Anger under Control: Neural Correlates of Frustration as a Function of Trait Aggression

Antisocial behavior and aggression are prominent symptoms in several psychiatric disorders including antisocial personality disorder. An established precursor to aggression is a frustrating event, which can elicit anger or exasperation, thereby prompting aggressive responses. While some studies have investigated the neural correlates of frustration and aggression, examination of their relation to trait aggression in healthy populations are rare. Based on a screening of 550 males, we formed two extreme groups, one including individuals reporting high (n=21) and one reporting low (n=18) trait aggression. Using functional magnetic resonance imaging (fMRI) at 3T, all participants were put through a frustration task comprising unsolvable anagrams of German nouns. Despite similar behavioral performance, males with high trait aggression reported higher ratings of negative affect and anger after the frustration task. Moreover, they showed relatively decreased activation in the frontal brain regions and the dorsal anterior cingulate cortex (dACC) as well as relatively less amygdala activation in response to frustration. Our findings indicate distinct frontal and limbic processing mechanisms following frustration modulated by trait aggression. In response to a frustrating event, HA individuals show some of the personality characteristics and neural processing patterns observed in abnormally aggressive populations. Highlighting the impact of aggressive traits on the behavioral and neural responses to frustration in non-psychiatric extreme groups can facilitate further characterization of neural dysfunctions underlying psychiatric disorders that involve abnormal frustration processing and aggression.

[1]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[2]  R. Nelson,et al.  Neural mechanisms of aggression , 2007, Nature Reviews Neuroscience.

[3]  G. Pagnoni,et al.  Neural Correlates of Social Cooperation and Non-Cooperation as a Function of Psychopathy , 2007, Biological Psychiatry.

[4]  M. Buchsbaum,et al.  Selective reductions in prefrontal glucose metabolism in murderers , 1994, Biological Psychiatry.

[5]  M. Dolan,et al.  Psychopathic traits and deception: functional magnetic resonance imaging study , 2009, British Journal of Psychiatry.

[6]  Anirvan S. Nandy,et al.  The Angry Brain: Neural Correlates of Anger, Angry Rumination, and Aggressive Personality , 2009, Journal of Cognitive Neuroscience.

[7]  Reinout W. Wiers,et al.  How to push someone's buttons: A comparison of four anger-induction methods , 2008 .

[8]  Y. Okamoto,et al.  Negative correlation between right prefrontal activity during response inhibition and impulsiveness: A fMRI study , 2004, European Archives of Psychiatry and Clinical Neuroscience.

[9]  M. Potegal Temporal and frontal lobe initiation and regulation of the top-down escalation of anger and aggression , 2012, Behavioural Brain Research.

[10]  A. Buss,et al.  The aggression questionnaire. , 1992, Journal of personality and social psychology.

[11]  Nils Kohn,et al.  Inhibitory control and trait aggression: Neural and behavioral insights using the emotional stop signal task , 2013, NeuroImage.

[12]  L. Siever,et al.  The neurobiology of aggression and violence , 2015, CNS Spectrums.

[13]  Franz Petermann,et al.  Psychopathic Personality Inventory-Revised (PPI-R) , 2009 .

[14]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[15]  G. Stemmler Somatovisceral Activation During Anger , 2010 .

[16]  P. Lang,et al.  Emotion in the criminal psychopath: fear image processing. , 1994, Journal of abnormal psychology.

[17]  H. Ohira,et al.  Amygdala dysfunction attenuates frustration-induced aggression in psychopathic individuals in a non-criminal population. , 2012, Journal of affective disorders.

[18]  A. David,et al.  Predictors of amygdala activation during the processing of emotional stimuli: A meta-analysis of 385 PET and fMRI studies , 2008, Brain Research Reviews.

[19]  M. Botvinick,et al.  The Contribution of the Anterior Cingulate Cortex to Executive Processes in Cognition , 1999, Reviews in the neurosciences.

[20]  Ruben C. Gur,et al.  Standardized mood induction with happy and sad facial expressions , 1994, Psychiatry Research.

[21]  S. Lilienfeld,et al.  Development and preliminary validation of a self-report measure of psychopathic personality traits in noncriminal populations. , 1996, Journal of personality assessment.

[22]  L. Carretié,et al.  Negative brain: an integrative review on the neural processes activated by unpleasant stimuli. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[23]  E. Viding,et al.  Amygdala hypoactivity to fearful faces in boys with conduct problems and callous-unemotional traits. , 2009, The American journal of psychiatry.

[24]  A. Gelman,et al.  Splitting a Predictor at the Upper Quarter or Third and the Lower Quarter or Third , 2007 .

[25]  Patrick M Fisher,et al.  Interaction between trait anxiety and trait anger predict amygdala reactivity to angry facial expressions in men but not women. , 2012, Social cognitive and affective neuroscience.

[26]  M. Schlossberg The Halstead-Reitan Neuropsychological Test Battery: Theory and Clinical Interpretation. , 1986 .

[27]  E. Rolls,et al.  Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage , 1996, Neuropsychologia.

[28]  M. Potegal,et al.  International handbook of anger , 2010 .

[29]  I. Gottesman,et al.  The endophenotype concept in psychiatry: etymology and strategic intentions. , 2003, The American journal of psychiatry.

[30]  Kristopher J Preacher,et al.  Use of the extreme groups approach: a critical reexamination and new recommendations. , 2005, Psychological methods.

[31]  S. Shamay-Tsoory,et al.  Asymmetry in the dorsolateral prefrontal cortex and aggressive behavior: A continuous theta-burst magnetic stimulation study , 2013, Social neuroscience.

[32]  R. Post,et al.  Regional brain activity during transient self-induced anxiety and anger in healthy adults , 1999, Biological Psychiatry.

[33]  Philipp Sterzer,et al.  Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder , 2005, Biological Psychiatry.

[34]  M S Buchsbaum,et al.  Reduced prefrontal and increased subcortical brain functioning assessed using positron emission tomography in predatory and affective murderers. , 1998, Behavioral sciences & the law.

[35]  Leonard Berkowitz,et al.  Toward an understanding of the determinants of anger. , 2004, Emotion.

[36]  J. Barth,et al.  The Halstead-Reitan Neuropsychological Test Battery. , 2000 .

[37]  J. Grafman,et al.  Developmental effects of aggressive behavior in male adolescents assessed with structural and functional brain imaging. , 2011, Social cognitive and affective neuroscience.

[38]  „Empirische Forschung in der forensischen Psychiatrie, Psychologie und Psychotherapie“ , 2012, Forensische Psychiatrie, Psychologie, Kriminologie.

[39]  Chandra Sekhar Sripada,et al.  Corticolimbic Function in Impulsive Aggressive Behavior , 2011, Biological Psychiatry.

[40]  Essi Viding,et al.  Neural responses to affective and cognitive theory of mind in children with conduct problems and varying levels of callous-unemotional traits. , 2012, Archives of general psychiatry.

[41]  G. Pagnoni,et al.  A Neural Basis for Social Cooperation , 2002, Neuron.

[42]  A. Bond,et al.  The Neurochemistry and Psychopharmacology of Anger , 2010 .

[43]  David Silbersweig,et al.  Failure of frontolimbic inhibitory function in the context of negative emotion in borderline personality disorder. , 2007, The American journal of psychiatry.

[44]  Matthew D. Lieberman,et al.  Does Rejection Hurt? An fMRI Study of Social Exclusion , 2003, Science.

[45]  C. Li,et al.  Antisocial personality and stress-induced brain activation in cocaine-dependent patients , 2006, Neuroreport.

[46]  L. Berkowitz,et al.  On the formation and regulation of anger and aggression. A cognitive-neoassociationistic analysis. , 1990, The American psychologist.

[47]  B. Bettencourt,et al.  Personality and aggressive behavior under provoking and neutral conditions: a meta-analytic review. , 2006, Psychological bulletin.

[48]  James Lani,et al.  Positive and Negative Affect Schedule (PANAS) , 2010 .

[49]  K. Zilles,et al.  Differential brain activation according to chronic social reward frustration , 2005, Neuroreport.

[50]  Janice E. Williams Anger/Hostility and Cardiovascular Disease , 2010 .

[51]  L. Berkowitz Frustration-aggression hypothesis: examination and reformulation. , 1989, Psychological bulletin.

[52]  E. Rolls,et al.  Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. , 2003, Brain : a journal of neurology.

[53]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[54]  S. Herpertz,et al.  Emotion in criminal offenders with psychopathy and borderline personality disorder. , 2001, Archives of general psychiatry.

[55]  D. Perrett,et al.  Dissociable neural responses to facial expressions of sadness and anger. , 1999, Brain : a journal of neurology.

[56]  Matthew D. Lieberman,et al.  Neural pathways link social support to attenuated neuroendocrine stress responses , 2007, NeuroImage.

[57]  A. Alavi,et al.  Cerebral blood flow changes in limbic regions induced by unsolvable anagram tasks. , 1996, The American journal of psychiatry.

[58]  David A. Gansler,et al.  Prefrontal regional correlates of self-control in male psychiatric patients: Impulsivity facets and aggression , 2011, Psychiatry Research: Neuroimaging.

[59]  R. Blair,et al.  The amygdala and ventromedial prefrontal cortex: functional contributions and dysfunction in psychopathy , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[60]  Henrik Walter,et al.  Neural correlates of frustration , 2005, Neuroreport.

[61]  K. Phan,et al.  Amygdala and Orbitofrontal Reactivity to Social Threat in Individuals with Impulsive Aggression , 2007, Biological Psychiatry.

[62]  Christopher J Patrick,et al.  Estimating Facets of Psychopathy From Normal Personality Traits , 2005, Assessment.

[63]  R. Reitan,et al.  The Halstead-Reitan neuropsychological test battery: Theory and clinical interpretation , 1993 .

[64]  E. Coccaro,et al.  Assessment of life history of aggression: development and psychometric characteristics , 1997, Psychiatry Research.

[65]  K. Amunts,et al.  Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps , 2005, Anatomy and Embryology.

[66]  R. Blair The amygdala and ventromedial prefrontal cortex in morality and psychopathy , 2007, Trends in Cognitive Sciences.

[67]  Abigail A. Baird,et al.  Functional differences among those high and low on a trait measure of psychopathy , 2004, Biological Psychiatry.

[68]  Neuronale Korrelate von Frustration und Impulsivität , 2012 .

[69]  Carl-Walter Kohlmann,et al.  Untersuchungen mit einer deutschen Version der "Positive and Negative Affect Schedule" (PANAS). , 1996 .

[70]  Jonathan D. Cohen,et al.  The Neural Basis of Economic Decision-Making in the Ultimatum Game , 2003, Science.

[71]  Monte S. Buchsbaum,et al.  Laboratory Induced Aggression: A Positron Emission Tomography Study of Aggressive Individuals with Borderline Personality Disorder , 2009, Biological Psychiatry.

[72]  K. Williams The Effects of Frustration, Violence, and Trait Hostility After Playing a Video Game , 2009 .

[73]  Adrianna Mendrek,et al.  Limbic abnormalities in affective processing by criminal psychopaths as revealed by functional magnetic resonance imaging , 2001, Biological Psychiatry.

[74]  E. Harmon-Jones,et al.  State anger and prefrontal brain activity: evidence that insult-related relative left-prefrontal activation is associated with experienced anger and aggression. , 2001, Journal of personality and social psychology.

[75]  Daniel Tranel,et al.  Asymmetric Functional Roles of Right and Left Ventromedial Prefrontal Cortices in Social Conduct, Decision-Making, and Emotional Processing , 2002, Cortex.

[76]  D. Weinberger,et al.  Neocortical modulation of the amygdala response to fearful stimuli , 2003, Biological Psychiatry.

[77]  J. Gorman,et al.  The Human Dimension: How the Prefrontal Cortex Modulates the Subcortical Fear Response , 2007, Reviews in the neurosciences.

[78]  Michael Erb,et al.  Deficient fear conditioning in psychopathy: a functional magnetic resonance imaging study. , 2005, Archives of general psychiatry.

[79]  William D S Killgore,et al.  Sex differences in amygdala activation during the perception of facial affect , 2001, Neuroreport.

[80]  Simon B. Eickhoff,et al.  Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps , 2006, NeuroImage.

[81]  Adrian Raine,et al.  Prefrontal structural and functional brain imaging findings in antisocial, violent, and psychopathic individuals: A meta-analysis , 2009, Psychiatry Research: Neuroimaging.