Neural processing of dynamic emotional facial expressions in psychopaths

Facial expressions play a critical role in social interactions by eliciting rapid responses in the observer. Failure to perceive and experience a normal range and depth of emotion seriously impact interpersonal communication and relationships. As has been demonstrated across a number of domains, abnormal emotion processing in individuals with psychopathy plays a key role in their lack of empathy. However, the neuroimaging literature is unclear as to whether deficits are specific to particular emotions such as fear and perhaps sadness. Moreover, findings are inconsistent across studies. In the current experiment, 80 incarcerated adult males scoring high, medium, and low on the Hare Psychopathy Checklist-Revised (PCL-R) underwent functional magnetic resonance imaging (fMRI) scanning while viewing dynamic facial expressions of fear, sadness, happiness, and pain. Participants who scored high on the PCL-R showed a reduction in neuro-hemodynamic response to all four categories of facial expressions in the face processing network (inferior occipital gyrus, fusiform gyrus, and superior temporal sulcus (STS)) as well as the extended network (inferior frontal gyrus and orbitofrontal cortex (OFC)), which supports a pervasive deficit across emotion domains. Unexpectedly, the response in dorsal insula to fear, sadness, and pain was greater in psychopaths than non-psychopaths. Importantly, the orbitofrontal cortex and ventromedial prefrontal cortex (vmPFC), regions critically implicated in affective and motivated behaviors, were significantly less active in individuals with psychopathy during the perception of all four emotional expressions.

[1]  Kent A. Kiehl,et al.  A cognitive neuroscience perspective on psychopathy: Evidence for paralimbic system dysfunction , 2006, Psychiatry Research.

[2]  Abigail A. Marsh,et al.  Deficits in facial affect recognition among antisocial populations: A meta-analysis , 2008, Neuroscience & Biobehavioral Reviews.

[3]  K. Kiehl,et al.  An fMRI study of affective perspective taking in individuals with psychopathy: imagining another in pain does not evoke empathy , 2013, Front. Hum. Neurosci..

[4]  S. Rombouts,et al.  Behavioral and neural reactions to emotions of others in the distribution of resources , 2013, Social neuroscience.

[5]  Lesley K. Fellows,et al.  Ventromedial Frontal Lobe Plays a Critical Role in Facial Emotion Recognition , 2008, Journal of Cognitive Neuroscience.

[6]  T. Rosenthal,et al.  Vicarious classical conditioning as a function of arousal level. , 1966, Journal of personality and social psychology.

[7]  L. F. Barrett,et al.  Handbook of emotions, 2nd ed. , 2000 .

[8]  A. Ishai,et al.  Distributed neural systems for the generation of visual images , 2000, NeuroImage.

[9]  J. Decety Dissecting the Neural Mechanisms Mediating Empathy , 2011 .

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

[11]  J. Licinio New editorial policies: content and electronic submission , 2002, Molecular Psychiatry.

[12]  J. Decety,et al.  The Oxford handbook of social neuroscience , 2011 .

[13]  D. Schutter,et al.  Unmasking feigned sanity: A neurobiological model of emotion processing in primary psychopathy , 2006, Cognitive neuropsychiatry.

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

[15]  Thomas E. Nichols,et al.  Optimization of experimental design in fMRI: a general framework using a genetic algorithm , 2003, NeuroImage.

[16]  J. Newman,et al.  Recognition of facial affect in psychopathic offenders. , 2006, Journal of abnormal psychology.

[17]  J. Decety,et al.  Dissociation between affective sharing and emotion understanding in juvenile psychopaths , 2012, Development and Psychopathology.

[18]  J. Decety,et al.  The Role of Affect in the Neurodevelopment of Morality , 2013 .

[19]  Tobias Brosch,et al.  Motivational Salience , 2012 .

[20]  Jean Decety,et al.  Brain response to empathy-eliciting scenarios involving pain in incarcerated individuals with psychopathy. , 2013, JAMA psychiatry.

[21]  K. R. Ridderinkhof,et al.  Conscious perception of errors and its relation to the anterior insula , 2010, Brain Structure and Function.

[22]  J. Decety,et al.  The functional architecture of human empathy. , 2004, Behavioral and cognitive neuroscience reviews.

[23]  Jia Liu,et al.  The Hierarchical Brain Network for Face Recognition , 2013, PloS one.

[24]  M. Herrmann,et al.  Emotions in motion: Dynamic compared to static facial expressions of disgust and happiness reveal more widespread emotion-specific activations , 2009, Brain Research.

[25]  Katherine D. Kinzler,et al.  The contribution of emotion and cognition to moral sensitivity: a neurodevelopmental study. , 2012, Cerebral cortex.

[26]  Geraint Rees,et al.  Inter-individual differences in empathy are reflected in human brain structure , 2012, NeuroImage.

[27]  Pierre Philippot,et al.  Decoding of facial expression of emotion in criminal psychopaths. , 2010, Journal of personality disorders.

[28]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[29]  E. Valentini,et al.  The role of anterior insula and anterior cingulate in empathy for pain. , 2010, Journal of neurophysiology.

[30]  V. Bruce,et al.  Dynamic Properties Influence the Perception of Facial Expressions , 2013, Perception.

[31]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[32]  L. F. Barrett,et al.  Handbook of Emotions , 1993 .

[33]  S. Killcross,et al.  A model of differential amygdala activation in psychopathy. , 2012, Psychological review.

[34]  J. Tangney,et al.  Psychopathy and Identification of Facial Expressions of Emotion. , 2008, Personality and individual differences.

[35]  M. Hoffman,et al.  Developmental synthesis of affect and cognition and its implications for altruistic motivation. , 1975 .

[36]  C. Keysers,et al.  Facial expressions: What the mirror neuron system can and cannot tell us , 2007, Social neuroscience.

[37]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[38]  K. Blair,et al.  The Psychopath: Emotion and the Brain , 2005 .

[39]  Jorge Moll,et al.  Psychopathy as a disorder of the moral brain: Fronto-temporo-limbic grey matter reductions demonstrated by voxel-based morphometry , 2008, NeuroImage.

[40]  Pierre Rainville,et al.  Brain responses to dynamic facial expressions of pain , 2006, Pain.

[41]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[42]  C. Zahn-Waxler,et al.  Concern for Others in the First Year of Life: Theory, Evidence, and Avenues for Research , 2013 .

[43]  M. Dadds,et al.  Attention to the eyes and fear-recognition deficits in child psychopathy , 2006, British Journal of Psychiatry.

[44]  Benjamin B. Lahey,et al.  Atypical empathic responses in adolescents with aggressive conduct disorder: A functional MRI investigation , 2009, Biological Psychology.

[45]  Fredrick C. Redlich,et al.  Social class and mental illness: Community study. , 1958 .

[46]  Vicki Bruce,et al.  Dynamic properties influence the perception of facial , 2001 .

[47]  Elinor McKone,et al.  Not just fear and sadness: Meta-analytic evidence of pervasive emotion recognition deficits for facial and vocal expressions in psychopathy , 2012, Neuroscience & Biobehavioral Reviews.

[48]  A. Marsh What can we learn about emotion by studying psychopathy? , 2013, Front. Hum. Neurosci..

[49]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

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

[51]  D. Zald The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[52]  Riitta Hari,et al.  The compassionate brain: humans detect intensity of pain from another's face. , 2006, Cerebral cortex.

[53]  A. Hariri,et al.  The neural signatures of distinct psychopathic traits , 2013, Social neuroscience.

[54]  Maarten A. S. Boksem,et al.  A Potential Role of the Inferior Frontal Gyrus and Anterior Insula in Cognitive Control, Brain Rhythms, and Event-Related Potentials , 2011, Front. Psychology.

[55]  R. Blair Should Affective Arousal be Grounded in Perception-Action Coupling? , 2011 .

[56]  Dan J Stein,et al.  Testosterone administration in women increases amygdala responses to fearful and happy faces , 2013, Psychoneuroendocrinology.

[57]  John O. Willis,et al.  Wechsler Adult Intelligence Scale–Third Edition , 2008 .

[58]  Shigeru Akamatsu,et al.  Dynamic Properties Influence the Perception of Facial Expressions , 2001, Perception.

[59]  R. Adolphs,et al.  Annals of the New York Academy of Sciences What Does the Amygdala Contribute to Social Cognition? , 2022 .

[60]  J. Haxby,et al.  Human neural systems for face recognition and social communication , 2002, Biological Psychiatry.

[61]  Robert T. Knight,et al.  Neural activity during social signal perception correlates with self-reported empathy , 2010, Brain Research.

[62]  N. Rempel-Clower,et al.  Role of Orbitofrontal Cortex Connections in Emotion , 2007, Annals of the New York Academy of Sciences.

[63]  K. Roelofs,et al.  Psychopaths lack the automatic avoidance of social threat: Relation to instrumental aggression , 2012, Psychiatry Research.

[64]  K. R. Ridderinkhof,et al.  Error Awareness and Salience Processing in the Oddball Task: Shared Neural Mechanisms , 2012, Front. Hum. Neurosci..

[65]  Gesine L. Alders,et al.  Do fearful eyes activate empathy-related brain regions in individuals with callous traits? , 2012, Social cognitive and affective neuroscience.

[66]  K. Scherer,et al.  Studying the dynamics of emotional expression using synthesized facial muscle movements. , 2000, Journal of personality and social psychology.

[67]  Claus Lamm,et al.  The Neural Substrate of Human Empathy: Effects of Perspective-taking and Cognitive Appraisal , 2007, Journal of Cognitive Neuroscience.

[68]  T. Singer,et al.  The Social Neuroscience of Empathy , 2009, Annals of the New York Academy of Sciences.

[69]  Sheilagh Hodgins,et al.  Ventral frontal deficits in psychopathy: Neuropsychological test findings , 1995, Neuropsychologia.

[70]  J. Decety,et al.  Passive and Motivated Perception of Emotional Faces: Qualitative and Quantitative Changes in the Face Processing Network , 2012, PloS one.

[71]  K. Kiehl,et al.  Reduced Prefrontal Connectivity in Psychopathy , 2011, The Journal of Neuroscience.

[72]  M. Dolan,et al.  Face affect recognition deficits in personality-disordered offenders: association with psychopathy , 2006, Psychological Medicine.

[73]  E. Leibenluft,et al.  Reduced amygdala response to fearful expressions in children and adolescents with callous-unemotional traits and disruptive behavior disorders. , 2008, The American journal of psychiatry.

[74]  D. G. Perry,et al.  Denial of suffering in the victim as a stimulus to violence in aggressive boys. , 1974, Child development.

[75]  M. Koenigs,et al.  Investigating the neural correlates of psychopathy: a critical review , 2011, Molecular Psychiatry.

[76]  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.

[77]  R. Blair,et al.  The emergence of psychopathy: Implications for the neuropsychological approach to developmental disorders , 2006, Cognition.

[78]  Naomi B. Pitskel,et al.  Three Systems of Insular Functional Connectivity Identified with Cluster Analysis , 2010, Cerebral cortex.

[79]  M. Annett A classification of hand preference by association analysis. , 1970, British journal of psychology.

[80]  Carl Senior,et al.  Dynamic Facial Expressions Evoke Distinct Activation in the Face Perception Network: A Connectivity Analysis Study , 2012, Journal of Cognitive Neuroscience.

[81]  Matthew L. Davidson,et al.  The neuroimaging of emotion. , 2008 .

[82]  D. Kosson,et al.  Impaired cognitive empathy in criminal psychopathy: evidence from a laboratory measure of empathic accuracy. , 2013, Journal of abnormal psychology.

[83]  Robert D. Hare,et al.  The Hare Psychopathy Checklist-Revised , 1996 .

[84]  Claus Lamm,et al.  Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain , 2011, NeuroImage.

[85]  C. Spielberger,et al.  STAXI-2 : State-Trait Anger Expression Inventory-2 : professional manual , 1999 .

[86]  Amishi P. Jha,et al.  Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain , 2005, NeuroImage.

[87]  A. Bechara,et al.  A somatic marker perspective of immoral and corrupt behavior , 2011, Social neuroscience.

[88]  K. Scherer,et al.  Handbook of affective sciences. , 2003 .

[89]  Pierre Rainville,et al.  Brain responses to facial expressions of pain: Emotional or motor mirroring? , 2010, NeuroImage.

[90]  Jean Decety,et al.  Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood. , 2010, Developmental science.

[91]  Jason B. Mattingley,et al.  Differential amygdala responses to happy and fearful facial expressions depend on selective attention , 2005, NeuroImage.