Is the early modulation of brain activity by fearful facial expressions primarily mediated by coarse low spatial frequency information?

Rapidly decoding the emotional content of a face is an important skill for successful social behavior. Several Event Related brain Potential (ERP) have indicated that emotional expressions already influence brain activity as early as 100 ms. Some studies hypothesized that this early brain response to fear depends on coarse-magnocellular inputs, which are primarily driven by Low Spatial Frequency (LSF) cues. Until now however, evidence is inconclusive probably due to the divergent methods used to match luminance and contrast across spatial frequencies and emotional stimuli. In the present study, we measured ERPs to LSF and HSF faces with fearful or neutral expressions when contrast and luminance was matched across SF or not. Our findings clearly show that fearful facial expressions increases the amplitude of P1 (only for contrast-luminance equated images) and N170 in comparison to neutral faces but only in LSF faces, irrespective of contrast or luminance equalization, further suggesting that LSF information plays a crucial role in the early brain responses to fear. Furthermore, we found that, irrespective of luminance or contrast equalization, N170 occurred faster when perceiving LSF faces than HSF faces, again emphasizing the primacy of LSF processing in early face perception.

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

[2]  Le Song,et al.  The ‘when’ and ‘where’ of perceiving signals of threat versus non-threat , 2006, NeuroImage.

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

[4]  I. Craw,et al.  Effects of high-pass and low-pass spatial filtering on face identification , 1996, Perception & psychophysics.

[5]  S. Luck,et al.  Sources of attention-sensitive visual event-related potentials , 2005, Brain Topography.

[6]  Leanne M Williams,et al.  Mapping the time course of nonconscious and conscious perception of fear: An integration of central and peripheral measures , 2004, Human brain mapping.

[7]  A. Klistorner,et al.  Separate magnocellular and parvocellular contributions from temporal analysis of the multifocal VEP , 1997, Vision Research.

[8]  R. Ihl,et al.  Electrophysiological correlates of emotional and structural face processing in humans , 2000, Neuroscience Letters.

[9]  Dietrich Lehmann,et al.  Affective judgments of faces modulate early activity (approximately 160 ms) within the fusiform gyri. , 2002, NeuroImage.

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

[11]  J. Bullier,et al.  Functional streams in occipito-frontal connections in the monkey , 1996, Behavioural Brain Research.

[12]  T. Allison,et al.  Electrophysiological Studies of Face Perception in Humans , 1996, Journal of Cognitive Neuroscience.

[13]  Patrik Vuilleumier,et al.  Time course and specificity of event-related potentials to emotional expressions , 2004, Neuroreport.

[14]  M. Eimer,et al.  The role of spatial frequency information for ERP components sensitive to faces and emotional facial expression. , 2005, Brain research. Cognitive brain research.

[15]  B. Rossion,et al.  Task modulation of brain activity related to familiar and unfamiliar face processing: an ERP study , 1999, Clinical Neurophysiology.

[16]  Urs Maurer,et al.  The face-specific N170 component is modulated by emotional facial expression , 2007, Behavioral and Brain Functions.

[17]  J R Lishman,et al.  Temporal Integration of Spatially Filtered Visual Images , 1992, Perception.

[18]  P. Bex,et al.  Spatial frequency, phase, and the contrast of natural images. , 2002, Journal of the Optical Society of America. A, Optics, image science, and vision.

[19]  B. Rossion.  Picture-plane inversion leads to qualitative changes of face perception. , 2008, Acta psychologica.

[20]  M. Harris.  Estimation of Time-to-Contact from Retinal Flow , 1997 .

[21]  Bruno Rossion,et al.  Early lateralization and orientation tuning for face, word, and object processing in the visual cortex , 2003, NeuroImage.

[22]  C. Jacques,et al.  The Speed of Individual Face Categorization , 2006, Psychological science.

[23]  R. Hari,et al.  Face recognition and cortical responses show similar sensitivity to noise spatial frequency. , 2005, Cerebral cortex.

[24]  H Stanislaw,et al.  Calculation of signal detection theory measures , 1999, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[25]  R. Henson,et al.  Electrophysiological and haemodynamic correlates of face perception, recognition and priming. , 2003, Cerebral cortex.

[26]  Bruno Rossion,et al.  Faces are "spatial"--holistic face perception is supported by low spatial frequencies. , 2006, Journal of experimental psychology. Human perception and performance.

[27]  E. Gordon,et al.  A Temporal Dissociation of Subliminal versus Supraliminal Fear Perception: An Event-related Potential Study , 2004, Journal of Cognitive Neuroscience.

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

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

[30]  D. Maurer,et al.  The many faces of configural processing , 2002, Trends in Cognitive Sciences.

[31]  H. Halit,et al.  Is high-spatial frequency information used in the early stages of face detection? , 2006, Brain Research.

[32]  Margot J. Taylor,et al.  Early processing of the six basic facial emotional expressions. , 2003, Brain research. Cognitive brain research.

[33]  Dietrich Lehmann,et al.  Affective Judgments of Faces Modulate Early Activity (∼160 ms) within the Fusiform Gyri , 2002, NeuroImage.

[34]  D. Lehmann,et al.  Rapid emotional face processing in the human right and left brain hemispheres: an ERP study. , 1999, Neuroreport.

[35]  M. Gazzaniga,et al.  Combined spatial and temporal imaging of brain activity during visual selective attention in humans , 1994, Nature.

[36]  Tetsuya Iidaka,et al.  Spatial frequency of visual image modulates neural responses in the temporo-occipital lobe. An investigation with event-related fMRI. , 2004, Brain research. Cognitive brain research.

[37]  Lucy S. Petro,et al.  Dynamics of Visual Information Integration in the Brain for Categorizing Facial Expressions , 2007, Current Biology.

[38]  A. Holmes,et al.  The involvement of distinct visual channels in rapid attention towards fearful facial expressions , 2005 .

[39]  C. Jacques,et al.  Concurrent processing reveals competition between visual representations of faces , 2004, Neuroreport.

[40]  J. Hsieh,et al.  The effects of face spatial frequencies on cortical processing revealed by magnetoencephalography , 2005, Neuroscience Letters.

[41]  C. Tardif,et al.  Spatial Frequency and Face Processing in Children with Autism and Asperger Syndrome , 2004, Journal of autism and developmental disorders.

[42]  M. Eimer,et al.  The processing of emotional facial expression is gated by spatial attention: evidence from event-related brain potentials. , 2003, Brain research. Cognitive brain research.

[43]  S. Campanella,et al.  Categorical Perception of Happiness and Fear Facial Expressions: An ERP Study , 2002, Journal of Cognitive Neuroscience.

[44]  I. Gauthier,et al.  Spatial scale contribution to early visual differences between face and object processing. , 2003, Brain research. Cognitive brain research.

[45]  A. Jedynak,et al.  Rapid extraction of emotional expression: evidence from evoked potential fields during brief presentation of face stimuli , 2003, Neuropsychologia.

[46]  J. Fagot,et al.  Categorizing facial identities, emotions, and genders: attention to high- and low-spatial frequencies by children and adults. , 2005, Journal of experimental child psychology.

[47]  T. Allison,et al.  Electrophysiological studies of human face perception. II: Response properties of face-specific potentials generated in occipitotemporal cortex. , 1999, Cerebral cortex.

[48]  Nicholas Costen,et al.  One extreme or the other or perhaps the golden mean? Issues of spatial resolution in face processing , 1999 .

[49]  C. Deruelle,et al.  Attention to low- and high-spatial frequencies in categorizing facial identities, emotions and gender in children with autism , 2008, Brain and Cognition.

[50]  H. Engeland,et al.  Face processing in Pervasive Developmental Disorder (PDD): the roles of expertise and spatial frequency , 2007, Journal of Neural Transmission.

[51]  John H. R. Maunsell,et al.  Visual response latencies of magnocellular and parvocellular LGN neurons in macaque monkeys , 1999, Visual Neuroscience.

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

[53]  E. Halgren,et al.  Cognitive response profile of the human fusiform face area as determined by MEG. , 2000, Cerebral cortex.

[54]  M. Roy,et al.  Contrast dependency of VEPs as a function of spatial frequency: the parvocellular and magnocellular contributions to human VEPs. , 2001, Spatial vision.

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

[56]  J R Lishman,et al.  Evidence for the View That Temporospatial Integration in Vision is Temporally Anisotropic , 1997, Perception.

[57]  S. Crewther,et al.  A role for the ‘magnocellular advantage’ in visual impairments in neurodevelopmental and psychiatric disorders , 2007, Neuroscience & Biobehavioral Reviews.

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

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

[60]  J. Stekelenburg,et al.  The neural correlates of perceiving human bodies: an ERP study on the body-inversion effect , 2004, Neuroreport.

[61]  T. Hendler,et al.  Feeling or Features Different Sensitivity to Emotion in High-Order Visual Cortex and Amygdala , 2001, Neuron.

[62]  D. Jeffreys,et al.  The influence of spatial frequency on the reaction times and evoked potentials recorded to grating pattern stimuli , 1985, Vision Research.

[63]  Sara López-Martín,et al.  An electrophysiological study on the interaction between emotional content and spatial frequency of visual stimuli , 2007, Neuropsychologia.

[64]  N. Guyader,et al.  How Diagnostic are Spatial Frequencies for Fear Recognition , 2005 .

[65]  C. E. Schroeder,et al.  Timing and distribution of flash-evoked activity in the lateral geniculate nucleus of the alert monkey , 1989, Brain Research.

[66]  Wolfram Boucsein,et al.  Modification of N170 by different emotional expression of schematic faces , 2007, Biological Psychology.

[67]  Rémy Versace,et al.  Role of spatial frequencies and exposure duration in face processing : potential consequences on the memory format of facial representations , 1992 .

[68]  H. Wilson,et al.  Quantifying facial expression recognition across viewing conditions , 2006, Vision Research.

[69]  Erin M. Harley,et al.  Why is it easier to identify someone close than far away? , 2005, Psychonomic Bulletin & Review.

[70]  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.

[71]  I. Craw,et al.  Spatial Content and Spatial Quantisation Effects in Face Recognition , 1994, Perception.

[72]  Beatrice de Gelder,et al.  Context influences early perceptual analysis of faces--an electrophysiological study. , 2006, Cerebral cortex.

[73]  D. Grandjean,et al.  Electrophysiological correlates of rapid spatial orienting towards fearful faces. , 2004, Cerebral cortex.

[74]  Milena Mihaylova,et al.  Peripheral and central delay in processing high spatial frequencies: reaction time and VEP latency studies , 1999, Vision Research.

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

[76]  J. Moran,et al.  Sensation and perception , 1980 .

[77]  D. Grandjean,et al.  Enhanced extrastriate visual response to bandpass spatial frequency filtered fearful faces: Time course and topographic evoked‐potentials mapping , 2005, Human brain mapping.

[78]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.