Selectivity for the configural cues that identify the gender, ethnicity, and identity of faces in human cortex

We used psychophysical and functional MRI (fMRI) adaptation to examine how and where the visual configural cues underlying identification of facial ethnicity, gender, and identity are processed. We found that the cortical regions showing selectivity to these cues are distributed widely across the inferior occipital cortex, fusiform areas, and the cingulate gyrus. These regions were not colocalized with areas activated by traditional face area localizer scans. Traditional face area localizer scans isolate regions defined by stronger fMRI responses to a random series of face images than to a series of non-face images. Because these scans present a random assortment of face images, they presumably produce the strongest responses within regions containing neurons that are face-sensitive but not highly tuned for face type. These areas might be expected to show only weak selective adaptation effects. In contrast, the largest responses to our selective adaptation paradigm would be expected within areas containing more selectively tuned neurons that might be expected to show only a sparse collective response to a series of random faces. Many aspects of face processing (e.g., prosopagnosia, recognition, and configural vs. featural processing) are likely to rely heavily on regions containing high proportions of neurons that show selective tuning for faces.

[1]  J. Gibson,et al.  Adaptation, after-effect and contrast in the perception of tilted lines. I. Quantitative studies , 1937 .

[2]  C. McCollough Color Adaptation of Edge-Detectors in the Human Visual System , 1965, Science.

[3]  R. Over,et al.  Color Adaptation of Spatial Frequency Detectors in the Human Visual System , 1972, Science.

[4]  Spatial processing of luminance and color information. , 1978, Investigative ophthalmology & visual science.

[5]  C F Stromeyer,et al.  Form-Colour Aftereffects: Selectivity to Local Luminance Contrast , 1978, Perception.

[6]  J. Winn,et al.  Brain , 1878, The Lancet.

[7]  P. Lennie,et al.  Pattern-selective adaptation in visual cortical neurones , 1979, Nature.

[8]  D. W. Heeley,et al.  Cardinal directions of color space , 1982, Vision Research.

[9]  G. V. Van Hoesen,et al.  Prosopagnosia , 1982, Neurology.

[10]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  E. Rolls,et al.  Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey , 1985, Brain Research.

[12]  M. Lévesque Perception , 1986, The Yale Journal of Biology and Medicine.

[13]  K. McGraw,et al.  The relative salience of sex, race, age, and glasses in children's social perception. , 1989, The Journal of genetic psychology.

[14]  M. Hasselmo,et al.  The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey , 1989, Behavioural Brain Research.

[15]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[16]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

[17]  J Sergent,et al.  Functional and anatomical decomposition of face processing: evidence from prosopagnosia and PET study of normal subjects. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[18]  M I Sereno,et al.  Analysis of retinotopic maps in extrastriate cortex. , 1994, Cerebral cortex.

[19]  T. Allison,et al.  Face recognition in human extrastriate cortex. , 1994, Journal of neurophysiology.

[20]  Martha J. Farah,et al.  Face perception and within-category discrimination in prosopagnosia , 1995, Neuropsychologia.

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

[22]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[23]  Leslie G. Ungerleider,et al.  Face encoding and recognition in the human brain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Guillermo Sapiro,et al.  Creating connected representations of cortical gray matter for functional MRI visualization , 1997, IEEE Transactions on Medical Imaging.

[25]  S. Engel,et al.  Colour tuning in human visual cortex measured with functional magnetic resonance imaging , 1997, Nature.

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

[27]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[28]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[29]  Leslie G. Ungerleider,et al.  Sustained Activity in the Medial Wall during Working Memory Delays , 1998, The Journal of Neuroscience.

[30]  Frans A. J. Verstraten,et al.  The Motion Aftereffect:A Modern Perspective , 1998 .

[31]  Brian A Wandell,et al.  Color Signals in Human Motion-Selective Cortex , 1999, Neuron.

[32]  Otto H. MacLin,et al.  Figural aftereffects in the perception of faces , 1999, Psychonomic bulletin & review.

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

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

[35]  A. O'Toole,et al.  Prototype-referenced shape encoding revealed by high-level aftereffects , 2001, Nature Neuroscience.

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

[37]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[38]  C. Chubb,et al.  The size-tuning of the face-distortion after-effect , 2001, Vision Research.

[39]  Manjit,et al.  Neurology , 1912, NeuroImage.

[40]  Itzhak Fried,et al.  Inhibitory and excitatory responses of single neurons in the human medial temporal lobe during recognition of faces and objects. , 2002, Cerebral cortex.

[41]  Talma Hendler,et al.  Analysis of the Neuronal Selectivity Underlying Low fMRI Signals , 2002, Current Biology.

[42]  B. Richmond,et al.  Anterior Cingulate: Single Neuronal Signals Related to Degree of Reward Expectancy , 2002, Science.

[43]  Frank S. Werblin,et al.  Mechanisms and circuitry underlying directional selectivity in the retina , 2002, Nature.

[44]  Morten L Kringelbach,et al.  Neural correlates of rapid reversal learning in a simple model of human social interaction , 2003, NeuroImage.

[45]  M. Webster,et al.  Adaptation to natural facial categories , 2002, Nature.

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

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

[48]  R. Dolan,et al.  fMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. , 2004, Journal of neurophysiology.

[49]  S. Yamane,et al.  What facial features activate face neurons in the inferotemporal cortex of the monkey? , 2004, Experimental Brain Research.

[50]  E. Rolls,et al.  Size and contrast have only small effects on the responses to faces of neurons in the cortex of the superior temporal sulcus of the monkey , 2004, Experimental Brain Research.

[51]  A. Treves,et al.  Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain , 2005, Nature Neuroscience.

[52]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[53]  G. Rees,et al.  Predicting the orientation of invisible stimuli from activity in human primary visual cortex , 2005, Nature Neuroscience.

[54]  H. Wilson,et al.  fMRI evidence for the neural representation of faces , 2005, Nature Neuroscience.

[55]  D. Kersten,et al.  Orientation-tuned FMRI adaptation in human visual cortex. , 2005, Journal of neurophysiology.

[56]  R. Schultz,et al.  Functional Neuroimaging Studies of Autism Spectrum Disorders , 2005 .

[57]  Karl J. Friston,et al.  A critique of functional localisers , 2006, NeuroImage.

[58]  K. Grill-Spector,et al.  High-resolution imaging reveals highly selective nonface clusters in the fusiform face area , 2006, Nature Neuroscience.