The BOLD signal in the amygdala does not differentiate between dynamic facial expressions.

The amygdala has been considered to be essential for recognizing fear in other people's facial expressions. Recent studies shed doubt on this interpretation. Here we used movies of facial expressions instead of static photographs to investigate the putative fear selectivity of the amygdala using fMRI under more ecological conditions. The amygdala was found to respond more to movies of facial expressions than to pattern motion, but no differences were found between the responses to neutral, happy, disgusted and fearful facial expressions. This lack of emotional selectivity was replicated in three experiments using three different tasks (passive observation, delayed match to sample and viewing for imitation) and two different analysis methods (voxel-by-voxel and anatomical region of interest). Our data therefore provide strong support for the idea that under more ecologically valid conditions, the contribution of the amygdala towards the detection of fearful facial expressions must be more indirect than previously assumed.

[1]  A. Young,et al.  Task instructions modulate neural responses to fearful facial expressions , 2003, Biological Psychiatry.

[2]  Adam P. Morris,et al.  Amygdala Responses to Fearful and Happy Facial Expressions under Conditions of Binocular Suppression , 2004, The Journal of Neuroscience.

[3]  D. Amaral,et al.  The Amygdala Is Enlarged in Children But Not Adolescents with Autism; the Hippocampus Is Enlarged at All Ages , 2004, The Journal of Neuroscience.

[4]  Stephan Eliez,et al.  Amygdalar activation associated with positive and negative facial expressions , 2002, Neuroreport.

[5]  J. Mazziotta,et al.  Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[7]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[8]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[9]  R. J Dolan,et al.  Common and distinct neural responses during direct and incidental processing of multiple facial emotions , 2003, NeuroImage.

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

[11]  John D E Gabrieli,et al.  Amygdala Response to Happy Faces as a Function of Extraversion , 2002, Science.

[12]  S. Rauch,et al.  Brain habituation during repeated exposure to fearful and neutral faces: A functional MRI study , 2003, Brain Research Bulletin.

[13]  R. Adolphs.  Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala , 1997 .

[14]  D. Amaral,et al.  Topographic organization of cortical inputs to the lateral nucleus of the macaque monkey amygdala: A retrograde tracing study , 2000, The Journal of comparative neurology.

[15]  D. Weinberger,et al.  Functional neuroimaging of genetic variation in serotonergic neurotransmission , 2003, Genes, brain, and behavior.

[16]  G. McCarthy,et al.  Amygdala activation to sad pictures during high-field (4 tesla) functional magnetic resonance imaging. , 2005, Emotion.

[17]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

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

[19]  J. Mazziotta,et al.  Modulating emotional responses: effects of a neocortical network on the limbic system , 2000, Neuroreport.

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

[21]  G. Rizzolatti,et al.  Both of Us Disgusted in My Insula The Common Neural Basis of Seeing and Feeling Disgust , 2003, Neuron.

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

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

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

[25]  P. Holland,et al.  Amygdala circuitry in attentional and representational processes , 1999, Trends in Cognitive Sciences.

[26]  Itzhak Fried,et al.  Inhibitory and excitatory responses of single neurons in the human medial temporal lobe during recognition of faces and objects. , 2002, Cerebral cortex.

[27]  Yijun Liu,et al.  Neutral faces activate the amygdala during identity matching , 2006, NeuroImage.

[28]  Jennifer H. Pfeifer,et al.  Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders , 2006, Nature Neuroscience.

[29]  C. Koch,et al.  Category-specific visual responses of single neurons in the human medial temporal lobe , 2000, Nature Neuroscience.

[30]  D. Perrett,et al.  A differential neural response in the human amygdala to fearful and happy facial expressions , 1996, Nature.

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

[32]  A. McDonald.  Cortical pathways to the mammalian amygdala , 1998, Progress in Neurobiology.

[33]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[34]  C. Keysers,et al.  Towards a unifying neural theory of social cognition. , 2006, Progress in brain research.

[35]  R. Kahn,et al.  Lateralization of amygdala activation: a systematic review of functional neuroimaging studies , 2004, Brain Research Reviews.

[36]  Charles L. Wilson,et al.  Single Neuron Activity in Human Hippocampus and Amygdala during Recognition of Faces and Objects , 1997, Neuron.

[37]  Hans-Jochen Heinze,et al.  Asymmetrical Activation in the Human Brain during Processing of Fearful Faces , 2005, Current Biology.

[38]  H Nishijo,et al.  Single neuron responses in amygdala of alert monkey during complex sensory stimulation with affective significance , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  A. David,et al.  The human amygdala: a systematic review and meta-analysis of volumetric magnetic resonance imaging , 2002, Brain Research Reviews.

[40]  Michelle M. Wedig,et al.  Differential amygdala habituation to neutral faces in young and elderly adults , 2005, Neuroscience Letters.

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

[42]  Asaid Khateb,et al.  Discriminating emotional faces without primary visual cortices involves the right amygdala , 2005, Nature Neuroscience.

[43]  S. Rauch,et al.  A functional MRI study of human amygdala responses to facial expressions of fear versus anger. , 2001, Emotion.

[44]  D. Amaral,et al.  Some observations on cortical inputs to the macaque monkey amygdala: An anterograde tracing study , 2002, The Journal of comparative neurology.

[45]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[46]  Brian N. Pasley,et al.  Subcortical Discrimination of Unperceived Objects during Binocular Rivalry , 2004, Neuron.

[47]  Joseph E LeDoux,et al.  Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior , 2005, Neuron.

[48]  Michael Angstadt,et al.  Beyond threat: Amygdala reactivity across multiple expressions of facial affect , 2006, NeuroImage.

[49]  S. Rauch,et al.  Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli , 2001, Neuroreport.

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

[51]  J. Gabrieli,et al.  Rethinking Feelings: An fMRI Study of the Cognitive Regulation of Emotion , 2002, Journal of Cognitive Neuroscience.

[52]  Allan L. Reiss,et al.  Reliability and validity of MRI measurement of the amygdala and hippocampus in children with fragile X syndrome , 1997, Psychiatry Research: Neuroimaging.

[53]  Simon J Graham,et al.  An fMRI study investigating cognitive modulation of brain regions associated with emotional processing of visual stimuli , 2003, Neuropsychologia.

[54]  C. Büchel,et al.  The robustness of perception , 2005, The European journal of neuroscience.

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

[56]  H. Critchley,et al.  Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study , 2000, Human brain mapping.

[57]  C. J. Price,et al.  The Effect of Varying Stimulus Rate and Duration on Brain Activity during Reading , 1996, NeuroImage.

[58]  Joseph J. Paton,et al.  The primate amygdala represents the positive and negative value of visual stimuli during learning , 2006, Nature.