The neural correlates of alcohol-related aggression

  • Thomas F. Denson
  • Kate A. Blundell
  • Timothy P. Schofield
  • Mark M. Schira
  • Ulrike M. Krämer
Article
First Online:

Abstract

Alcohol intoxication is implicated in approximately half of all violent crimes. Over the past several decades, numerous theories have been proposed to account for the influence of alcohol on aggression. Nearly all of these theories imply that altered functioning in the prefrontal cortex is a proximal cause. In the present functional magnetic resonance imaging (fMRI) experiment, 50 healthy young men consumed either a low dose of alcohol or a placebo and completed an aggression paradigm against provocative and nonprovocative opponents. Provocation did not affect neural responses. However, relative to sober participants, during acts of aggression, intoxicated participants showed decreased activity in the prefrontal cortex, caudate, and ventral striatum, but heightened activation in the hippocampus. Among intoxicated participants, but not among sober participants, aggressive behavior was positively correlated with activation in the medial and dorsolateral prefrontal cortex. These results support theories that posit a role for prefrontal cortical dysfunction as an important factor in intoxicated aggression.

Keywords

Alcohol Aggression Prefrontal cortex fMRI 
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Supplementary material

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References

  1. Achterberg, M., van Duijvenvoorde, A. C., Bakermans-Kranenburg, M. J., & Crone, E. A. (2016). Control your anger! The neural basis of aggression regulation in response to negative social feedback. Social Cognitive and Affective Neuroscience, 11, 712–720.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aiken, L. S., West, S. G., & Reno, R. R. (1991). Multiple regression: Testing and interpreting interactions. Thousand Oaks, CA: Sage.Google Scholar
  3. Anderson, B. M., Stevens, M. C., Meda, S. A., Jordan, K., Calhoun, V. D., & Pearlson, G. D. (2011). Functional imaging of cognitive control during acute alcohol intoxication. Alcoholism: Clinical and Experimental Research, 35, 156–165.CrossRefGoogle Scholar
  4. Bartholow, B. D., & Heinz, A. (2006). Alcohol and aggression without consumption alcohol cues, aggressive thoughts, and hostile perception bias. Psychological Science, 17(1), 30–37.CrossRefPubMedGoogle Scholar
  5. Beyer, F., Münte, T. F., Erdmann, C., & Krämer, U. M. (2014). Emotional reactivity to threat modulates activity in mentalizing network during aggression. Social Cognitive and Affective Neuroscience, 9(10), 1552–1560.CrossRefPubMedGoogle Scholar
  6. Buckholtz, J. W., Martin, J. W., Treadway, M. T., Jan, K., Zald, D. H., Jones, O., & Marois, R. (2015). From blame to punishment: Disrupting prefrontal cortex activity reveals norm enforcement mechanisms. Neuron, 87(6), 1369–1380.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bushman, B. J. (1993). Human aggression while under the influence of alcohol and other drugs: An integrative research review. Current Directions in Psychological Science, 2, 148–151.CrossRefGoogle Scholar
  8. Bushman B. J., & Cooper H. (1990). Effects of alcohol on human aggression: An integrative research review. Psychological Bulletin, 107, 341–354.CrossRefPubMedGoogle Scholar
  9. Buss, A. H., & Perry, M. P. (1992). The Aggression Questionnaire. Journal of Personality and Social Psychology, 63, 452–459.CrossRefPubMedGoogle Scholar
  10. Cherek, D. R. (1981). Effects of smoking different doses of nicotine on human aggressive behavior. Psychopharmacology, 75, 339–345.CrossRefPubMedGoogle Scholar
  11. Chester, D. S., & DeWall, C. N. (2016). The pleasure of revenge: Retaliatory aggression arises from a neural imbalance toward reward. Social Cognitive and Affective Neuroscience, 11, 1173–1182.CrossRefPubMedGoogle Scholar
  12. Chester, D. S., Eisenberger, N. I., Pond, R. S., Richman, S. B., Bushman, B. J., & DeWall, C. N. (2013). The interactive effect of social pain and executive functioning on aggression: An fMRI experiment. Social Cognitive and Affective Neuroscience, 9, 699–704.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dambacher, F., Sack, A. T., Lobbestael, J., Arntz, A., Brugman, S., & Schuhmann, T. (2015a). Out of control: Evidence for anterior insula involvement in motor impulsivity and reactive aggression. Social Cognitive and Affective Neuroscience, 10(4), 508–516.CrossRefPubMedGoogle Scholar
  14. Dambacher, F., Schuhmann, T., Lobbestael, J., Arntz, A., Brugman, S., & Sack, A. T. (2015b). Reducing proactive aggression through non-invasive brain stimulation. Social Cognitive and Affective Neuroscience, 10, 1303–1309.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Denson, T. F., Aviles, F. E., Pollock, V. E., Earleywine, M., Vasquez, E. A., & Miller, N. (2008). The effects of alcohol and the salience of aggressive cues on triggered displaced aggression. Aggressive Behavior, 34(1), 25–33.CrossRefPubMedGoogle Scholar
  16. Denson, T. F., DeWall, C. N., & Finkel, E. J. (2012). Self-control and aggression. Current Directions in Psychological Science, 21, 20–25.CrossRefGoogle Scholar
  17. Denson, T. F., Pedersen, W. C., Ronquillo, J., & Nandy, A. S. (2009). The angry brain: Neural correlates of anger, angry rumination, and aggressive personality. Journal of Cognitive Neuroscience, 21, 734–744.CrossRefPubMedGoogle Scholar
  18. Duke, A. A., Giancola, P. R., Morris, D. H., Holt, J. C., & Gunn, R. L. (2011). Alcohol dose and aggression: Another reason why drinking more is a bad idea. Journal of Studies on Alcohol and Drugs, 72, 34–43.Google Scholar
  19. Easdon, C. M., & Vogel-Sprott, M. (2000). Alcohol and behavioral control: Impaired response inhibition and flexibility in social drinkers. Experimental Clinical Psychopharmacology, 8, 387–394.CrossRefPubMedGoogle Scholar
  20. Emmerling, F., Schuhmann, T., Lobbestael, J., Arntz, A., Brugman, S., & Sack, A. T. (2016). The role of the insular cortex in retaliation. PLOS ONE, 11(4), e0152000.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Fals-Stewart, W., Leonard, K. E., & Birchler, G. R. (2005). The occurrence of male-to-female intimate partner violence on days of men’s drinking: The moderating effects of antisocial personality disorder. Journal of Consulting and Clinical Psychology, 73, 239–248.CrossRefPubMedGoogle Scholar
  22. Finkel, E. J., & Hall, A. N. (2017). The I3 model: A metatheoretical framework for understanding aggression. Current Opinion in Psychology, 19, 125–130.  https://doi.org/10.1016/j.copsyc.2017.03.013 CrossRefPubMedGoogle Scholar
  23. Finn, P. R., Justus, A., Mazas, C. & Steinmetz, J. E. (1999). 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.CrossRefPubMedGoogle Scholar
  24. Foran, H. M., & O’Leary, K. D. (2008). Alcohol and intimate partner violence: A meta-analytic review. Clinical Psychology Review, 28(7), 1222–1234.CrossRefPubMedGoogle Scholar
  25. Gan, G., Guevara, A., Marxen, M., Neumann, M., Jünger, E., Kobiella, A., ... & Smolka, M. N. (2014). Alcohol-induced impairment of inhibitory control is linked to attenuated brain responses in right fronto-temporal cortex. Biological Psychiatry, 76(9), 698–707.Google Scholar
  26. Gan, G., Sterzer, P., Marxen, M., Zimmermann, U. S., & Smolka, M. N. (2015). Neural and behavioral correlates of alcohol-induced aggression under provocation. Neuropsychopharmacology, 40, 2886–2896.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Giancola, P. R. (2000). Executive functioning: A conceptual framework for alcohol-related aggression. Experimental and Clinical Psychopharmacology, 8, 576.CrossRefPubMedGoogle Scholar
  28. Giancola, P. R., Josephs, R. A., Parrott, D. J., & Duke, A. A. (2010). Alcohol myopia revisited clarifying aggression and other acts of disinhibition through a distorted lens. Perspectives on Psychological Science, 5, 265–278.CrossRefPubMedGoogle Scholar
  29. Gorka, S. M., Fitzgerald, D. A., King, A. C., & Phan, K. L. (2013). Alcohol attenuates amygdala–frontal connectivity during processing social signals in heavy social drinkers. Psychopharmacology, 229, 141–154.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Graham, K. (1980). Theories of intoxicated aggression. Canadian Journal of Behavioural Science/Revue canadienne des sciences du comportement, 12, 141–158.CrossRefGoogle Scholar
  31. Guillot, C. R., Fanning, J. R., Bullock, J. S., McCloskey, M. S., & Berman, M. E. (2010). Effects of alcohol on tests of executive functioning in men and women: A dose response examination. Experimental Clinical Psychopharmacology, 18, 409–417.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Heinz, A. J., Beck, A., Meyer-Lindenberg, A., Sterzer, P., & Heinz, A. (2011). Cognitive and neurobiological mechanisms of alcohol-related aggression. Nature Reviews Neuroscience, 12, 400–413.CrossRefPubMedGoogle Scholar
  33. Henke, K., Buck, A., Weber, B., & Wieser, H. G. (1997). Human hippocampus establishes associations in memory. Hippocampus, 7, 249–256.CrossRefPubMedGoogle Scholar
  34. Hoaken, P. N., & Stewart, S. H. (2003). Drugs of abuse and the elicitation of human aggressive behavior. Addictive Behaviors, 28(9), 1533–1554.CrossRefPubMedGoogle Scholar
  35. Hull, J., & Bond, C. (1986). Social and behavioral consequences of alcohol consumption and expectancy: A meta-analysis. Psychological Bulletin, 99, 347–360.CrossRefPubMedGoogle Scholar
  36. Ito, T., Miller, N., & Pollock, V. (1996). Alcohol and aggression: A meta-analysis on the moderating effects of inhibitory cues, triggering events, and self-focused attention. Psychological Bulletin, 120, 60–82.CrossRefPubMedGoogle Scholar
  37. Kareken, D. A., Liang, T., Wetherill, L., Dzemidzic, M., Bragulat, V., Cox, C., ... & Foroud, T. (2010). A polymorphism in GABRA2 is associated with the medial frontal response to alcohol cues in an fMRI study. Alcoholism: Clinical and Experimental Research, 34(12), 2169–2178.Google Scholar
  38. Kose, S., Steinberg, J. L., Moeller, F. G., Gowin, J. L., Zuniga, E., Kamdar, Z. N., ... & Lane, S. D. (2015). Neural correlates of impulsive aggressive behavior in subjects with a history of alcohol dependence. Behavioral neuroscience, 129(2), 183–196.Google Scholar
  39. Krämer, U. M., Jansma, H., Tempelmann, C., & Münte, T. F. (2007). Tit-for-tat: The neural basis of reactive aggression. NeuroImage, 38, 203–211.CrossRefPubMedGoogle Scholar
  40. Krämer, U. M., Riba, J., Richter, S., & Münte, T. F. (2011). An fMRI study on the role of serotonin in reactive aggression. PLOS ONE, 6(11), e27668.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lotze, M., Veit, R., Anders, S., & Birbaumer, N. (2007). Evidence for a different role of the ventral and dorsal medial prefrontal cortex for social reactive aggression: An interactive fMRI study. NeuroImage, 34, 470–478.CrossRefPubMedGoogle Scholar
  42. Lyvers, M. F., & Maltzman, I. (1991). Selective effects of alcohol on Wisconsin card sorting test-performance. British Journal of Addiction, 86, 399–407.CrossRefPubMedGoogle Scholar
  43. Marxen, M., Gan, G., Schwarz, D., Mennigen, E., Pilhatsch, M., Zimmermann, U. S., ... & Smolka, M. N. (2014). Acute effects of alcohol on brain perfusion monitored with arterial spin labeling magnetic resonance imaging in young adults. Journal of Cerebral Blood Flow & Metabolism, 34, 472–479.Google Scholar
  44. Miczek, K. A., Barros, H. M., Sakoda, L., & Weerts, E. M. (1998). Alcohol and heightened aggression in individual mice. Alcoholism: Clinical and Experimental Research, 22, 1698–1705.CrossRefGoogle Scholar
  45. Murdoch, D., & Ross, D. (1990). Alcohol and crimes of violence: Present issues. International Journal of the Addictions, 25(9), 1065–1081.CrossRefPubMedGoogle Scholar
  46. Owen, A. M., McMillan, K. M., Laird, A. R., & Bullmore, E. (2005). N-back working memory paradigm: A meta-analysis of normative functional neuroimaging studies. Human Brain Mapping, 25, 46–59.CrossRefPubMedGoogle Scholar
  47. Parrott, D. J., & Zeichner, A. (2002). Effects of alcohol and trait anger on physical aggression in men. Journal of Studies on Alcohol, 63, 196–204.CrossRefPubMedGoogle Scholar
  48. Peterson, J. B., Rothfleisch, J., Zelazo, P. D., & Pihl, R. O. (1990). Acute alcohol-intoxication and cognitive functioning. Journal of Studies on Alcohol, 51, 114–122.CrossRefPubMedGoogle Scholar
  49. Quigley, B. M., & Leonard, K. E. (2000). Alcohol, drugs, and violence. In V. B. Van Hasselt & M. Hersen (Eds.), Aggression and violence: An introductory text (pp. 259–283). Needham Heights, MA: Allyn & Bacon.Google Scholar
  50. R Core Team. (2016). R: A language and environment for statistical computing [Computer software]. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/
  51. Raine, A. (2008). From genes to brain to antisocial behavior. Current Directions in Psychological Science, 17, 323–328.CrossRefGoogle Scholar
  52. Riva, P., Romero Lauro, L. J., DeWall, C. N., Chester, D. S., & Bushman, B. J. (2015). Reducing aggressive responses to social exclusion using transcranial direct current stimulation. Social cognitive and affective neuroscience, 10, 352–356.Google Scholar
  53. Room, R., & Rossow, I. (2001). The share of violence attributable to drinking. Journal of Substance Use, 6, 218–228.CrossRefGoogle Scholar
  54. Schofield, T. P., Unkelbach, C., & Denson, T. F. (2017). Alcohol consumption increases the bias to shoot at Middle Eastern but not White targets. Group Processes & Intergroup Relations, 20, 202–215.CrossRefGoogle Scholar
  55. Schreckenberger, M., Amberg, R., Scheurich, A., Lochmann, M., Tichy, W., Kiega, A., ... Urban, R. (2004). Acute alcohol effects on neuronal and attentional processing: Striatal reward system and inhibitory sensory interactions under acute ethanol challenge. Neuropsychopharmacology 29, 1527–1537.CrossRefPubMedGoogle Scholar
  56. Smith, S., Jenkinson, M., Woolrich, M., Beckmann, C., Behrens, T., Johansen-Berg, H., ... Matthews, P. M. (2004). Advances in structural and functional MR image analysis and implementation in FSL. NeuroImage, 23, 208–209.CrossRefGoogle Scholar
  57. Steele, C. M., & Southwick, L. (1985). Alcohol and social behavior: I. The psychology of drunken excess. Journal of Personality and Social Psychology, 48, 18–34.CrossRefPubMedGoogle Scholar
  58. Subra, B., Muller, D., Bègue, L., Bushman, B. J., & Delmas, F. (2010). Automatic effects of alcohol and aggressive cues on aggressive thoughts and behaviors. Personality and Social Psychology Bulletin, 36, 1052–1057.CrossRefPubMedGoogle Scholar
  59. Swanson, J. W., Holzer, C. E., III, Ganju, V. K., & Jono, R. T. (1990). Violence and psychiatric disorder in the community: Evidence from the Epidemiologic Catchment Area surveys. Psychiatric Services, 41, 761–770.CrossRefGoogle Scholar
  60. Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York, NY: Thieme.Google Scholar
  61. Taylor, S. P. (1967). Aggressive behavior and physiological arousal as a function of provocation and the tendency to inhibit aggression. Journal of Personality, 35, 297–310.CrossRefPubMedGoogle Scholar
  62. U.S. Department of Justice. (1998). Alcohol and crime: An analysis of national data on the prevalence of alcohol involvement in crime. Retrieved from http://www.bjs.gov/content/pub/pdf/ac.pdf

Copyright information

© Psychonomic Society, Inc. 2018

Authors and Affiliations

  • Thomas F. Denson
    • 1
  • Kate A. Blundell
    • 1
  • Timothy P. Schofield
    • 1
  • Mark M. Schira
    • 2
    • 3
  • Ulrike M. Krämer
    • 4
    • 5
  1. 1.School of PsychologyUniversity of New South WalesSydneyAustralia
  2. 2.Neuroscience Research AustraliaRandwickAustralia
  3. 3.School of PsychologyUniversity of WollongongWollongongAustralia
  4. 4.Department of NeurologyUniversity of LübeckLübeckGermany
  5. 5.Institute of Psychology IIUniversity of LübeckLübeckGermany

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