Neural processing of emotional faces requires attention

Attention gates the processing of stimuli relatively early in visual cortex. Yet, existing data suggest that emotional stimuli activate brain regions automatically, largely immune from attentional control. To resolve this puzzle, we used functional magnetic resonance imaging to first measure activation in regions that responded differentially to faces with emotional expressions (fearful and happy) compared with neutral faces. We then measured the modulation of these responses by attention, using a competing task with a high attentional load. Contrary to the prevailing view, all brain regions responding differentially to emotional faces, including the amygdala, did so only when sufficient attentional resources were available to process the faces. Thus, the processing of facial expression appears to be under top-down control.

[1]  O. John,et al.  Automatic vigilance: the attention-grabbing power of negative social information. , 1991, Journal of personality and social psychology.

[2]  P. Eslinger The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction edited by J.P. Aggleton, Wiley-Liss, 1992. $125.00 (xii + 615 pages) ISBN 0 4715 6129 0 , 1992, Trends in Neurosciences.

[3]  John P. Aggleton,et al.  The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction. , 1992 .

[4]  L. Goldstein The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction , 1992, The Yale Journal of Biology and Medicine.

[5]  Leslie G. Ungerleider,et al.  The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  A. Wells,et al.  Attention and Emotion: A Clinical Perspective , 1994 .

[7]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[8]  L. Cosmides From : The Cognitive Neurosciences , 1995 .

[9]  N. Lavie Perceptual load as a necessary condition for selective attention. , 1995, Journal of experimental psychology. Human perception and performance.

[10]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

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

[12]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[13]  Karl J. Friston,et al.  A multivariate analysis of PET activation studies , 1996, Human brain mapping.

[14]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

[15]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[16]  Ken Nakayama,et al.  Attentional requirements in a ‘preattentive’ feature search task , 1997, Nature.

[17]  Edward R. Watkins,et al.  Attention and emotion: A clinical perspective , 1997 .

[18]  C D Frith,et al.  Modulating irrelevant motion perception by varying attentional load in an unrelated task. , 1997, Science.

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

[20]  Mark S. Cohen,et al.  Parametric Analysis of fMRI Data Using Linear Systems Methods , 1997, NeuroImage.

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

[22]  R. Adolphs,et al.  The human amygdala in social judgment , 1998, Nature.

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

[24]  G. Schoenbaum,et al.  Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning , 1998, Nature Neuroscience.

[25]  N. Kanwisher,et al.  Covert visual attention modulates face-specific activity in the human fusiform gyrus: fMRI study. , 1998, Journal of neurophysiology.

[26]  R. Dolan,et al.  Conscious and unconscious emotional learning in the human amygdala , 1998, Nature.

[27]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[28]  A. Ohman,et al.  Fear appears fast: temporal course of startle reflex potentiation in animal fearful subjects. , 1999, Psychophysiology.

[29]  R. Knight,et al.  Transient interference of right hemispheric function due to automatic emotional processing , 2000, Neuropsychologia.

[30]  John Patrick Aggleton,et al.  The Amygdala : a functional analysis , 2000 .

[31]  A. Anderson,et al.  Lesions of the human amygdala impair enhanced perception of emotionally salient events , 2001, Nature.

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

[33]  D. Wilkin,et al.  Neuron , 2001, Brain Research.