Seeing the face through the eyes: a developmental perspective on face expertise.

Most people are experts in face recognition. We propose that the special status of this particular body part in telling individuals apart is the result of a developmental process that heavily biases human infants and children to attend towards the eyes of others. We review the evidence supporting this proposal, including neuroimaging results and studies in developmental disorders, like autism. We propose that the most likely explanation of infants' bias towards eyes is the fact that eye gaze serves important communicative functions in humans.

[1]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

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

[3]  D. Maurer,et al.  Expert face processing requires visual input to the right hemisphere during infancy , 2003, Nature Neuroscience.

[4]  M. Behrmann,et al.  Seeing it differently: visual processing in autism , 2006, Trends in Cognitive Sciences.

[5]  E. Blass,et al.  The ontogeny of face recognition: eye contact and sweet taste induce face preference in 9- and 12-week-old human infants. , 2001, Developmental psychology.

[6]  Sylvia M. J. Hains,et al.  Look at me: five-month-old infants' sensitivity to very small deviations in eye-gaze during social interactions , 1998 .

[7]  Jacqueline Nadel,et al.  Do Children with Autism have Expectancies about the Social Behaviour of Unfamiliar People? , 2000 .

[8]  A. Johnston,et al.  Categorizing sex and identity from the biological motion of faces , 2001, Current Biology.

[9]  S. Carey,et al.  Why faces are and are not special: an effect of expertise. , 1986, Journal of experimental psychology. General.

[10]  M. Tarr,et al.  Becoming a “Greeble” Expert: Exploring Mechanisms for Face Recognition , 1997, Vision Research.

[11]  Jon Driver,et al.  Seen Gaze-Direction Modulates Fusiform Activity and Its Coupling with Other Brain Areas during Face Processing , 2001, NeuroImage.

[12]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[13]  M. Tomasello.  Perceiving intentions and learning words in the second year of life , 2000 .

[14]  I. Gauthier,et al.  Expertise for cars and birds recruits brain areas involved in face recognition , 2000, Nature Neuroscience.

[15]  G McCarthy.  Event-related potentials and functional MRI: a comparison of localization in sensory, perceptual and cognitive tasks. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[16]  J. Werker,et al.  Infant preference for both male and female infant-directed talk: a developmental study of attentional and affective responsiveness. , 1989, Canadian journal of psychology.

[17]  V. Stone,et al.  The Body-Inversion Effect , 2003, Psychological science.

[18]  Michael W. Spratling,et al.  Gamma oscillations and object processing in the infant brain. , 2000, Science.

[19]  B. Hood,et al.  Eye remember you: the effects of gaze direction on face recognition in children and adults , 2003 .

[20]  D. Muir,et al.  Infant sensitivity to adult eye direction. , 1996, Child development.

[21]  C. Coffey,et al.  Textbook of pediatric neuropsychiatry , 1998 .

[22]  R. Adolphs,et al.  Impaired Recognition of Social Emotions following Amygdala Damage , 2002, Journal of Cognitive Neuroscience.

[23]  P. Schyns,et al.  Show Me the Features! Understanding Recognition From the Use of Visual Information , 2002, Psychological science.

[24]  S. Dehaene,et al.  The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. , 2001, Cerebral cortex.

[25]  Kim M. Dalton,et al.  Gaze fixation and the neural circuitry of face processing in autism , 2005, Nature Neuroscience.

[26]  S. de Schonen,et al.  Recognition of own-race and other-race faces by three-month-old infants. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[27]  A. Bailey,et al.  Face‐ and gaze‐sensitive neural responses in children with autism: a magnetoencephalographic study , 2006, The European journal of neuroscience.

[28]  G. Dawson,et al.  Brief Report: Recognition of Autism Spectrum Disorder Before One Year of Age: A Retrospective Study Based on Home Videotapes , 2000, Journal of autism and developmental disorders.

[29]  Mark H Johnson,et al.  Representing occluded objects in the human infant brain , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[30]  N. Ambady,et al.  Effects of Gaze on Amygdala Sensitivity to Anger and Fear Faces , 2003, Science.

[31]  V. Corkum,et al.  Patterns of movement in the first 6 months of life: new directions. , 1989, Canadian journal of psychology.

[32]  J. Langlois,et al.  Infants' Differential Processing of Female and Male Faces , 2006 .

[33]  N. Kanwisher,et al.  Does the human brain process objects of expertise like faces? A review of the evidence , 2005 .

[34]  Y. Bar-Haim,et al.  Nature and Nurture in Own-Race Face Processing , 2006, Psychological science.

[35]  P. Bloom.  How Children Learn the Meaning of Words and How LSA Does It ( Too ) , 2005 .

[36]  Mark H Johnson,et al.  Factors influencing newborns' preference for faces with eye contact. , 2006, Journal of experimental child psychology.

[37]  Evolutionary Origins of the Human Mother-Infant Relationship , 2006 .

[38]  Mark H. Johnson,et al.  Understanding the referential nature of looking: Infants’ preference for object-directed gaze , 2008, Cognition.

[39]  G. Dawson,et al.  Early recognition of children with autism: A study of first birthday home videotapes , 1994, Journal of autism and developmental disorders.

[40]  Mark H. Johnson,et al.  Newborns' preference for face-relevant stimuli: effects of contrast polarity. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[42]  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.

[43]  Anneli Kylliäinen,et al.  Skin Conductance Responses to Another Person’s Gaze in Children with Autism , 2006, Journal of autism and developmental disorders.

[44]  R. Rosenfeld.  Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[45]  E. Bullmore,et al.  Social intelligence in the normal and autistic brain: an fMRI study , 1999, The European journal of neuroscience.

[46]  S. Baron-Cohen,et al.  Is there an innate gaze module? Evidence from human neonates , 2000 .

[47]  F. Simion,et al.  Can a Nonspecific Bias Toward Top-Heavy Patterns Explain Newborns' Face Preference? , 2004, Psychological science.

[48]  J. Watson.  Smiling, cooing, and "the game." , 1972 .

[49]  Mark H. Johnson,et al.  Infants perceiving and acting on the eyes: tests of an evolutionary hypothesis. , 2003, Journal of experimental child psychology.

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

[51]  O. Pascalis,et al.  Three-month-olds, but not newborns, prefer own-race faces. , 2005, Developmental science.

[52]  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.

[53]  S. Levinson,et al.  Language Acquisition and Conceptual Development , 2001 .

[54]  Avi Chaudhuri,et al.  Reassessing the 3/4 view effect in face recognition , 2002, Cognition.

[55]  M. Corbetta,et al.  Extrastriate body area in human occipital cortex responds to the performance of motor actions , 2004, Nature Neuroscience.

[56]  Virginia Slaughter,et al.  Development of preferences for the human body shape in infancy , 2002, Cognition.

[57]  H. Ellis,et al.  Perceiving and remembering faces , 1983 .

[58]  Mark H. Johnson,et al.  Direct gaze modulates face recognition in young infants , 2007, Cognition.

[59]  N. Kanwisher,et al.  A Cortical Area Selective for Visual Processing of the Human Body , 2001, Science.

[60]  A. Lee,et al.  What's in a face? The case of autism. , 1988, British journal of psychology.

[61]  K. Nakamura,et al.  The human amygdala plays an important role in gaze monitoring. A PET study. , 1999, Brain : a journal of neurology.

[62]  R. Joseph,et al.  Holistic and part-based face recognition in children with autism. , 2003, Journal of child psychology and psychiatry, and allied disciplines.

[63]  Cindy M. Bukach,et al.  Beyond faces and modularity: the power of an expertise framework , 2006, Trends in Cognitive Sciences.

[64]  C. N. Macrae,et al.  Are You Looking at Me? Eye Gaze and Person Perception , 2002, Psychological science.

[65]  R. Aslin,et al.  Preference for infant-directed speech in the first month after birth. , 1990, Child development.

[66]  T. Striano,et al.  Crossmodal integration of emotional information from face and voice in the infant brain. , 2006, Developmental science.

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

[68]  Sidney R. Lehky.  Fine Discrimination of Faces can be Performed Rapidly , 2000, Journal of Cognitive Neuroscience.

[69]  Margot J. Taylor,et al.  Application of EEG, ERP and intracranial recordings to the investigation of cognitive functions in children , 2002 .

[70]  E. Courchesne,et al.  Face processing occurs outside the fusiform 'face area' in autism: evidence from functional MRI. , 2001, Brain : a journal of neurology.

[71]  Geraldine Dawson,et al.  Links between social and linguistic processing of speech in preschool children with autism: behavioral and electrophysiological measures. , 2005, Developmental science.

[72]  Teodora Gliga,et al.  Structural Encoding of Body and Face in Human Infants and Adults , 2005, Journal of Cognitive Neuroscience.

[73]  Dare A. Baldwin,et al.  Infants' ability to consult the speaker for clues to word reference , 1993, Journal of Child Language.

[74]  Philippe G Schyns,et al.  Using "Bubbles" with babies: a new technique for investigating the informational basis of infant perception. , 2006, Infant behavior & development.

[75]  J. Tanaka,et al.  Object categories and expertise: Is the basic level in the eye of the beholder? , 1991, Cognitive Psychology.

[76]  C. Lord,et al.  Follow-up of two-year-olds referred for possible autism. , 1995, Journal of child psychology and psychiatry, and allied disciplines.

[77]  Mark H. Johnson,et al.  Newborns' preferential tracking of face-like stimuli and its subsequent decline , 1991, Cognition.

[78]  G. Csibra,et al.  Social learning and social cognition: The case for pedagogy , 2006 .

[79]  H. Keller,et al.  Maternal Interactive Behaviour in Early Infancy and Later Attachment , 1999 .

[80]  S. Edelman,et al.  Human Brain Mapping 6:316–328(1998) � A Sequence of Object-Processing Stages Revealed by fMRI in the Human Occipital Lobe , 2022 .

[81]  H. Nicholson,et al.  Autistic children's ability to interpret faces: a research note. , 1989, Journal of child psychology and psychiatry, and allied disciplines.

[82]  Bruno Rossion,et al.  The fusiform face area is tuned for curvilinear patterns with more high-contrasted elements in the upper part , 2006, NeuroImage.

[83]  C. Frith,et al.  “Hey John”: Signals Conveying Communicative Intention toward the Self Activate Brain Regions Associated with “Mentalizing,” Regardless of Modality , 2003, The Journal of Neuroscience.

[84]  A. Senju,et al.  Does perceived direct gaze boost detection in adults and children with and without autism? The stare-in-the-crowd effect revisited , 2005 .

[85]  T. Kemper,et al.  Neuroanatomic observations of the brain in autism: a review and future directions , 2005, International Journal of Developmental Neuroscience.

[86]  Mark H. Johnson,et al.  Mechanisms of Eye Gaze Perception during Infancy , 2004, Journal of Cognitive Neuroscience.

[87]  J. Boucher,et al.  Unfamiliar face recognition in relatively able autistic children. , 1992, Journal of child psychology and psychiatry, and allied disciplines.

[88]  Daniel Stahl,et al.  Sensitivity to social contingencies between 1 and 3 months of age. , 2005, Developmental science.

[89]  Mark H. Johnson,et al.  Maternal personality and infants' neural and visual responsivity to facial expressions of emotion. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[90]  Frédéric Gosselin,et al.  Spatio-temporal dynamics of face recognition in a flash: it's in the eyes , 2004, Cogn. Sci..

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

[92]  Margot J. Taylor,et al.  The Faces of Development: A Review of Early Face Processing over Childhood , 2004, Journal of Cognitive Neuroscience.

[93]  Patrik Vuilleumier,et al.  Effects of perceived mutual gaze and gender on face processing and recognition memory , 2005 .

[94]  F. Volkmar,et al.  Impairments in monkey and human face recognition in 2-year-old toddlers with Autism Spectrum Disorder and Developmental Delay. , 2007, Developmental science.

[95]  T. Langdell,et al.  Recognition of faces: an approach to the study of autism. , 1978, Journal of child psychology and psychiatry, and allied disciplines.

[96]  D. Bishop,et al.  Face perception in children with autism and Asperger's syndrome. , 1994, Journal of child psychology and psychiatry, and allied disciplines.

[97]  F. Volkmar,et al.  Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. , 2002, Archives of general psychiatry.

[98]  Beatrice de Gelder,et al.  Face processing in autistics: Evidence for a generalised deficit? , 1996 .

[99]  R. Näätänen,et al.  Speech–sound-selective auditory impairment in children with autism: They can perceive but do not attend , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[100]  T. Gliga,et al.  Development of a view-invariant representation of the human head , 2007, Cognition.

[101]  Tetsuro Matsuzawa,et al.  Cognitive Development in Chimpanzees , 2021, Oxford Research Encyclopedia of Psychology.

[102]  Mark H. Johnson,et al.  The development and neural basis of referential gaze perception , 2006, Social neuroscience.

[103]  E. Bullmore,et al.  The amygdala theory of autism , 2000, Neuroscience & Biobehavioral Reviews.

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

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

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

[107]  Geraldine Dawson,et al.  Amygdalar volume and behavioral development in autism. , 2006, Archives of general psychiatry.

[108]  E. Murray,et al.  The amygdala and reward , 2002, Nature Reviews Neuroscience.

[109]  E K Warrington,et al.  Prosopagnosia: A Face-Specific Disorder , 1993, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[110]  G. Pourtois,et al.  Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging , 2007, Neuropsychologia.

[111]  M J Tarr,et al.  Perceptual categorization of cat and dog silhouettes by 3- to 4-month-old infants. , 2001, Journal of experimental child psychology.

[112]  Isabel Gauthier,et al.  Social interest and the development of cortical face specialization: what autism teaches us about face processing. , 2002, Developmental psychobiology.

[113]  Lionel Haward,et al.  Evaluating witness evidence: S. Llyod-Bostock and R. Clifford (Eds): Wiley, Chichester, England (1983). x + 305 pages. £19.95. , 1984 .

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

[115]  Mark H. Johnson,et al.  Social perception in the infant brain: gamma oscillatory activity in response to eye gaze. , 2007, Social cognitive and affective neuroscience.

[116]  G. Schwarzer,et al.  Face processing in 8-month-old infants: evidence for configural and analytical processing , 2003, Vision Research.

[117]  Mark H. Johnson,et al.  The perception of facial expressions in newborns , 2007, The European journal of developmental psychology.

[118]  G. Rhodes.  The evolutionary psychology of facial beauty. , 2006, Annual review of psychology.

[119]  J. Shepherd.  Studies of cue saliency , 1981 .

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

[121]  Isabel Gauthier,et al.  fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism , 2005, Neuropsychologia.

[122]  Mark H. Johnson,et al.  CONSPEC and CONLERN: a two-process theory of infant face recognition. , 1991, Psychological review.

[123]  C Umiltà,et al.  Preferential orienting to faces in newborns: a temporal-nasal asymmetry. , 1998, Journal of experimental psychology. Human perception and performance.

[124]  Azriel Rosenfeld,et al.  Face recognition: A literature survey , 2003, CSUR.

[125]  S. Carey.  Becoming a face expert. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[126]  J. Watson,et al.  Contingency perception and misperception in infancy: some potential implications for attachment. , 2001, Bulletin of the Menninger Clinic.

[127]  K. Jellinger.  Processes of Change in Brain and Cognitive Development Attention and Performance XXI , 2007 .

[128]  Frédéric Gosselin,et al.  Bubbles: a technique to reveal the use of information in recognition tasks , 2001, Vision Research.

[129]  V. Bruce,et al.  Remembering facial configurations , 1991, Cognition.

[130]  Cosimo Urgesi,et al.  Magnetic Stimulation of Extrastriate Body Area Impairs Visual Processing of Nonfacial Body Parts , 2004, Current Biology.

[131]  Mark H. Johnson,et al.  Processes of change in brain and cognitive development , 2005, Trends in Cognitive Sciences.

[132]  D. Maurer,et al.  Face Perception During Early Infancy , 1999 .