The importance of low spatial frequency information for recognising fearful facial expressions

A recent brain imaging study (Vuilleumier, Armony, Driver and Dolan 2003, Nature Neuroscience, 6, 624–631) has shown that amygdala responses to fearful expressions are preferentially driven by intact or low spatial frequency (LSF) images of faces, rather than by high spatial frequency (HSF) images. These results suggest that LSF components processed rapidly via magnocellular pathways within the visual system might be very efficiently conveyed to the amygdala for the rapid recognition of fearful expressions, perhaps via a subcortical pathway that activates the pulvinar and superior colliculus, but which bypasses any finer visual analysis of HSF cues in the striate and temporal extrastriate cortex. The purpose of this paper is to analyse the statistical properties of LSF compared with HSF and intact faces. The statistical analysis shows that the LSF components in faces, which are typically extracted rapidly by the visual system, provide a better source of information than HSF components for the correct categorisation of fearful expressions in faces. These results support the idea that visual pathways from the magnocellular visual neurons might be optimal, at a computational level, for the rapid classification of fearful emotional expressions in human faces.

[1]  J. P. Jones,et al.  The two-dimensional spatial structure of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[2]  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.

[3]  G. Cottrell,et al.  EMPATH: A Neural Network that Categorizes Facial Expressions , 2002, Journal of Cognitive Neuroscience.

[4]  L. Weiskrantz,et al.  Psychophysical and pupillometric study of spatial channels of visual processing in blindsight , 2002, Experimental Brain Research.

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

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

[7]  Garrison W. Cottrell,et al.  Organization of face and object recognition in modular neural network models , 1999, Neural Networks.

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

[9]  Joseph E LeDoux,et al.  Human Amygdala Activation during Conditioned Fear Acquisition and Extinction: a Mixed-Trial fMRI Study , 1998, Neuron.

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

[11]  A. Oliva,et al.  Dr. Angry and Mr. Smile: when categorization flexibly modifies the perception of faces in rapid visual presentations , 1999, Cognition.

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

[13]  L Weiskrantz,et al.  Non-conscious recognition of affect in the absence of striate cortex. , 1999, Neuroreport.

[14]  Christoph M. Michel,et al.  Two electrophysiological stages of spatial orienting towards fearful faces: early temporo-parietal activation preceding gain control in extrastriate visual cortex , 2005, NeuroImage.

[15]  S. Paradiso.  The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1998 .

[16]  A. Ohman,et al.  Masking the face: recognition of emotional facial expressions as a function of the parameters of backward masking. , 1993, Scandinavian journal of psychology.

[17]  Martial Mermillod,et al.  The role of bottom-up processing in perceptual categorization by 3- to 4-month-old infants: simulations and data. , 2004, Journal of experimental psychology. General.

[18]  L Weiskrantz,et al.  Early extrastriate activity without primary visual cortex in humans , 2000, Neuroscience Letters.

[19]  P. Vuilleumier,et al.  How brains beware: neural mechanisms of emotional attention , 2005, Trends in Cognitive Sciences.

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

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

[22]  A. Young,et al.  Configural information in facial expression perception. , 2000, Journal of experimental psychology. Human perception and performance.

[23]  L. Weiskrantz,et al.  Spatial and temporal response properties of residual vision in a case of hemianopia. , 1994, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[24]  M. Eimer,et al.  An ERP study on the time course of emotional face processing , 2002, Neuroreport.

[25]  M. Bar.  Visual objects in context , 2004, Nature Reviews Neuroscience.

[26]  A. Anderson,et al.  Neural Correlates of the Automatic Processing of Threat Facial Signals , 2022 .

[27]  D. Hubel,et al.  Segregation of form, color, movement, and depth: anatomy, physiology, and perception. , 1988, Science.

[28]  J. P. Jones,et al.  The two-dimensional spectral structure of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[29]  Nathalie Guyader,et al.  Improving generalisation skills in a neural network on the basis of neurophysiological data , 2005, Brain and Cognition.

[30]  R. Adolphs,et al.  Fear and the human amygdala , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  Nathalie Guyader,et al.  Image phase or amplitude? Rapid scene categorization is an amplitude-based process. , 2004, Comptes rendus biologies.

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

[33]  J. Daugman.  Uncertainty relation for resolution in space, spatial frequency, and orientation optimized by two-dimensional visual cortical filters. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[34]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[35]  P. Schiller,et al.  Composition of geniculostriate input ot superior colliculus of the rhesus monkey. , 1979, Journal of neurophysiology.

[36]  P. O. Bishop,et al.  Spatial vision. , 1971, Annual review of psychology.

[37]  Hanna Damasio,et al.  Single-neuron responses to emotional visual stimuli recorded in human ventral prefrontal cortex , 2001, Nature Neuroscience.

[38]  Martial Mermillod,et al.  Effect of temporal constraints on hemispheric asymmetries during spatial frequency processing , 2006, Brain and Cognition.

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

[40]  Nathalie Guyader,et al.  The coarse-to-fine hypothesis revisited: Evidence from neuro-computational modeling , 2005, Brain and Cognition.

[41]  P. Ekman.  Pictures of Facial Affect , 1976 .

[42]  J. Bullier.  Integrated model of visual processing , 2001, Brain Research Reviews.

[43]  Patrik Vuilleumier,et al.  Effects of Low-Spatial Frequency Components of Fearful Faces on Fusiform Cortex Activity , 2003, Current Biology.