Loci of the release from fMRI adaptation for changes in facial expression, identity, and viewpoint.

Face recognition involves collaboration of a distributed network of neural correlates. However, how different attributes of faces are represented has remained unclear. We used functional magnetic resonance imaging-adaptation (fMRIa) to investigate the representation of viewpoint, expression, and identity of faces in the fusiform face area (FFA) and the occipital face area (OFA). In an event-related experiment, subjects viewed sequences of two faces and judged whether they depicted the same person. The images could vary in viewpoint, expression and/or identity. Critically, the physical similarity between view-changed and between expression-changed faces of the same person were matched by the Gabor-jet metric, a measure that predicts almost perfectly the effects of image similarity on face discrimination performance. In FFA, changes of identity produced the largest release from adaptation followed by changes of expression; but the release caused by changes of viewpoint was smaller and not reliable. OFA was sensitive only to changes in identity, even when image changes produced by identity variations were matched to those of expression and orientation. These results suggest that FFA is involved in the perception of both identity and expression of faces, a result contrary to the hypothesis of independent processing of changeable and invariant attributes of faces in the face-processing network.

[1]  James R. Pomerantz,et al.  Stimules configuration in selective attention tasks , 1973 .

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

[3]  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.

[4]  Joachim M. Buhmann,et al.  Distortion Invariant Object Recognition in the Dynamic Link Architecture , 1993, IEEE Trans. Computers.

[5]  R. Adolphs,et al.  Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala , 1994, Nature.

[6]  T. Allison,et al.  Differential Sensitivity of Human Visual Cortex to Faces, Letterstrings, and Textures: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

[7]  I Biederman,et al.  To what extent can matching algorithms based on direct outputs of spatial filters account for human object recognition? , 1996, Spatial vision.

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

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

[10]  S. Schweinberger,et al.  Asymmetric relationships among perceptions of facial identity, emotion, and facial speech. , 1998, Journal of experimental psychology. Human perception and performance.

[11]  Kenji Kawano,et al.  Global and fine information coded by single neurons in the temporal visual cortex , 1999, Nature.

[12]  A M Burton,et al.  Asymmetric dependencies in perceiving identity and emotion: Experiments with morphed faces , 1999, Perception & psychophysics.

[13]  S. Edelman,et al.  Differential Processing of Objects under Various Viewing Conditions in the Human Lateral Occipital Complex , 1999, Neuron.

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

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

[16]  N. Kanwisher,et al.  Cortical Regions Involved in Perceiving Object Shape , 2000, The Journal of Neuroscience.

[17]  G. Pagnoni,et al.  Explicit and Incidental Facial Expression Processing: An fMRI Study , 2001, NeuroImage.

[18]  Nicolas Franck,et al.  Selective attention to facial emotion and identity in schizophrenia , 2002, Neuropsychologia.

[19]  N. Kanwisher,et al.  Stages of processing in face perception: an MEG study , 2002, Nature Neuroscience.

[20]  A. O'Toole,et al.  Recognizing moving faces: a psychological and neural synthesis , 2002, Trends in Cognitive Sciences.

[21]  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.

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

[23]  Hisao Nishijo,et al.  Neuronal correlates of face identification in the monkey anterior temporal cortical areas. , 2004, Journal of neurophysiology.

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

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

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

[27]  A. Young,et al.  Understanding the recognition of facial identity and facial expression , 2005, Nature Reviews Neuroscience.

[28]  Sheng He,et al.  Viewer-Centered Object Representation in the Human Visual System Revealed by Viewpoint Aftereffects , 2005, Neuron.

[29]  Kenneth F. Valyear,et al.  The involvement of the “fusiform face area” in processing facial expression , 2005, Neuropsychologia.

[30]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

[31]  R. Goebel,et al.  Cerebral Cortex doi:10.1093/cercor/bhj005 Impaired Face Discrimination in Acquired Prosopagnosia Is Associated with Abnormal Response to Individual Faces in the Right Middle Fusiform Gyrus , 2005 .

[32]  G. Boynton,et al.  Adaptation: from single cells to BOLD signals , 2006, Trends in Neurosciences.

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

[34]  J. Haxby,et al.  Neural systems for recognition of familiar faces , 2007, Neuropsychologia.

[35]  F. Fang,et al.  Transfer of the face viewpoint aftereffect from adaptation to different and inverted faces. , 2007, Journal of vision.

[36]  R. Malach,et al.  Sub-exemplar shape tuning in human face-related areas. , 2007, Cerebral cortex.

[37]  G. Yovel,et al.  TMS Evidence for the Involvement of the Right Occipital Face Area in Early Face Processing , 2007, Current Biology.

[38]  A. Anderson,et al.  Examinations of identity invariance in facial expression adaptation , 2008, Cognitive, affective & behavioral neuroscience.

[39]  Christopher J. Fox,et al.  It doesn't matter how you feel. The facial identity aftereffect is invariant to changes in facial expression. , 2008, Journal of vision.

[40]  Timothy J. Andrews,et al.  Differential sensitivity for viewpoint between familiar and unfamiliar faces in human visual cortex , 2008, NeuroImage.

[41]  R Goebel,et al.  Inverse mapping the neuronal substrates of face categorizations. , 2009, Cerebral cortex.

[42]  Doris Y. Tsao,et al.  A face feature space in the macaque temporal lobe , 2009, Nature Neuroscience.

[43]  J. Devlin,et al.  Triple Dissociation of Faces, Bodies, and Objects in Extrastriate Cortex , 2009, Current Biology.

[44]  M. Herrmann,et al.  Emotions in motion: Dynamic compared to static facial expressions of disgust and happiness reveal more widespread emotion-specific activations , 2009, Brain Research.

[45]  Jiye G. Kim,et al.  Adaptation in the fusiform face area (FFA): Image or person? , 2009, Vision Research.

[46]  C. Mondloch,et al.  Children's representations of facial expression and identity: identity-contingent expression aftereffects. , 2009, Journal of experimental child psychology.

[47]  Christopher J. Fox,et al.  Defining the face processing network: Optimization of the functional localizer in fMRI , 2009, Human brain mapping.

[48]  D. Burke,et al.  Evidence that identity-dependent and identity-independent neural populations are recruited in the perception of five basic emotional facial expressions , 2009, Vision Research.

[49]  Giuseppe Iaria,et al.  The correlates of subjective perception of identity and expression in the face network: An fMRI adaptation study , 2009, NeuroImage.

[50]  J. Schultz,et al.  Natural facial motion enhances cortical responses to faces , 2009, Experimental Brain Research.

[51]  Kathrin Cohen Kadosh,et al.  Task-dependent Activation of Face-sensitive Cortex: An fMRI Adaptation Study , 2010, Journal of Cognitive Neuroscience.

[52]  Brittany S. Cassidy,et al.  Lower-Level Stimulus Features Strongly Influence Responses in the Fusiform Face Area , 2010, Cerebral cortex.