenine and Serotonin Pathways. Progress in Tryptophan Research. (eds Schwarcz, R., Young, S. N. & Brown, R. R.) 289–298 (Plenum Press, New York, london, 1991).

    Google Scholar 

  181. 181

    Knutson, B., Panksepp, J., Narayanana, T. K. & Rossi, J. Early central serotonin damage increases “anxious” behaviors in juvenile rats. Soc. Neurosci. 22, 446 (1996).

    Google Scholar 

  182. 182

    Phillips, J. P. & Giancola, P. R. Experimentally induced anxiety attenuates alcohol-related aggression in men. Exp. Clin. Psychopharmacol. 16, 43–56 (2008).

    Article  PubMed  Google Scholar 

  183. 183

    Petty, F., Kramer, G., Wilson, L. & Jordan, S. In vivo serotonin release and learned helplessness. Psychiatry Res. 52, 285–293 (1994).

    CAS  Article  PubMed  Google Scholar 

  184. 184

    Glenn, A. L. & Raine, A. The neurobiology of psychopathy. Psychiatr. Clin. North Am. 31, 463–475 (2008).

    Article  PubMed  Google Scholar 

  185. 185

    Luria, A. Higher Cortical functions in Man. (Basic Books, New York, 1980).

    Google Scholar 

  186. 186

    Giancola, P. R. The underlying role of aggressivity in the relation between executive functioning and alcohol consumption. Addict. Behav. 32, 765–783 (2007).

    Article  PubMed  Google Scholar 

  187. 187

    Morgan, A. B. & Lilienfeld, S. O. A meta-analytic review of the relation between antisocial behavior and neuropsychological measures of executive function. Clin. Psychol. Rev. 20, 113–136 (2000).

    CAS  Article  PubMed  Google Scholar 

  188. 188

    MacAndrews, C. & Edgerton, R. Drunken Comportment. (Aldine, Chicago. 1969).

    Google Scholar 

  189. 189

    Goldman, M. S., Darkes, J. & Del Boca, F. K. How Expectancies Shape Experience. (ed. Kirch, L.) 233–262 (American Psychological Association, Washington D.C., 1999).

    Google Scholar 

  190. 190

    Goldman, M. S., Del Boca, F. K. & Darkes, J. Psychological Theories Of Drinking And Alcoholism. (eds Leonard, K. E. & Blane, H. T.) 203–246 (Guilford Press, New York, 1999).

    Google Scholar 

  191. 191

    Jones, B. T., Corbin, W. & Fromme, K. A review of expectancy theory and alcohol consumption. Addiction 96, 57–72 (2001).

    CAS  Article  PubMed  Google Scholar 

  192. 192

    Zucker, R. A., Kincaid, S. B., Fitzgerald, H. E. & Bingham, C. R. Alcohol schema acquisition in preschoolers: differences between children of alcoholics and children of nonalcoholics. Alcohol. Clin. Exp. Res. 19, 1011–1017 (1995).

    CAS  Article  PubMed  Google Scholar 

  193. 193

    Bandura, A. Social Learning Theory. (Prentice-Hall, New Jersey, 1977).

    Google Scholar 

  194. 194

    Maisto, S. A., Carey, K. B. & Bradizza, C. M. Psychological Theories of Drinking and Alcoholism. (eds Leonard, K. E. & Blane, H. T.) 106–163 (Guilford Press, New York, 1999).

    Google Scholar 

  195. 195

    Leigh, B. C. & Stacy, A. W. Individual differences in memory associations involving the positive and negative outcomes of alcohol use. Psychol. Addict. Behav. 12, 39–46 (1998).

    Article  Google Scholar 

  196. 196

    Tiffany, S. T. A Cognitive model of drug urges and drug-use behavior: role of automatic and nonautomatic processes. Psychol. Rev. 97, 147–168 (1990).

    CAS  Article  PubMed  Google Scholar 

  197. 197

    Bartholow, B. D. & Heinz, A. Alcohol and aggression without consumption. Alcohol cues, aggressive thoughts, and hostile perception bias. Psychol. Sci. 17, 30–37 (2006).

    Article  PubMed  Google Scholar 

  198. 198

    Buckholtz, J. W. & Meyer-Lindenberg, A. MAOA and the neurogenetic architecture of human aggression. Trends Neurosci. 31, 120–129 (2008).

    CAS  Article  PubMed  Google Scholar 

  199. 199

    Steele, C. M. & Josephs, R. A. Alcohol myopia. Its prized and dangerous effects. Am. Psychol. 45, 921–933 (1990).

    CAS  Article  PubMed  Google Scholar 

  200. 200

    Steele, C. M. & Southwick, L. Alcohol and social behavior I: The psychology of drunken excess. J. Pers. Soc. Psychol. 48, 18–34 (1985).

    CAS  Article  PubMed  Google Scholar 

  201. 201

    Giancola, P. R. & Corman, M. D. Alcohol and aggression: a test of the attention-allocation model. Psychol. Sci. 18, 649–655 (2007).

    Article  PubMed  Google Scholar 

  202. 202

    Nasby, W., Hayden, B. & Depaulo, B. M. Attributional bias among aggressive boys to interpret unambiguous social-stimuli as displays of hostility. J. Abnorm. Psychol. 89, 459–468 (1980).

    CAS  Article  PubMed  Google Scholar 

  203. 203

    Hull, J. G. A self-awareness model of the causes and effects of alcohol-consumption. J. Abnorm. Psychol. 90, 586–600 (1981).

    CAS  Article  PubMed  Google Scholar 

  204. 204

    Sayette, M. A., Wilson, G. T. & Elias, M. J. Alcohol and aggression: a social information-processing analysis. J. Stud. Alcohol 54, 399–407 (1993).

    CAS  Article  PubMed  Google Scholar 

  205. 205

    Pihl, R. O., Peterson, J. B. & Lau, M. A. A biosocial model of the alcohol-aggression relationship. J. Stud. Alcohol Suppl. 11, 28–139 (1993).

    Google Scholar 

  206. 206

    Hoaken, P. N. S., Campbell, T., Stewart, S. H. & Pihl, R. O. Effects of alcohol on cardiovascular reactivity and the mediation of aggressive behaviour in adult men and women. Alcohol Alcohol. 38, 84–92 (2003).

    Article  PubMed  Google Scholar 

  207. 207

    Lange, J. E. Alcohol's effect on aggression identification: a two-channel theory. Psychol. Addict. Behav. 16, 47–55 (2002).

    Article  PubMed  Google Scholar 

  208. 208

    Wiers, R. W., Beckers, L., Houben, K. & Hofmann, W. A short fuse after alcohol: implicit power associations predict aggressiveness after alcohol consumption in young heavy drinkers with limited executive control. Pharmacol. Biochem. Behav. 93, 300–305 (2009).

    CAS  Article  PubMed  Google Scholar 

  209. 209

    Deutsch, R. & Strack, F. Handbook on Implicit Cognition and Addiction. (eds Wiers, R. W. and Stacy, A. W.) 45–57 (Sage publishers, California, 2006).

    Google Scholar 

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Acknowledgements

The authors were supported in part by the Deutsche Forschungsgemeinschaft (Excellence Cluster EXC 257 & STE 1430/2-1), the Centre for Integrated Life Sciences (CILS) and the US National Institute on Alcohol Abuse and Alcoholism (F31 AA018918). This work was also supported by the German Federal Ministry of Education and Research (Bundesministerium für Bildung und Forschung; 01QG87164 and NGFN Plus, and 01GS08152).

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Glossary

Alcohol outcome expectancies

Predictions or beliefs about the social, cognitive and affective consequences of alcohol consumption that are shaped by social learning and personal experience with alcohol.

Bandura's social learning theory

A theory that proposes that learning takes place in a social context in which we can learn from observing others, and that this learning can occur without a change in behaviour.

Alcohol schema

The theoretical structure in which information about alcohol (for example, experience and beliefs) is organized and stored in memory.

Go/No-Go task

A task that requires participants to press a key in response to one type of stimulus and not to press a key when another stimulus type occurs. Go/No-Go tasks are typically used to assess cognitive inhibitory control of behaviour.

Reward expectation

Reward expectation describes an anticipatory processing in the face of upcoming positive reinforcement (a reward).

Delay discounting

The reduced ability to choose larger but delayed rewards compared with smaller but earlier rewards (seen as an index of impulsive tendencies).

Fenfluramine

A pharmacological drug that releases serotonin; it reverses reuptake by serotonin transporters and disrupts vesicular storage of serotonin.

'Hot' and 'cold' systems of emotion regulation

Neural systems implicated in emotion regulation; the cold system refers to the rational and logical reasoning usually conducted under low emotion and arousal, whereas the hot system is implicated in decision making under high levels of emotion and arousal that occur in the immediate situation.

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Heinz, A., Beck, A., Meyer-Lindenberg, A. et al. Cognitive and neurobiological mechanisms of alcohol-related aggression. Nat Rev Neurosci 12, 400–413 (2011). https://doi.org/10.1038/nrn3042

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