Abstract
Although sex differences in aggression have been investigated for decades, little is known about the underlying neurobiology of this phenomenon. To address this gap, the present study implemented a social reactive aggression paradigm in 20 women and 22 men, employing a modified Taylor Aggression Task (mTAT) to provoke aggressive behavior in an fMRI setting. Subjects were provoked by money subtraction from a fake opponent and given the opportunity to retaliate likewise. In the absence of behavioral differences, male and female subjects showed differential brain activation patterns in response to provocation. Men had higher left amygdala activation during high provocation. This amygdala activation correlated with trait anger scores in men, but not in women. Also, men showed a positive association between orbitofrontal cortex, rectal gyrus and anterior cingulate cortex (ACC) activity in the provocation contrast and their tendency to respond aggressively, whereas women displayed a negative association. As the rectal gyrus and OFC have been attributed a crucial role in automatic emotion regulation, this finding points toward the assumption that highly aggressive men use automatic emotion regulation to a greater extent in response to provocation compared to highly aggressive women.
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References
Anderson CA, Bushman BJ (2001) Human aggression. Annu Rev Psychol 53:27–51. https://doi.org/10.1146/annurev.psych.53.100901.135231
Archer J (2004) Sex differences in aggression in real-world settings: a meta-analytic review. Rev Gen Psychol 8:291–322. https://doi.org/10.1037/1089-2680.8.4.291
Archer J (2009) Does sexual selection explain human sex differences in aggression? Behav Brain Sci 32:249–266. https://doi.org/10.1017/S0140525X09990951
Asahi S, Okamoto Y, Okada G et al (2004) Negative correlation between right prefrontal activity during response inhibition and impulsiveness: a fMRI study. Eur Arch Psychiatry Clin Neurosci 254:245–251. https://doi.org/10.1007/s00406-004-0488-z
Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26:839–851. https://doi.org/10.1016/j.neuroimage.2005.02.018
Bao A-M, Swaab DF (2011) Sexual differentiation of the human brain: relation to gender identity, sexual orientation and neuropsychiatric disorders. Front Neuroendocrinol 32:214–226. https://doi.org/10.1016/j.yfrne.2011.02.007
Bettencourt BA, Miller N (1996) Gender differences in aggression as a function of provocation: a meta-analysis. Psychol Bull 119:422–447. https://doi.org/10.1037/0033-2909.119.3.422
Beyer F, Münte TF, Erdmann C, Krämer UM (2013) Emotional reactivity to threat modulates activity in mentalizing network during aggression. Soc Cogn Affect Neurosci I. https://doi.org/10.1093/scan/nst146
Beyer F, Muente TF, Goettlich M, Kraemer UM (2015) Orbitofrontal cortex reactivity to angry facial expression in a social interaction correlates with aggressive behavior. Cereb Cortex 25:3057–3063. https://doi.org/10.1093/cercor/bhu101
Blair RJR (2012) Considering anger from a cognitive neuroscience perspective. Wiley Interdiscip Rev Cogn Sci 3:65–74. https://doi.org/10.1002/wcs.154
Blair RJR (2016) The neurobiology of impulsive aggression. J Child Adolesc Psychopharmacol 26:4–9. https://doi.org/10.1089/cap.2015.0088
Bobes M, Ostrosky F, Diaz K et al (2013) Linkage of functional and structural anomalies in the left amygdala of reactive-aggressive men. Soc Cogn Affect Neurosci 8:928–936. https://doi.org/10.1093/scan/nss101
Broidy L, Agnew R (1997) Gender and crime: a general strain theory perspective. J Res Crime Delinq 34:275–306. https://doi.org/10.1177/0022427897034003001
Buhle JT, Silvers JA, Wage TD et al (2014) Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. Cereb Cortex 24:2981–2990. https://doi.org/10.1093/cercor/bht154
Buss AH, Perry M (1992) Personality processes and individual the aggression questionnaire. J Pers 63:452–459. https://doi.org/10.1037/0022-3514.63.3.452
Cahill L (2006) Why sex matters for neuroscience. Nat Rev Neurosci 7:477–484. https://doi.org/10.1038/nrn1909
Campbell A (2006) Sex differences in direct aggression: what are the psychological mediators? Aggress Violent Behav 11:237–264. https://doi.org/10.1016/j.avb.2005.09.002
Carré JM, Olmstead NA (2015) Social neuroendocrinology of human aggression: examining the role of competition-induced testosterone dynamics. Neuroscience 286:171–186
Chester DS, Eisenberger NI, Pond RS et al (2014) The interactive effect of social pain and executive functioning on aggression: an fMRI experiment. Soc Cogn Affect Neurosci 9:699–704. https://doi.org/10.1093/scan/nst038
Coccaro EF, Sripada CS, Yanowitch RN, Phan KL (2011) Corticolimbic function in impulsive aggressive behavior. Biol Psychiatry 69:1153–1159. https://doi.org/10.1016/j.biopsych.2011.02.032
Daigle LE, Cullen FT, Wright JP (2007) Gender differences in the predictors of juvenile delinquency. Youth Violence Juv Justice 5:254–286. https://doi.org/10.1177/1541204007301289
Damasio H, Grabowski T, Frank R et al (1994) The return of Phineas Gage: clues about the brain from the skull of a famous patient. Science 264:1102–1105. https://doi.org/10.1126/science.8178168
Dambacher F, Schuhmann T, Lobbestael J et al (2015) No effects of bilateral tDCS over inferior frontal gyrus on response inhibition and aggression. PLoS One. https://doi.org/10.1371/journal.pone.0132170
DeKeseredy WS (2011) Feminist contributions to understanding woman abuse: myths, controversies, and realities. Aggress Violent Behav 16:297–302. https://doi.org/10.1016/j.avb.2011.04.002
Derntl B, Windischberger C, Robinson S et al (2009) Amygdala activity to fear and anger in healthy young males is associated with testosterone. Psychoneuroendocrinology 34:687–693. https://doi.org/10.1016/j.psyneuen.2008.11.007
Domes G, Schulze L, Böttger M et al (2010) The neural correlates of sex differences in emotional reactivity and emotion regulation. Hum Brain Map 31:758–769. https://doi.org/10.1002/hbm.20903
Eickhoff SB, Stephan KE, Mohlberg H et al (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325–1335. https://doi.org/10.1016/j.neuroimage.2004.12.034
Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15:85–93. https://doi.org/10.1016/j.tics.2010.11.004
Etkin A, Büchel C, Gross JJ (2015) The neural bases of emotion regulation. Nat Rev Neurosci 16:693–700. https://doi.org/10.1038/nrn4044
Fine JG, Semrud-Clikeman M, Zhu DC (2009) Gender differences in BOLD activation to face photographs and video vignettes. Behav Brain Res 201:137–146. https://doi.org/10.1016/j.bbr.2009.02.009
Gan G, Sterzer P, Marxen M et al (2015) Neural and behavioral correlates of alcohol-induced aggression under provocation. Neuropsychopharmacology. https://doi.org/10.1038/npp.2015.141
Giancola PR, Parrott DJ (2008) Further evidence for the validity of the Taylor aggression paradigm. Aggress Behav 34:214–229. https://doi.org/10.1002/ab.20235
Goetz SMM, Tang L, Thomason ME et al (2014) Testosterone rapidly increases neural reactivity to threat in healthy men: a novel two-step pharmacological challenge paradigm. Biol Psychiatry 76:324–331. https://doi.org/10.1016/j.biopsych.2014.01.016
Gopal A, Clark E, Allgair A et al (2013) Dorsal/ventral parcellation of the amygdala: Relevance to impulsivity and aggression. Psychiatry Res Neuroimag 211:24–30. https://doi.org/10.1016/j.pscychresns.2012.10.010
Gustafsson A, Lindenfors P (2004) Human size evolution: No evolutionary allometric relationship between male and female stature. J Hum Evol 47:253–266. https://doi.org/10.1016/j.jhevol.2004.07.004
Hay DF (2007) The gradual emergence of sex differences in aggression: alternative hypotheses. Psychol Med 37:1527–1537. https://doi.org/10.1017/S0033291707000165
Herpertz SC, Nagy K, Ueltzhöffer K et al (2017) Brain mechanisms underlying reactive aggression in borderline personality disorder—sex matters. Biol Psychiatry 82:257–266. https://doi.org/10.1016/j.biopsych.2017.02.1175
Kohn N, Kellermann T, Gur RC et al (2011) Gender differences in the neural correlates of humor processing: Implications for different processing modes. Neuropsychologia 49:888–897. https://doi.org/10.1016/j.neuropsychologia.2011.02.010
Kohn N, Eickhoff SB, Scheller M et al (2014) Neural network of cognitive emotion regulation—an ALE meta-analysis and MACM analysis. Neuroimage 87:345–355. https://doi.org/10.1016/j.neuroimage.2013.11.001
Kopsida E, Berrebi J, Petrovic P, Ingvar M (2016) Testosterone administration related differences in brain activation during the Ultimatum Game. Front Neurosci 10:. https://doi.org/10.3389/fnins.2016.00066
Krämer UM, Riba J, Richter S et al (2011) An fMRI study on the role of serotonin in reactive aggression. PLoS One 6:e27668. https://doi.org/10.1371/journal.pone.0027668
Kret MEE, De Gelder B (2012) A review on sex differences in processing emotional signals. Neuropsychologia 50:1211–1221. https://doi.org/10.1016/j.neuropsychologia.2011.12.022
Lancaster JL, Woldorff MG, Parsons LM et al (2000) Automated Talairach atlas labels for functional brain mapping. Hum Brain Map 10:120–131
Liu J, Zubieta J-K, Heitzeg M (2012) Sex differences in anterior cingulate cortex activation during impulse inhibition and behavioral correlates. Psychiatry Res 201:54–62. https://doi.org/10.1016/j.pscychresns.2011.05.008
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. https://doi.org/10.1016/j.neuroimage.2006.09.028
Mattavelli G, Sormaz M, Flack T et al (2014) Neural responses to facial expressions support the role of the amygdala in processing threat. Soc Cogn Affect Neurosci 9:1684–1689. https://doi.org/10.1093/scan/nst162
Mauss IB, Evers C, Wilhelm FH, Gross JJ (2006) How to bite your tongue without blowing your top: Implicit evaluation of emotion regulation predicts affective responding to anger provocation. Pers Soc Psychol Bull 32:589–602. https://doi.org/10.1177/0146167205283841
McRae K, Ochsner KN, Mauss IB et al (2008) Gender differences in emotion regulation: an fMRI study of cognitive reappraisal. Gr Process Intergr Relat 11:143–162. https://doi.org/10.1177/1368430207088035
Wittchen H, Zaudig M, Fydrich T (1997) Strukturiertes Klinisches Interview für DSM-IV, Hogrefe
Rahko J, Paakki JJ, Starck T et al (2010) Functional mapping of dynamic happy and fearful facial expression processing in adolescents. Brain Imaging Behav 4:164–176. https://doi.org/10.1007/s11682-010-9096-x
Repple J, Pawliczek CM, Voss B et al (2017) From provocation to aggression: the neural network. BMC Neurosci 18:73. https://doi.org/10.1186/s12868-017-0390-z
Richardson DS, Hammock GS (2007) Social context of human aggression: are we paying too much attention to gender? Aggress Violent Behav 12:417–426. https://doi.org/10.1016/j.avb.2006.11.001
Scarduzio JA, Carlyle KE, Harris KL, Savage MW (2017) Maybe she was provoked. Violence Against Women 23:89–113. https://doi.org/10.1177/1077801216636240
Schienle A, Schäfer A, Stark R et al (2005) Gender differences in the processing of disgust- and fear-inducing pictures: an fMRI study. Neuroreport 16:277–280. https://doi.org/10.1097/00001756-200502280-00015
Schneider F, Habel U, Kessler C et al (2000) Gender differences in regional cerebral activity during sadness. Hum Brain Map 9:226–238. https://doi.org/10.1002/(SICI)1097-0193(200004)9:4%3C226::AID-HBM4%3E3.0.CO;2-K
Schwenkmezger P, Hodapp V, Spielberger CD (1992) Das State-Trait Aerger-Ausdrucks-Inventar. Huber, Bern
Siever LJ (2008) Reviews and overviews neurobiology of aggression and violence. Am J Psychiatry 165:429–442. https://doi.org/10.1176/appi.ajp.2008.07111774
Strüber D, Lück M, Roth G (2008) Sex, aggression and impulse control: an integrative account. Neurocase Neural Basis Cogn 14:93–121. https://doi.org/10.1080/13554790801992743
Wagels L, Votinov M, Kellermann T et al (2018) Exogenous testosterone enhances the reactivity to social provocation in males. Front Behav Neurosci 12:37. https://doi.org/10.3389/FNBEH.2018.00037
Weaver JR, Vandello JA, Bosson JK, Burnaford RM (2010) The proof is in the punch: gender differences in perceptions of action and aggression as components of manhood. Sex Roles 62:241–251. https://doi.org/10.1007/s11199-009-9713-6
Wrase J, Klein S, Gruesser SM et al (2003) Gender differences in the processing of standardized emotional visual stimuli in humans: a functional magnetic resonance imaging study. Neurosci Lett 348:41–45. https://doi.org/10.1016/S0304-3940(03)00565-2
Yang Y, Raine A (2009) Prefrontal structural and functional brain imaging findings in antisocial, violent, and psychopathic individuals: a meta-analysis. Psychiatry Res 174:81–88. https://doi.org/10.1016/j.pscychresns.2009.03.012
Acknowledgements
The authors thank all subjects for participation. The study was supported by the German Research Foundation (IRTG 1328, DFG), IZKF Aachen (Interdisciplinary Center for Clinical Research within the Faculty of Medicine at the RWTH Aachen University, N4-4) and the Brain Imaging Facility of the Interdisciplinary Centre for Clinical Research within the Faculty of Medicine at the RWTH Aachen University, Germany.
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Repple, J., Habel, U., Wagels, L. et al. Sex differences in the neural correlates of aggression. Brain Struct Funct 223, 4115–4124 (2018). https://doi.org/10.1007/s00429-018-1739-5
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DOI: https://doi.org/10.1007/s00429-018-1739-5