Do anger perception and the experience of anger share common neural mechanisms? Coordinate-based meta-analytic evidence of similar and different mechanisms from functional neuroimaging studies

The neural bases of anger are still a matter of debate. In particular we do not know whether anger perception and anger experience rely on similar or different neural mechanisms. To study this topic, we performed activation-likelihood-estimation meta-analyses of human neuroimaging studies on 61 previous studies on anger perception and experience. Anger perception analysis resulted in significant activation in the amygdala, the right superior temporal gyrus, the right fusiform gyrus and the right IFG, thus revealing the role of perceptual temporal areas for perceiving angry stimuli. Anger experience analysis resulted in the bilateral activations of the insula and the ventrolateral prefrontal cortex, thus revealing a role for these areas in the subjective experience of anger and, possibly, in a subsequent evaluation of the situation. Conjunction analyses revealed a common area localized in the right inferior frontal gyrus, probably involved in the conceptualization of anger for both perception and experience. Altogether these results provide new insights on the functional architecture underlying the neural processing of anger that involves separate and joint mechanisms. According to our tentative model, angry stimuli are processed by temporal areas, such as the superior temporal gyrus, the fusiform gyrus and the amygdala; on the other hand, the subjective experience of anger mainly relies on the anterior insula; finally, this pattern of activations converges in the right IFG. This region seems to play a key role in the elaboration of a general meaning of this emotion, when anger is perceived or experienced.

[1]  N. Alpert,et al.  Anger in healthy men: a PET study using script-driven imagery , 1999, Biological Psychiatry.

[2]  Jennifer A. Silvers,et al.  Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. , 2014, Cerebral cortex.

[3]  Anina N. Rich,et al.  Moral Violations and the Experience of Disgust and Anger , 2018, Front. Behav. Neurosci..

[4]  Richard J. Maddock,et al.  Separating subjective emotion from the perception of emotion-inducing stimuli: An fMRI study , 2006, NeuroImage.

[5]  Mark M. Schira,et al.  A Functional Polymorphism of the MAOA Gene Is Associated with Neural Responses to Induced Anger Control , 2014, Journal of Cognitive Neuroscience.

[6]  C. Montag,et al.  Exogenous testosterone and the monoamine-oxidase A polymorphism influence anger, aggression and neural responses to provocation in males , 2019, Neuropharmacology.

[7]  Talma Hendler,et al.  Neural substrates underlying the tendency to accept anger-infused ultimatum offers during dynamic social interactions , 2015, NeuroImage.

[8]  M. Osaka,et al.  Extrapunitive and Intropunitive Individuals Activate Different Parts of the Prefrontal Cortex under an Ego-Blocking Frustration , 2014, PloS one.

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

[10]  Kevin N. Ochsner,et al.  The neural bases of emotion and emotion regulation: A valuation perspective. , 2014 .

[11]  R. Job,et al.  Baseline and Strategic Effects behind Mindful Emotion Regulation: Behavioral and Physiological Investigation , 2015, PloS one.

[12]  Claus Tempelmann,et al.  Tit-for-tat: The neural basis of reactive aggression , 2007, NeuroImage.

[13]  Martin A Giese,et al.  Common neural correlates of emotion perception in humans , 2015, Human brain mapping.

[14]  C. DeWall,et al.  Intimate partner violence perpetration corresponds to a dorsal-ventral gradient in medial PFC reactivity to interpersonal provocation , 2019, Social neuroscience.

[16]  Carrie L. Masten,et al.  Do neural responses to rejection depend on attachment style? An fMRI study. , 2012, Social cognitive and affective neuroscience.

[17]  W. Miltner,et al.  Visual Attention Modulates Brain Activation to Angry Voices , 2011, The Journal of Neuroscience.

[18]  Stella W. Y. Chan,et al.  Deactivation in anterior cingulate cortex during facial processing in young individuals with high familial risk and early development of depression: fMRI findings from the Scottish Bipolar Family Study. , 2016, Journal of child psychology and psychiatry, and allied disciplines.

[19]  John Duncan,et al.  Selective tuning of the right inferior frontal gyrus during target detection , 2009, Cognitive, affective & behavioral neuroscience.

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

[21]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[22]  R. Knight,et al.  PSYCHOLOGICAL SCIENCE Research Article Controlling the Integration of Emotion and Cognition The Role of Frontal Cortex in Distinguishing Helpful From Hurtful Emotional Information , 2022 .

[23]  Angela R. Laird,et al.  Ten simple rules for neuroimaging meta-analysis , 2018, Neuroscience & Biobehavioral Reviews.

[24]  P. Belin,et al.  Binge drinking influences the cerebral processing of vocal affective bursts in young adults☆ , 2013, NeuroImage: Clinical.

[25]  Matthew D. Lieberman,et al.  Putting Feelings Into Words , 2007, Psychological science.

[26]  Sharlene D. Newman,et al.  Baseline conditions and subtractive logic in neuroimaging , 2001, Human Brain Mapping.

[27]  U. Habel,et al.  Immediate and delayed neuroendocrine responses to social exclusion in males and females , 2018, Psychoneuroendocrinology.

[28]  Shannon M. Sheppard,et al.  That's right! Language comprehension beyond the left hemisphere. , 2018, Brain : a journal of neurology.

[29]  P. McGuire,et al.  Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. , 2009, Journal of psychiatry & neuroscience : JPN.

[30]  U. Dimberg,et al.  Facial reactions, autonomic activity and experienced emotion: A three component model of emotional conditioning , 1987, Biological Psychology.

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

[32]  G. Brabant,et al.  Endogenous testosterone is associated with lower amygdala reactivity to angry faces and reduced aggressive behavior in healthy young women , 2016, Scientific Reports.

[33]  D. Dougherty,et al.  Autonomic and prefrontal cortex responses to autobiographical recall of emotions , 2007, Cognitive, affective & behavioral neuroscience.

[34]  L. F. Barrett Solving the Emotion Paradox: Categorization and the Experience of Emotion , 2006, Personality and social psychology review : an official journal of the Society for Personality and Social Psychology, Inc.

[35]  A. Grecucci,et al.  Emotions at the Border: Increased Punishment Behavior During Fair Interpersonal Exchanges in Borderline Personality Disorder , 2019, Journal of abnormal psychology.

[36]  Jennifer C. Britton,et al.  Facial expressions and complex IAPS pictures: Common and differential networks , 2006, NeuroImage.

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

[38]  Christina M. Pawliczek,et al.  Sex differences in the neural correlates of aggression , 2018, Brain Structure and Function.

[39]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[40]  Maria Arioli,et al.  Neural processing of social interaction: Coordinate‐based meta‐analytic evidence from human neuroimaging studies , 2019, Human brain mapping.

[41]  M. Brüne,et al.  Borderline Personality Disorder , 2016, Evolution, medicine, and public health.

[42]  U. Eysel,et al.  Neural structures associated with recognition of facial expressions of basic emotions , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[43]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

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

[45]  T. Hendler,et al.  Deconstructing Anger in the Human Brain. , 2015, Current topics in behavioral neurosciences.

[46]  Karl Aquino,et al.  Getting even or moving on? Power, procedural justice, and types of offense as predictors of revenge, forgiveness, reconciliation, and avoidance in organizations. , 2006, The Journal of applied psychology.

[47]  Ji-Woo Seok,et al.  Dynamic Causal Modeling of Effective Connectivity During Anger Experience in Healthy Young Men: 7T Magnetic Resonance Imaging Study , 2019, Advances in cognitive psychology.

[48]  T. Hendler,et al.  Tracing the Neural Carryover Effects of Interpersonal Anger on Resting-State fMRI in Men and Their Relation to Traumatic Stress Symptoms in a Subsample of Soldiers , 2017, Front. Behav. Neurosci..

[49]  R. Blair Considering anger from a cognitive neuroscience perspective. , 2012, Wiley interdisciplinary reviews. Cognitive science.

[50]  Nicole R. Zürcher,et al.  Hypersensitivity to low intensity fearful faces in autism when fixation is constrained to the eyes , 2017, Human brain mapping.

[51]  A. Sack,et al.  The Role of the Insular Cortex in Retaliation , 2016, PloS one.

[52]  Diego L. Lorca-Puls,et al.  How right hemisphere damage after stroke can impair speech comprehension , 2018, Brain : a journal of neurology.

[53]  René Hurlemann,et al.  Segregating intra-amygdalar responses to dynamic facial emotion with cytoarchitectonic maximum probability maps , 2008, Journal of Neuroscience Methods.

[54]  A. Grecucci,et al.  Dysregulated Anxiety and Dysregulating Defenses: Toward an Emotion Regulation Informed Dynamic Psychotherapy , 2018, Front. Psychol..

[55]  C. Montag,et al.  The influence of the OPRM1 (A118G) polymorphism on behavioral and neural correlates of aggression in healthy males , 2019, Neuropharmacology.

[56]  Didier Grandjean,et al.  Modulation of Auditory Spatial Attention by Angry Prosody: An fMRI Auditory Dot-Probe Study , 2016, Front. Neurosci..

[57]  M. Jones-Gotman,et al.  Bilateral Skin Conductance Responses to Emotional Faces , 2012, Applied Psychophysiology and Biofeedback.

[58]  Mark M. Schira,et al.  Cognitive : Executive Function Don ' t look back in anger : Neural correlates of reappraisal , analytical rumination , and angry rumination during recall of an anger-inducing autobiographical memory ☆ , 2011 .

[59]  William A. Cunningham,et al.  Neural components of social evaluation. , 2003, Journal of personality and social psychology.

[60]  Clinton D. Kilts,et al.  Dissociable Neural Pathways Are Involved in the Recognition of Emotion in Static and Dynamic Facial Expressions , 2003, NeuroImage.

[61]  L. F. Barrett,et al.  From affect to control: Functional specialization of the insula in motivation and regulation , 2017, bioRxiv.

[62]  Cassandra L. Govan,et al.  Excluded emotions: The role of anger in antisocial responses to ostracism , 2008 .

[63]  U. Krämer,et al.  Avoidant Responses to Interpersonal Provocation Are Associated with Increased Amygdala and Decreased Mentalizing Network Activity , 2017, eNeuro.

[64]  A. Villringer,et al.  Alexithymic features and the labeling of brief emotional facial expressions – An fMRI study , 2014, Neuropsychologia.

[65]  Brent L. Hughes,et al.  Prefrontal-Subcortical Pathways Mediating Successful Emotion Regulation , 2008, Neuron.

[66]  U. Habel,et al.  The impact of social exclusion vs. inclusion on subjective and hormonal reactions in females and males☆ , 2013, Psychoneuroendocrinology.

[67]  Alan G. Sanfey,et al.  Reappraising social emotions: the role of inferior frontal gyrus, temporo-parietal junction and insula in interpersonal emotion regulation , 2013, Front. Hum. Neurosci..

[68]  T. Robbins,et al.  Effects of Acute Tryptophan Depletion on Prefrontal-Amygdala Connectivity While Viewing Facial Signals of Aggression , 2012, Biological Psychiatry.

[69]  Didier Grandjean,et al.  Talking in Fury: The Cortico-Subcortical Network Underlying Angry Vocalizations. , 2015, Cerebral cortex.

[70]  Sakiko Yoshikawa,et al.  The amygdala processes the emotional significance of facial expressions: an fMRI investigation using the interaction between expression and face direction , 2004, NeuroImage.

[71]  A. Damasio,et al.  Subcortical and cortical brain activity during the feeling of self-generated emotions , 2000, Nature Neuroscience.

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

[73]  Thomas F Münte,et al.  Orbitofrontal Cortex Reactivity to Angry Facial Expression in a Social Interaction Correlates with Aggressive Behavior. , 2015, Cerebral cortex.

[74]  Petra Schwingenschuh,et al.  Facial Emotion Recognition in Parkinson's Disease: An fMRI Investigation , 2015, PloS one.

[75]  K. Luan Phan,et al.  Perceptual load modulates anterior cingulate cortex response to threat distractors in generalized social anxiety disorder , 2014, Biological Psychology.

[76]  M. Guazzelli,et al.  Neural correlates of imaginal aggressive behavior assessed by positron emission tomography in healthy subjects. , 2000, The American journal of psychiatry.

[77]  C. Büchel,et al.  The neural bases of emotion regulation , 2015, Nature Reviews Neuroscience.

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

[79]  Birgit Derntl,et al.  Intrinsic functional connectivity underlying successful emotion regulation of angry faces. , 2016, Social cognitive and affective neuroscience.

[80]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex: one decade on , 2014, Trends in Cognitive Sciences.

[81]  Angela R. Laird,et al.  Activation likelihood estimation meta-analysis revisited , 2012, NeuroImage.

[82]  Niels Birbaumer,et al.  Evidence for a different role of the ventral and dorsal medial prefrontal cortex for social reactive aggression: An interactive fMRI study , 2007, NeuroImage.

[83]  Hugo D Critchley,et al.  Imitating expressions: emotion-specific neural substrates in facial mimicry. , 2006, Social cognitive and affective neuroscience.

[84]  Alan G. Sanfey,et al.  Affective state and decision-making in the Ultimatum Game , 2006, Experimental Brain Research.

[85]  Craig E. L. Stark,et al.  When zero is not zero: The problem of ambiguous baseline conditions in fMRI , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[86]  M. McInnis,et al.  Reduced emotion processing efficiency in healthy males relative to females. , 2014, Social cognitive and affective neuroscience.

[87]  Darin D Dougherty,et al.  Ventromedial prefrontal cortex and amygdala dysfunction during an anger induction positron emission tomography study in patients with major depressive disorder with anger attacks. , 2004, Archives of general psychiatry.

[88]  M. Schira,et al.  Endogenous testosterone and cortisol modulate neural responses during induced anger control , 2013, Social neuroscience.

[89]  A. Sack,et al.  Out of control: evidence for anterior insula involvement in motor impulsivity and reactive aggression. , 2015, Social cognitive and affective neuroscience.

[90]  Simon Baron-Cohen,et al.  Empathizing with basic emotions: Common and discrete neural substrates , 2006, Social neuroscience.

[91]  Mary McMurran,et al.  Increasing Recognition of Happiness in Ambiguous Facial Expressions Reduces Anger and Aggressive Behavior , 2013, Psychological science.

[92]  Łukasz Żurawski,et al.  Neural Correlates of Facial Mimicry: Simultaneous Measurements of EMG and BOLD Responses during Perception of Dynamic Compared to Static Facial Expressions , 2018, Front. Psychol..

[93]  S. Taylor Aggressive behavior and physiological arousal as a function of provocation and the tendency to inhibit aggression. , 1967, Journal of personality.

[94]  K. Scherer,et al.  The voices of wrath: brain responses to angry prosody in meaningless speech , 2005, Nature Neuroscience.

[95]  K. Berridge Faculty Opinions recommendation of Putting feelings into words: affect labeling disrupts amygdala activity in response to affective stimuli. , 2007 .

[96]  D. Grandjean,et al.  Peripheral responses to attended and unattended angry prosody: a dichotic listening paradigm. , 2011, Psychophysiology.

[97]  Reginald B. Adams,et al.  Knowing Who's Boss: fMRI and ERP Investigations of Social Dominance Perception , 2008, Group processes & intergroup relations : GPIR.

[98]  Kin-yin. Mak,et al.  Neural bases of emotion regulation , 2009 .

[99]  John Duncan,et al.  The role of the right inferior frontal gyrus: inhibition and attentional control , 2010, NeuroImage.

[100]  Sylvia D. Kreibig,et al.  Autonomic nervous system activity in emotion: A review , 2010, Biological Psychology.

[101]  T. Iidaka,et al.  Frontal lobe networks for effective processing of ambiguously expressed emotions in humans , 2003, Neuroscience Letters.

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

[103]  R. Veit,et al.  Self‐regulation of regional cortical activity using real‐time fMRI: The right inferior frontal gyrus and linguistic processing , 2009, Human brain mapping.

[104]  C. Neuper,et al.  Cognitively preserved MS patients demonstrate functional differences in processing neutral and emotional faces , 2011, Brain Imaging and Behavior.

[105]  A. Lawrence,et al.  Functional neuroanatomy of emotions: A meta-analysis , 2003, Cognitive, affective & behavioral neuroscience.

[106]  C. Neuper,et al.  The functional correlates of face perception and recognition of emotional facial expressions as evidenced by fMRI , 2011, Brain Research.

[107]  Luca Passamonti,et al.  Connectivity from the ventral anterior cingulate to the amygdala is modulated by appetitive motivation in response to facial signals of aggression , 2008, NeuroImage.

[108]  Ruben C. Gur,et al.  Anger under Control: Neural Correlates of Frustration as a Function of Trait Aggression , 2013, PloS one.

[109]  Neural substrates involved in anger induced by audio-visual film clips among patients with alcohol dependency , 2016, Journal of Physiological Anthropology.

[110]  M. J. Kim,et al.  Identifying the Representational Structure of Affect Using fMRI , 2018, Affective science.

[111]  Angela R. Laird,et al.  Behavior, sensitivity, and power of activation likelihood estimation characterized by massive empirical simulation , 2016, NeuroImage.

[112]  R. Baron,et al.  Toward an Ecological Theory of Social Perception , 1983 .

[113]  A. Marsh,et al.  Distinct neural activation patterns underlie economic decisions in high and low psychopathy scorers. , 2014, Social cognitive and affective neuroscience.

[114]  J. Russell Core affect and the psychological construction of emotion. , 2003, Psychological review.

[115]  G. Gainotti The Role of the Right Hemisphere in Emotional and Behavioral Disorders of Patients With Frontotemporal Lobar Degeneration: An Updated Review , 2019, Front. Aging Neurosci..

[116]  Karl J. Friston,et al.  Anterior insular cortex and emotional awareness , 2013, The Journal of comparative neurology.

[117]  T. Hendler,et al.  Attenuating anger and aggression with neuromodulation of the vmPFC: A simultaneous tDCS-fMRI study , 2018, Cortex.

[118]  Wolfgang Grodd,et al.  Differential Influences of Emotion, Task, and Novelty on Brain Regions Underlying the Processing of Speech Melody , 2009, Journal of Cognitive Neuroscience.

[119]  K. Nakamura,et al.  Activation of the right inferior frontal cortex during assessment of facial emotion. , 1999, Journal of neurophysiology.

[120]  D. Shohamy,et al.  Ventromedial prefrontal-subcortical systems and the generation of affective meaning , 2012, Trends in Cognitive Sciences.

[121]  D. Lynam,et al.  Neural mechanisms of the rejection–aggression link , 2018, Social cognitive and affective neuroscience.

[122]  M. Potegal,et al.  International handbook of anger : constituent and concomitant biological, psychological, and social processes , 2010 .

[123]  W. Penfield,et al.  The insula; further observations on its function. , 1955, Brain : a journal of neurology.

[124]  Emily B. Myers,et al.  Neural Substrates of Processing Anger in Language: Contributions of Prosody and Semantics , 2016, Journal of psycholinguistic research.

[125]  Joydeep Srivastava,et al.  Coupling and decoupling of unfairness and anger in ultimatum bargaining , 2009 .

[126]  Talma Hendler,et al.  Anger Modulates Influence Hierarchies Within and Between Emotional Reactivity and Regulation Networks , 2018, Front. Behav. Neurosci..

[127]  M. Angstadt,et al.  Amygdala hyperactivation to angry faces in intermittent explosive disorder. , 2016, Journal of psychiatric research.

[128]  R. Adolphs Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

[129]  G. Hajcak,et al.  In the face of anger: startle modulation to graded facial expressions. , 2010, Psychophysiology.

[130]  M. Phillips,et al.  Orbitofrontal cortex response to angry faces in men with histories of suicide attempts. , 2008, The American journal of psychiatry.

[131]  Almut Engelien,et al.  Cognitive coping style modulates neural responses to emotional faces in healthy humans: a 3-T FMRI study. , 2007, Cerebral cortex.

[132]  Loraine K. Obler,et al.  Right hemisphere specialization for the identification of emotional words and sentences: Evidence from stroke patients , 1992, Neuropsychologia.

[133]  Lauren A. J. Kirby,et al.  Affective mapping: An activation likelihood estimation (ALE) meta-analysis , 2014, Brain and Cognition.

[134]  Vinod Goel,et al.  Syllogisms delivered in an angry voice lead to improved performance and engagement of a different neural system compared to neutral voice , 2015, Front. Hum. Neurosci..

[135]  S. Kotz,et al.  Recruitment of Language-, Emotion- and Speech-Timing Associated Brain Regions for Expressing Emotional Prosody: Investigation of Functional Neuroanatomy with fMRI , 2016, Front. Hum. Neurosci..

[136]  P. Fisher,et al.  Aggression‐related brain function assessed with the Point Subtraction Aggression Paradigm in fMRI , 2017, Aggressive behavior.

[137]  Yue-Jia Luo,et al.  Neural signatures of fairness‐related normative decision making in the ultimatum game: A coordinate‐based meta‐analysis , 2015, Human brain mapping.

[138]  A. Sanfey,et al.  Living Emotions, Avoiding Emotions: Behavioral Investigation of the Regulation of Socially Driven Emotions , 2013, Front. Psychology.

[139]  J C Mazziotta,et al.  Automated labeling of the human brain: A preliminary report on the development and evaluation of a forward‐transform method , 1997, Human brain mapping.

[140]  Gilles Pourtois,et al.  Emotion and attention interactions in social cognition: Brain regions involved in processing anger prosody , 2005, NeuroImage.

[141]  Simon B Eickhoff,et al.  Minimizing within‐experiment and within‐group effects in activation likelihood estimation meta‐analyses , 2012, Human brain mapping.

[142]  Mark W. Baldwin,et al.  Relational schemas and the processing of social information. , 1992 .

[143]  A. Lawrence,et al.  Appetitive Motivation Predicts the Neural Response to Facial Signals of Aggression , 2008, The Journal of Neuroscience.

[144]  Kristen A. Lindquist,et al.  The brain basis of emotion: A meta-analytic review , 2012, Behavioral and Brain Sciences.

[145]  A. Sanfey,et al.  Reappraising the ultimatum: an fMRI study of emotion regulation and decision making. , 2013, Cerebral cortex.

[146]  A. Arntz,et al.  Anger provocation in violent offenders leads to emotion dysregulation , 2017, Scientific Reports.

[147]  R. Bies,et al.  The Study of Revenge in the Workplace: Conceptual, Ideological, and Empirical Issues. , 2005 .

[148]  D. Bowers,et al.  Differences in startle reactivity during the perception of angry and fearful faces. , 2007, Emotion.

[149]  W. Güth,et al.  An experimental analysis of ultimatum bargaining , 1982 .

[150]  Christina M. Pawliczek,et al.  From provocation to aggression: the neural network , 2017, BMC Neuroscience.