Self-relevance processing in the human amygdala: gaze direction, facial expression, and emotion intensity.

How the processing of emotional expression is influenced by perceived gaze remains a debated issue. Discrepancies between previous results may stem from differences in the nature of stimuli and task characteristics. Here we used a highly controlled set of computer-generated animated faces combining dynamic emotional expressions with varying intensity, and gaze shifts either directed at or averted from the observer. We predicted that perceived self-relevance of fearful faces would be higher with averted gaze-signaling a nearby danger; whereas conversely, direct gaze would be more relevant for angry faces-signaling aggressiveness. This interaction pattern was observed behaviorally for emotion intensity ratings, and neurally for functional magnetic resonance imaging activation in amygdala, as well as fusiform and medial prefrontal cortices, but only for mild- and not high-intensity expressions. These results support an involvement of human amygdala in the appraisal of self-relevance and reveal a crucial role of expression intensity in emotion and gaze interactions.

[1]  Garrison W. Cottrell,et al.  Transmitting and Decoding Facial Expressions , 2005, Psychological science.

[2]  J. Grafman,et al.  The Human Amygdala: An Evolved System for Relevance Detection , 2003, Reviews in the neurosciences.

[3]  Michael Andres,et al.  Dissociable roles of the human somatosensory and superior temporal cortices for processing social face signals , 2004, The European journal of neuroscience.

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

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

[6]  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.

[7]  S. Baron-Cohen,et al.  Gaze Perception Triggers Reflexive Visuospatial Orienting , 1999 .

[8]  Stefan Everling,et al.  Isolation of saccade inhibition processes: Rapid event-related fMRI of saccades and nogo trials , 2008, NeuroImage.

[9]  A. J. Mistlin,et al.  Visual cells in the temporal cortex sensitive to face view and gaze direction , 1985, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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

[11]  K. Scherer,et al.  Appraisal processes in emotion: Theory, methods, research. , 2001 .

[12]  K. Pelphrey,et al.  CURRENT DIRECTIONS IN PSYCHOLOGICAL SCIENCE Brain Mechanisms for Interpreting the Actions of Others From Biological-Motion Cues , 2022 .

[13]  P. Schyns,et al.  A mechanism for impaired fear recognition after amygdala damage , 2005, Nature.

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

[15]  Nikos K. Logothetis,et al.  Facial-Expression and Gaze-Selective Responses in the Monkey Amygdala , 2007, Current Biology.

[16]  Tom Johnstone,et al.  Inverse amygdala and medial prefrontal cortex responses to surprised faces , 2003, Neuroreport.

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

[18]  Christian Büchel,et al.  Elevated responses to constant facial emotions in different faces in the human amygdala: an fMRI study of facial identity and expression , 2004, BMC Neuroscience.

[19]  V. Bruce,et al.  Do the eyes have it? Cues to the direction of social attention , 2000, Trends in Cognitive Sciences.

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

[21]  P. Whalen Fear, Vigilance, and Ambiguity , 1998 .

[22]  E. Naito,et al.  Enhanced neural activity in response to dynamic facial expressions of emotion: an fMRI study. , 2004, Brain research. Cognitive brain research.

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

[24]  Jon Driver,et al.  Seen Gaze-Direction Modulates Fusiform Activity and Its Coupling with Other Brain Areas during Face Processing , 2001, NeuroImage.

[25]  G. McCarthy,et al.  Dynamic perception of facial affect and identity in the human brain. , 2003, Cerebral Cortex.

[26]  K. LaBar,et al.  Garner interference reveals dependencies between emotional expression and gaze in face perception. , 2007, Emotion.

[27]  A. Manstead,et al.  Social appraisal: the social world as object of and influence on appraisal processes , 2001 .

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

[29]  R. Dolan,et al.  Separate Coding of Different Gaze Directions in the Superior Temporal Sulcus and Inferior Parietal Lobule , 2007, Current Biology.

[30]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[31]  Dejan Todorović,et al.  Geometrical basis of perception of gaze direction , 2006, Vision Research.

[32]  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.

[33]  K. Scherer,et al.  Are facial expressions of emotion produced by categorical affect programs or dynamically driven by appraisal? , 2007, Emotion.

[34]  Cezary Biele,et al.  Sex differences in perception of emotion intensity in dynamic and static facial expressions , 2006, Experimental Brain Research.

[35]  N. George,et al.  When eye creates the contact! ERP evidence for early dissociation between direct and averted gaze motion processing , 2007, Neuropsychologia.

[36]  Michael J. Brammer,et al.  A preferential increase in the extrastriate response to signals of danger , 2003, NeuroImage.

[37]  C. Frith,et al.  The Neural Basis of Mentalizing , 2006, Neuron.

[38]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[39]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[40]  G. Glover,et al.  Reflecting upon Feelings: An fMRI Study of Neural Systems Supporting the Attribution of Emotion to Self and Other , 2004, Journal of Cognitive Neuroscience.

[41]  R. Dolan,et al.  Distant influences of amygdala lesion on visual cortical activation during emotional face processing , 2004, Nature Neuroscience.

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