Amygdala responds to direct gaze in real but not in computer-generated faces

Computer-generated (CG) faces are an important visual interface for human-computer interaction in social contexts. Here we investigated whether the human brain processes emotion and gaze similarly in real and carefully matched CG faces. Real faces evoked greater responses in the fusiform face area than CG faces, particularly for fearful expressions. Emotional (angry and fearful) facial expressions evoked similar activations in the amygdala in real and CG faces. Direct as compared with averted gaze elicited greater fMRI responses in the amygdala regardless of facial expression but only for real and not for CG faces. We observed an interaction effect between gaze and emotion (i.e., the shared signal effect) in the right posterior temporal sulcus and other regions, but not in the amygdala, and we found no evidence for different shared signal effects in real and CG faces. Taken together, the present findings highlight similarities (emotional processing in the amygdala) and differences (overall processing in the fusiform face area, gaze processing in the amygdala) in the neural processing of real and CG faces.

[1]  Christopher J. Fox,et al.  Defining the face processing network: Optimization of the functional localizer in fMRI , 2009, Human brain mapping.

[2]  R. Dolan,et al.  Distinct spatial frequency sensitivities for processing faces and emotional expressions , 2003, Nature Neuroscience.

[3]  L. Jäncke,et al.  Human Neuroscience , 2022 .

[4]  Colin Camerer,et al.  Dissociating the Role of the Orbitofrontal Cortex and the Striatum in the Computation of Goal Values and Prediction Errors , 2008, The Journal of Neuroscience.

[5]  Jeffrey S. Maxwell,et al.  Human Amygdala Responsivity to Masked Fearful Eye Whites , 2004, Science.

[6]  J. Hietanen,et al.  Does it make a difference if I have an eye contact with you or with your picture? An ERP study. , 2011, Social cognitive and affective neuroscience.

[7]  Patrik Vuilleumier,et al.  Self-relevance processing in the human amygdala: gaze direction, facial expression, and emotion intensity. , 2009, Emotion.

[8]  W. Miltner,et al.  Effects of gaze direction, head orientation and valence of facial expression on amygdala activity. , 2014, Social cognitive and affective neuroscience.

[9]  J. Schultz,et al.  Natural facial motion enhances cortical responses to faces , 2009, Experimental Brain Research.

[10]  Mark H. Johnson,et al.  The eye contact effect: mechanisms and development , 2009, Trends in Cognitive Sciences.

[11]  A. Young,et al.  Reading the mind from eye gaze , 2002, Neuropsychologia.

[12]  R. Kleck,et al.  Perceived Gaze Direction and the Processing of Facial Displays of Emotion , 2003, Psychological science.

[13]  B. Rossion,et al.  Defining face perception areas in the human brain: A large-scale factorial fMRI face localizer analysis , 2012, Brain and Cognition.

[14]  K. Scherer,et al.  Interaction effects of perceived gaze direction and dynamic facial expression: Evidence for appraisal theories of emotion , 2007 .

[15]  Ewald Moser,et al.  Amygdala activation at 3T in response to human and avatar facial expressions of emotions , 2007, Journal of Neuroscience Methods.

[16]  Ikuko Mukai,et al.  A role of right middle frontal gyrus in reorienting of attention: a case study , 2015, Front. Syst. Neurosci..

[17]  Julie Grèzes,et al.  Anxiety dissociates the adaptive functions of sensory and motor response enhancements to social threats , 2015, eLife.

[18]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[19]  Mark H. Johnson.  Subcortical face processing , 2005, Nature Reviews Neuroscience.

[20]  L. Brothers,et al.  Mesial temporal neurons in the macaque monkey with responses selective for aspects of social stimuli , 1993, Behavioural Brain Research.

[21]  Joseph T. Devlin,et al.  Improving the reliability of functional localizers , 2011, NeuroImage.

[22]  E. Wagenmakers.  A practical solution to the pervasive problems ofp values , 2007, Psychonomic bulletin & review.

[23]  R. Goebel,et al.  Neural correlates of shape and surface reflectance information in individual faces , 2009, Neuroscience.

[24]  R. Kleck,et al.  Effects of direct and averted gaze on the perception of facially communicated emotion. , 2005, Emotion.

[25]  T. Iidaka.  Role of the fusiform gyrus and superior temporal sulcus in face perception and recognition: An empirical review , 2014 .

[26]  Alexis Hervais-Adelman,et al.  Amygdala Activation for Eye Contact Despite Complete Cortical Blindness , 2013, The Journal of Neuroscience.

[27]  B. de Gelder,et al.  Beyond localisation: a dynamical dual route account of face recognition. , 2001, Acta psychologica.

[28]  M. Tamietto,et al.  Neural bases of the non-conscious perception of emotional signals , 2010, Nature Reviews Neuroscience.

[29]  M. Bindemann,et al.  How do eye gaze and facial expression interact? , 2008 .

[30]  G. Rizzolatti,et al.  Brain Response to a Humanoid Robot in Areas Implicated in the Perception of Human Emotional Gestures , 2010, PloS one.

[31]  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.

[32]  Nouchine Hadjikhani,et al.  Pointing with the eyes: The role of gaze in communicating danger , 2008, Brain and Cognition.

[33]  Kenneth A. Norman,et al.  Graded Representations of Emotional Expressions in the Left Superior Temporal Sulcus , 2010, Front. Syst. Neurosci..

[34]  Andrew D. Engell,et al.  Facial expression and gaze-direction in human superior temporal sulcus , 2007, Neuropsychologia.

[35]  G. Pourtois,et al.  Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging , 2007, Neuropsychologia.

[36]  Mladen Sormaz,et al.  Neural responses to facial expressions support the role of the amygdala in processing threat. , 2014, Social cognitive and affective neuroscience.

[37]  A. Sack,et al.  A causal role for inferior parietal lobule in emotion body perception , 2015, Cortex.

[38]  B. de Gelder,et al.  Looking at the face and seeing the whole body. Neural basis of combined face and body expressions , 2017, Social cognitive and affective neuroscience.

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

[40]  D. Louis Collins,et al.  Unbiased average age-appropriate atlases for pediatric studies , 2011, NeuroImage.

[41]  K. Nakayama,et al.  RESPONSE PROPERTIES OF THE HUMAN FUSIFORM FACE AREA , 2000, Cognitive neuropsychology.

[42]  Emiliano Ricciardi,et al.  Distinct Neural Systems Involved in Agency and Animacy Detection , 2011, Journal of Cognitive Neuroscience.

[43]  Bruno Rossion,et al.  Personally familiar faces are perceived categorically in face‐selective regions other than the fusiform face area , 2010, The European journal of neuroscience.

[44]  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.

[45]  Annie Lang,et al.  How Realistic Should Avatars Be?An Initial fMRI Investigation of Activation of the Face Perception Network by Real and Animated Faces , 2015, J. Media Psychol. Theor. Methods Appl..

[46]  Michael E J Masson,et al.  A tutorial on a practical Bayesian alternative to null-hypothesis significance testing , 2011, Behavior research methods.

[47]  Patrice Renaud,et al.  Virtual Faces Expressing Emotions: An Initial Concomitant and Construct Validity Study , 2014, Front. Hum. Neurosci..

[48]  Alumit Ishai,et al.  Let’s face it: It’s a cortical network , 2008, NeuroImage.

[49]  K. Nakamura,et al.  The human amygdala plays an important role in gaze monitoring. A PET study. , 1999, Brain : a journal of neurology.

[50]  Mary J. Bravo,et al.  Perceptual discrimination of computer generated and photographic faces , 2012, Digit. Investig..

[51]  D. Sauter,et al.  Commonalities outweigh differences in the communication of emotions across human cultures [Letter to the editor] , 2013 .

[52]  A. Calder,et al.  Neural mechanisms of social attention , 2009, Trends in Cognitive Sciences.

[53]  Nirbhay N. Singh,et al.  Facial Expressions of Emotion , 1998 .

[54]  M. Botsch,et al.  Differential effects of face-realism and emotion on event-related brain potentials and their implications for the uncanny valley theory , 2017, Scientific Reports.

[55]  Reginald B. Adams,et al.  A 7 Tesla fMRI Study of Amygdala Responses to Fearful Faces , 2012, Brain Topography.

[56]  D. Perrett,et al.  Being the target of another’s emotion: a PET study , 2003, Neuropsychologia.

[57]  Skyler T. Hawk,et al.  Presentation and validation of the Radboud Faces Database , 2010 .

[58]  M. Frondel,et al.  On interaction effects , 2012 .

[59]  Conny F. Schmidt,et al.  Face perception is mediated by a distributed cortical network , 2005, Brain Research Bulletin.

[60]  J. Haxby,et al.  Neural systems for recognition of familiar faces , 2007, Neuropsychologia.

[61]  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.

[62]  Rainer Goebel,et al.  Integration of “what” and “where” in frontal cortex during visual imagery of scenes , 2012, NeuroImage.

[63]  Karl F. MacDorman,et al.  The Uncanny Valley [From the Field] , 2012, IEEE Robotics Autom. Mag..

[64]  Reginald B. Adams,et al.  Amygdala responses to averted vs direct gaze fear vary as a function of presentation speed. , 2012, Social cognitive and affective neuroscience.

[65]  N. Ambady,et al.  Effects of Gaze on Amygdala Sensitivity to Anger and Fear Faces , 2003, Science.

[66]  Rainer Goebel,et al.  Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single‐subject to cortically aligned group general linear model analysis and self‐organizing group independent component analysis , 2006, Human brain mapping.

[67]  Oliver G. B. Garrod,et al.  Facial expressions of emotion are not culturally universal , 2012, Proceedings of the National Academy of Sciences.

[68]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[69]  J. Nadel,et al.  Human brain spots emotion in non humanoid robots. , 2011, Social cognitive and affective neuroscience.

[70]  A. Raftery.  Bayes Factors and BIC , 1999 .

[71]  Thomas Straube,et al.  Increased amygdala activation to averted versus direct gaze in humans is independent of valence of facial expression , 2010, NeuroImage.

[72]  J. Decety,et al.  Brain Regions Involved in the Perception of Gaze: A PET Study , 1998, NeuroImage.