Species sensitivity of early face and eye processing

Humans are better at recognizing human faces than faces of other species. However, it is unclear whether this species sensitivity can be seen at early perceptual stages of face processing and whether it involves species sensitivity for important facial features like the eyes. These questions were addressed by comparing the modulations of the N170 ERP component to faces, eyes and eyeless faces of humans, apes, cats and dogs, presented upright and inverted. Although all faces and isolated eyes yielded larger responses than the control object category (houses), the N170 was shorter and smaller to human than animal faces and larger to human than animal eyes. Most importantly, while the classic inversion effect was found for human faces, animal faces yielded no inversion effect or an opposite inversion effect, as seen for objects, suggesting a different neural process involved for humans faces compared to faces of other species. Thus, in addition to its general face and eye categorical sensitivity, the N170 appears particularly sensitive to the human species for both faces and eyes. The results are discussed in the context of a recent model of the N170 response involving face and eye sensitive neurons (Itier et al., 2007) where the eyes play a central role in face perception. The data support the intuitive idea that eyes are what make animal head fronts look face-like and that proficiency for the human species involves visual expertise for the human eyes.

[1]  D. Perrett,et al.  Evidence accumulation in cell populations responsive to faces: an account of generalisation of recognition without mental transformations , 1998, Cognition.

[2]  M. Eimer The face‐specific N170 component reflects late stages in the structural encoding of faces , 2000, Neuroreport.

[3]  Margot J. Taylor,et al.  Holistic Processing of Faces: Learning Effects with Mooney Faces , 2005, Journal of Cognitive Neuroscience.

[4]  C. Jacques,et al.  Early adaptation to repeated unfamiliar faces across viewpoint changes in the right hemisphere: Evidence from the N170 ERP component , 2009, Neuropsychologia.

[5]  Hiromitsu Kobayashi,et al.  Unique morphology of the human eye , 1997, Nature.

[6]  Margot J. Taylor,et al.  Spatiotemporal analysis of event-related potentials to upright, inverted, and contrast-reversed faces: effects on encoding and recognition. , 2004, Psychophysiology.

[7]  Roxane J. Itier,et al.  Face, eye and object early processing: What is the face specificity? , 2006, NeuroImage.

[8]  Natasa Kovacevic,et al.  Groupwise independent component decomposition of EEG data and partial least square analysis , 2007, NeuroImage.

[9]  Hisao Nishijo,et al.  Generators of Visual Evoked Potentials for Faces and Eyes in the Human Brain as Determined by Dipole Localization , 2004, Brain Topography.

[10]  R. Yin Looking at Upside-down Faces , 1969 .

[11]  Judith M. Shedden,et al.  Semantic Learning Modifies Perceptual Face Processing , 2009, Journal of Cognitive Neuroscience.

[12]  M. Eimer,et al.  Response profile of the face-sensitive N170 component: a rapid adaptation study. , 2010, Cerebral cortex.

[13]  D. Perrett,et al.  Visual neurones responsive to faces in the monkey temporal cortex , 2004, Experimental Brain Research.

[14]  N. Fox,et al.  Social perception in infants , 1985 .

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

[16]  A. J. Mistlin,et al.  Neurones responsive to faces in the temporal cortex: studies of functional organization, sensitivity to identity and relation to perception. , 1984, Human neurobiology.

[17]  G. Rousselet,et al.  Animal and human faces in natural scenes: How specific to human faces is the N170 ERP component? , 2004, Journal of vision.

[18]  Margot J. Taylor,et al.  Inversion and Contrast Polarity Reversal Affect both Encoding and Recognition Processes of Unfamiliar Faces: A Repetition Study Using ERPs , 2002, NeuroImage.

[19]  B. Renault,et al.  Electrophysiological correlates of facial decision: insights from upright and upside-down Mooney-face perception. , 2005, Brain research. Cognitive brain research.

[20]  S. Bentin,et al.  Domain specificity versus expertise: factors influencing distinct processing of faces , 2002, Cognition.

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

[22]  Mark H. Johnson,et al.  Gaze Following in Newborns , 2004 .

[23]  G. E. Edmonds,et al.  Direction of gaze effects on early face processing: eyes-only versus full faces. , 2001, Brain research. Cognitive brain research.

[24]  M Eimer,et al.  Does the face‐specific N170 component reflect the activity of a specialized eye processor? , 1998, Neuroreport.

[25]  T. Allison,et al.  Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli. , 1999, Cerebral cortex.

[26]  S. Schweinberger Neurophysiological Correlates of Face Recognition , 2011 .

[27]  M. Tarr,et al.  The N170 occipito‐temporal component is delayed and enhanced to inverted faces but not to inverted objects: an electrophysiological account of face‐specific processes in the human brain , 2000, Neuroreport.

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

[29]  B Renault,et al.  Differential processing of part-to-whole and part-to-part face priming: an ERP study. , 1999, Neuroreport.

[30]  Roxane J. Itier,et al.  Neural bases of eye and gaze processing: The core of social cognition , 2009, Neuroscience & Biobehavioral Reviews.

[31]  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.

[32]  Michèle Fabre-Thorpe,et al.  Animal and human faces in natural scenes: How specific to human faces is the N170 ERP component? , 2004, Journal of vision.

[33]  Margot J. Taylor,et al.  N170 or N1? Spatiotemporal differences between object and face processing using ERPs. , 2004, Cerebral cortex.

[34]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[35]  Mark H. Johnson,et al.  Eye contact detection in humans from birth , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[36]  I. Gauthier,et al.  How does the brain process upright and inverted faces? , 2002, Behavioral and cognitive neuroscience reviews.

[37]  Olivier Pascalis,et al.  Specialization of Neural Mechanisms Underlying Face Recognition in Human Infants , 2002, Journal of Cognitive Neuroscience.

[38]  Anthony Randal McIntosh,et al.  Early Face Processing Specificity: It's in the Eyes! , 2007, Journal of Cognitive Neuroscience.

[39]  N. Sagiv,et al.  Structural Encoding of Human and Schematic Faces: Holistic and Part-Based Processes , 2001, Journal of Cognitive Neuroscience.

[40]  T. Allison,et al.  Electrophysiological studies of human face perception. III: Effects of top-down processing on face-specific potentials. , 1999, Cerebral cortex.

[41]  N. Emery,et al.  The eyes have it: the neuroethology, function and evolution of social gaze , 2000, Neuroscience & Biobehavioral Reviews.

[42]  Hans Forssberg,et al.  Increased Brain Activity in Frontal and Parietal Cortex Underlies the Development of Visuospatial Working Memory Capacity during Childhood , 2002, Journal of Cognitive Neuroscience.

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

[44]  O. Pascalis,et al.  Is Face Processing Species-Specific During the First Year of Life? , 2002, Science.