Portraits or People? Distinct Representations of Face Identity in the Human Visual Cortex

Humans can identify individual faces under different viewpoints, even after a single encounter. We determined brain regions responsible for processing face identity across view changes after variable delays with several intervening stimuli, using event-related functional magnetic resonance imaging during a long-term repetition priming paradigm. Unfamiliar faces were presented sequentially either in a frontal or three-quarter view. Each face identity was repeated once after an unpredictable lag, with either the same or another viewpoint. Behavioral data showed significant priming in response time, irrespective of view changes. Brain imaging results revealed a reduced response in the lateral occipital and fusiform cortex with face repetition. Bilateral face-selective fusiform areas showed view-sensitive repetition effects, generalizing only from three-quarter to front-views. More medial regions in the left (but not in the right) fusiform showed repetition effects across all types of viewpoint changes. These results reveal that distinct regions within the fusiform cortex hold view-sensitive or view-invariant traces of novel faces, and that face identity is represented in a view-sensitive manner in the functionally defined face-selective areas of both hemispheres. In addition, our finding of a better generalization after exposure to a 3/4-view than to a front-view demonstrates for the first time a neural substrate in the fusiform cortex for the common recognition advantage of three-quarter faces. This pattern provides new insights into the nature of face representation in the human visual system.

[1]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[2]  Heinrich H. Bülthoff,et al.  Object recognition in man, monkey, and machine , 1999 .

[3]  T. Shallice,et al.  Face repetition effects in implicit and explicit memory tests as measured by fMRI. , 2002, Cerebral cortex.

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

[5]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[6]  A. Benton,et al.  Prosopagnosia and facial discrimination. , 1972, Journal of the neurological sciences.

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

[8]  Ken A. Paller,et al.  Neural correlates of perceptual contributions to nondeclarative memory for faces , 2006, NeuroImage.

[9]  H H Bülthoff,et al.  How are three-dimensional objects represented in the brain? , 1994, Cerebral cortex.

[10]  M. Seghier,et al.  A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. , 2003, Brain : a journal of neurology.

[11]  Sakiko Yoshikawa,et al.  The amygdala processes the emotional significance of facial expressions: an fMRI investigation using the interaction between expression and face direction , 2004, NeuroImage.

[12]  Edmund T. Rolls,et al.  Functions of the Primate Temporal Lobe Cortical Visual Areas in Invariant Visual Object and Face Recognition , 2000, Neuron.

[13]  R. Henson,et al.  Multiple levels of visual object constancy revealed by event-related fMRI of repetition priming , 2002, Nature Neuroscience.

[14]  S. Ullman,et al.  Generalization to Novel Images in Upright and Inverted Faces , 1993, Perception.

[15]  L. Cohen,et al.  The neural bases of prosopagnosia and pure alexia: recent insights from functional neuroimaging , 2006, Current opinion in neurology.

[16]  K. Nakayama,et al.  RESPONSE PROPERTIES OF THE HUMAN FUSIFORM FACE AREA , 2000, Cognitive neuropsychology.

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

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

[19]  Richard J. Vondruska,et al.  Salience, similes, and the asymmetry of similarity , 1985 .

[20]  M. Hasselmo,et al.  The responses of neurons in the cortex in the superior temporal sulcus of the monkey to band-pass spatial frequency filtered faces , 1987, Vision Research.

[21]  N. Kanwisher Domain specificity in face perception , 2000, Nature Neuroscience.

[22]  N. Kanwisher,et al.  The fusiform face area: a cortical region specialized for the perception of faces , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[23]  N. Valenza,et al.  Hyperfamiliarity for unknown faces after left lateral temporo-occipital venous infarction: a double dissociation with prosopagnosia. , 2003, Brain : a journal of neurology.

[24]  S. Ullman Three-dimensional object recognition based on the combination of views , 1998, Cognition.

[25]  R. Dolan,et al.  Contrast polarity and face recognition in the human fusiform gyrus , 1999, Nature Neuroscience.

[26]  G. Rhodes Lateralized processes in face recognition. , 1985, British journal of psychology.

[27]  M. Tarr,et al.  The Fusiform Face Area is Part of a Network that Processes Faces at the Individual Level , 2000, Journal of Cognitive Neuroscience.

[28]  V. Bruce,et al.  Recognition of unfamiliar faces , 2000, Trends in Cognitive Sciences.

[29]  M. Hasselmo,et al.  Object-centered encoding by face-selective neurons in the cortex in the superior temporal sulcus of the monkey , 2004, Experimental Brain Research.

[30]  Andreas Kleinschmidt,et al.  Scale invariant adaptation in fusiform face-responsive regions , 2004, NeuroImage.

[31]  D. Schacter,et al.  Perceptual specificity in visual object priming: functional magnetic resonance imaging evidence for a laterality difference in fusiform cortex , 2001, Neuropsychologia.

[32]  P. Schyns,et al.  Information and viewpoint dependence in face recognition , 1997, Cognition.

[33]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[34]  J. Cronly-Dillon,et al.  Visual Agnosias and Other Disturbances of Visual Perception and Cognition , 1991 .

[35]  N. Logothetis,et al.  Shape representation in the inferior temporal cortex of monkeys , 1995, Current Biology.

[36]  N. Kanwisher,et al.  The fusiform face area subserves face perception, not generic within-category identification , 2004, Nature Neuroscience.

[37]  R. Desimone,et al.  A neural mechanism for working and recognition memory in inferior temporal cortex. , 1991, Science.

[38]  H. Wilson,et al.  Size-invariant but viewpoint-dependent representation of faces , 2006, Vision Research.

[39]  V. Bruce Changing faces: visual and non-visual coding processes in face recognition. , 1982, British journal of psychology.

[40]  Gilles Pourtois,et al.  View-independent coding of face identity in frontal and temporal cortices is modulated by familiarity: an event-related fMRI study , 2005, NeuroImage.

[41]  Nikolaus F. Troje,et al.  How is bilateral symmetry of human faces used for recognition of novel views? , 1998, Vision Research.

[42]  D. Schacter,et al.  Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming. , 2000, Brain : a journal of neurology.

[43]  Keiji Tanaka,et al.  Functional architecture in monkey inferotemporal cortex revealed by in vivo optical imaging , 1998, Neuroscience Research.

[44]  A. Baddeley,et al.  Face recognition, pose and ecological validity. , 1987 .

[45]  T. Allison,et al.  Face-sensitive regions in human extrastriate cortex studied by functional MRI. , 1995, Journal of neurophysiology.

[46]  S. Edelman,et al.  Cue-Invariant Activation in Object-Related Areas of the Human Occipital Lobe , 1998, Neuron.

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

[48]  I Biederman,et al.  Neurocomputational bases of object and face recognition. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[49]  I. Biederman,et al.  Inferior Temporal Neurons Show Greater Sensitivity to Nonaccidental than to Metric Shape Differences , 2001, Journal of Cognitive Neuroscience.

[50]  A. Young,et al.  Understanding face recognition. , 1986, British journal of psychology.

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

[52]  T J Sejnowski,et al.  Learning viewpoint-invariant face representations from visual experience in an attractor network. , 1998, Network.

[53]  Wilma Koutstaal,et al.  Neural mechanisms of visual object priming: evidence for perceptual and semantic distinctions in fusiform cortex , 2003, NeuroImage.

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

[55]  T. Valentine,et al.  Recognizing Unfamiliar Faces: The Effects of Distinctiveness and View , 1999, The Quarterly journal of experimental psychology. A, Human experimental psychology.

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

[57]  F. Fang,et al.  Duration-dependent FMRI adaptation and distributed viewer-centered face representation in human visual cortex. , 2007, Cerebral cortex.

[58]  Thomas Vetter,et al.  Three-dimensional shape and two-dimensional surface reflectance contributions to face recognition: an application of three-dimensional morphing , 1999, Vision Research.

[59]  Alex M. Andrew,et al.  Object Recognition in Man, Monkey, and Machine , 2000 .

[60]  E. D. Burgund,et al.  Viewpoint-invariant and viewpoint-dependent object recognition in dissociable neural subsystems , 2000, Psychonomic bulletin & review.

[61]  S. Langton The Mutual Influence of Gaze and Head Orientation in the Analysis of Social Attention Direction , 2000, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[62]  Refractor Vision , 2000, The Lancet.

[63]  A. O'Toole,et al.  Stimulus-specific effects in face recognition over changes in viewpoint , 1998, Vision Research.

[64]  A. Damasio,et al.  Face agnosia and the neural substrates of memory. , 1990, Annual review of neuroscience.

[65]  K. Grill-Spector,et al.  fMR-adaptation: a tool for studying the functional properties of human cortical neurons. , 2001, Acta psychologica.

[66]  Leslie G. Ungerleider,et al.  Distributed representation of objects in the human ventral visual pathway. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[67]  G. McCarthy,et al.  Evidence for a Refractory Period in the Hemodynamic Response to Visual Stimuli as Measured by MRI , 2000, NeuroImage.

[68]  V. Bruce,et al.  The basis of the 3/4 view advantage in face recognition , 1987 .

[69]  H. Abdi,et al.  What Represents a Face? A Computational Approach for the Integration of Physiological and Psychological Data , 1997, Perception.

[70]  A. Young,et al.  Understanding covert recognition , 1991, Cognition.

[71]  Timothy J. Andrews,et al.  Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe , 2004, NeuroImage.

[72]  Thomas Vetter,et al.  Face Recognition Based on Fitting a 3D Morphable Model , 2003, IEEE Trans. Pattern Anal. Mach. Intell..

[73]  Alex Martin,et al.  Properties and mechanisms of perceptual priming , 1998, Current Opinion in Neurobiology.

[74]  Y. Goshen-Gottstein,et al.  Repetition priming for familiar and unfamiliar faces in a sex-judgment task: evidence for a common route for the processing of sex and identity. , 2000, Journal of experimental psychology. Learning, memory, and cognition.

[75]  Irving Biederman,et al.  One-shot viewpoint invariance in matching novel objects , 1999, Vision Research.

[76]  J. O'Doherty,et al.  Automatic and intentional brain responses during evaluation of trustworthiness of faces , 2002, Nature Neuroscience.

[77]  R. Henson,et al.  Neural response suppression, haemodynamic repetition effects, and behavioural priming , 2003, Neuropsychologia.

[78]  J B Deregowski,et al.  Perceived Similarity of Shapes is an Asymmetrical Relationship: A Study of Typical Contours , 1998, Perception.