Abstract
How the brain represents different aspects of faces remains controversial. Here we presented subjects with stimuli drawn from morph continua between pairs of famous faces. In the paired presentations, a second face could be identical to the first, could share perceived identity but differ physically (30% along the morph continuum), or could differ physically by the same distance along the continuum (30%) but in the other direction. We show that, behaviorally, subjects are more likely to classify face pairs in the third paired presentation as different and that this effect is more pronounced for subjects who are more familiar with the faces. In functional magnetic resonance imaging (fMRI), inferior occipital gyrus (IOG) shows sensitivity to physical rather than to identity changes, whereas right fusiform gyrus (FFG) shows sensitivity to identity rather than to physical changes. Bilateral anterior temporal regions show sensitivity to identity change that varies with the subjects' pre-experimental familiarity with the faces. These findings provide neurobiological support for a hierarchical model of face perception.
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References
Posamentier, M.T. & Abdi, H. Processing faces and facial expressions. Neuropsychol. Rev. 13, 113–143 (2003).
Farah, M.J., Wilson, K.D., Drain, M. & Tanaka, J.N. What is 'special' about face perception? Psychol. Rev. 105, 482–498 (1998).
Kanwisher, N., McDermott, J. & Chun, M.M. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302–4311 (1997).
Malach, R., Levy, I. & Hasson, U. The topographic of high-order human object areas. Trends Cogn. Sci. 6, 176–184 (2002).
Haxby, J.V., Hoffman, E.A. & Gobbini, M.I. The distributed human neural system for face perception. Trends Cogn. Sci. 4, 223–233 (2000).
Leonard, C.M., Rolls, E.T., Wilson, F.A. & Baylis, G.C. Neurons in the amygdala of the monkey with responses selective for faces. Behav. Brain Res. 15, 159–176 (1985).
Ishai, A., Haxby, J.V. & Ungerleider, L.G. Visual imagery of famous faces: effects of memory and attention revealed by fMRI. NeuroImage 17, 1729–1741 (2002).
Rajah, M.N., McIntosh, A.R. & Grady, C.L. Frontotemporal interactions in face encoding and recognition. Brain Res. Cogn Brain Res. 8, 259–269 (1999).
Seeck, M. et al. Intracranial neurophysiological correlates related to the processing of faces. Epilepsy Behav. 2, 545–557 (2001).
Perrett, D., Rolls, E.T. & Caan, W. Visual neurons responsive to faces in the monkey temporal cortex. Exp. Brain Res. 47, 329–342 (1982).
McCarthy, G., Puce, A., Belger, A. & Allison, T. Electrophysiological studies of human face perception. II. Response properties of face-specific potentials generated in occipitotemporal cortex. Cereb. Cortex 9, 431–444 (1999).
De Renzi, E. Prosopagnosia in two patients with CT scan evidence of damage confined to the right hemisphere. Neuropsychologia 24, 385–389 (1986).
Tranel, D., Damasio, H. & Damasio, A.R. A neural basis for the retrieval of conceptual knowledge. Neuropsychologia 35, 1319–1327 (1997).
Dolan, R. et al. How the brain learns to see objects and faces in an impoverished context. Nature 389, 596–569 (1997).
Henson, R.N. et al. Electrophysiological and heamodynamic correlates of face perception, recognition and priming. Cereb. Cortex 13, 793–805 (2003).
Beale, J.M. & Keil, F.C. Categorical effects in perception of faces. Cognition 57, 217–239 (1995).
Nosofsky, R.M. Attention, similarity, and the identification-categorization relationship. J. Exp. Psychol. Gen. 115, 39–61 (1986).
Valentine, T. A unified account of the effects of distinctiveness, inversion and race in face recognition. Q. J. Exp. Psychol. A 43, 161–204 (1991).
Harnad, S. Psychophysical and cognitive aspects of categorical perception. in Categorical Perception: The Ground of Cognition (ed. Harnad, S.) 1–25 (Cambridge Univ. Press, New York, 1987).
Campanella, S. et al. Right N170 modulation in a face discrimination task: an account for categorical perception of familiar faces. Psychophysiology 37, 796–806 (2000).
Kourtzi, Z. & Kanwisher, N. Representation of perceived object shape by the human lateral occipital complex. Science 293, 1506–1509 (2000).
Grill-Spector, K., Kushnir, T., Edelman, S., Itzchak, Y. & Malach, R. Cue-invariant activation in object-related areas of the human occipital lobe. Neuron 21, 191–202 (1998).
Henson, R.N., Shallice, T. & Dolan, R. Neuroimaging evidence for dissociable forms of repetition priming. Science 287, 1269–1272 (2000).
Henson, R.N. Neuroimaging studies of priming. Prog. Neurobiol. 70, 53–81 (2004)
Grill-Spector, K., Kourtzi, Z. & Kanwisher, N. The fusiform face area subserves face perception not generic within-category identification. Nat. Neurosci. 7, 555–562 (2004).
de Gelder, B. & Rouw, R. Beyond localization: a dynamical dual route account of face recognition. Acta. Psychol. 107, 183–207 (2001).
Bruce, V. & Young, A. Understanding face recognition. Br. J. Psychol. 77, 305–327 (1986).
Gauthier, I. et al. The fusiform 'face area' is part of a network that processes faces at the individual level. J. Cogn. Neurosci. 12, 495–504 (2000).
George, N. et al. Contrast polarity and face recognition in the human fusiform gyrus. Nat. Neurosci. 2, 574–580 (1999).
Hasselmo, M.E., Rolls, E.T. & Baylis, G.C. The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey. Behav. Brain Res. 32, 203–218 (1989).
Mundel, T. et al. Transient inability to distinguish between faces: electrophysiologic studies. J. Clin. Exp. Neuropsychol. 20, 102–110 (2003).
Winston, J.S., Henson, R.N., Fine-Goulden, M.R. & Dolan, R.J. fMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. J. Neurophysiol. 92, 1830–1839 (2004).
Sirovich, L. & Kirby, M. Low-dimensional procedure for the characterization of human faces. J. Opt. Soc. Am. 4, 519–524 (1987).
Tanaka, J., Giles, M., Kremen, S. & Simon, V. Mapping attractor fields in face space: the atypicality bias in face recognition. Cognition 68, 199–220 (1998).
Sigala, N. & Logothetis, N.K. Visual categorization shapes feature selectivity in the primate temporal cortex. Nature 415, 318–320 (2002).
Rolls, E.T., Treves, A., Tovee, M.J. & Panzeri, S. Information in the neuronal representation of individual stimuli in the primate temporal visual cortex. J. Comput. Neurosci. 4, 309–333 (1997).
Gorno-Tempini, M.L. et al. The neural systems sustaining face and proper-name processing. Brain 121, 2103–2118 (1998).
Leveroni, C.L. et al. Neural systems underlying the recognition of familiar and newly learned faces. J. Neurosci. 20, 878–886 (2000).
Sugiura, M. et al. Activation reduction in anterior temporal cortices during repeated recognition of faces of personal acquaintances. NeuroImage 13, 877–890 (2001).
Glosser, G., Salvucci, A.E. & Chiaravalloti, N.D. Naming and recognizing famous faces in temporal lobe epilepsy. Neurology 61, 81–86 (2003).
Barton, J.J.S. & Cherkasova, M. face imagery and its relation to perception and covert recognition in prosopagnosia. Neurology 61, 220–225 (2003).
Winston, J.S., O'Doherty, J. & Dolan, R.J. Common and distinct neural response during direct and incidental processing of multiple facial emotions. NeuroImage 20, 84–97 (2003).
Josephs, O., Deichmann, R. & Turner, R. Trajectory measurment and generalised reconstruction in rectilinear EPI. NeuroImage 11, S543 (2000).
Deichmann, R., Gottfried, J.A. & Turner, R. Optimized EPI for fMRI studies of the orbitofrontal cortex. NeuroImage 19, 430–441 (2003).
Friston, K.J., Williams, S.R., Howard, R., Frackowiak, R.S.J. & Turner, R. Movement-related effects in fMRI time-series. Magn. Reson. Med. 35, 346–355 (1996).
Andersson, J.L., Hutton, C., Ashburner, J., Turner, R. & Friston, K.J. Modeling geometric deformations in EPI time series. NeuroImage 13, 903–919 (2001).
Ashburner, J. & Friston, K.J. Nonlinear spatial normalization using basis function. Hum. Brain. Mapp. 7, 254–266 (1999).
Penny, W. & Friston, K.J. Hierarchical models. in Human Brain Function II (eds. Frackowiak, R.S., Friston, K.J., Dolan, R. & Ashburner, J.) 851–863 (Elsevier Academic, 2003).
Friston, K.J. et al. Event-related fMRI: characterizing differential responses. NeuroImage 7, 30–40 (1998).
Friston, K.J., Holmes, A.P., Price, C.J., Buchel, C. & Worsley, K.J. Multisubject fMRI studies and conjunction analyses. NeuroImage 10, 385–396.
Acknowledgements
We thank J. Ashburner and A. Viaccoz for help with the stimuli. This work was carried out under a Programme Grant to R.J.D. from the Wellcome Trust. J.D., R.N.H and P.R. were also supported by the Wellcome Trust. Additional support came from the Human Frontier Science Program to A.T. and R.J.D.
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Supplementary Fig. 1
Identity classification experiment; further examples (JPG 54 kb)
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Rotshtein, P., Henson, R., Treves, A. et al. Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain. Nat Neurosci 8, 107–113 (2005). https://doi.org/10.1038/nn1370
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DOI: https://doi.org/10.1038/nn1370
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