The Fusiform Face Area Is Engaged in Holistic, Not Parts-Based, Representation of Faces

Numerous studies with functional magnetic resonance imaging have shown that the fusiform face area (FFA) in the human brain plays a key role in face perception. Recent studies have found that both the featural information of faces (e.g., eyes, nose, and mouth) and the configural information of faces (i.e., spatial relation among features) are encoded in the FFA. However, little is known about whether the featural information is encoded independent of or combined with the configural information in the FFA. Here we used multi-voxel pattern analysis to examine holistic representation of faces in the FFA by correlating spatial patterns of activation with behavioral performance in discriminating face parts with face configurations either present or absent. Behaviorally, the absence of face configurations (versus presence) impaired discrimination of face parts, suggesting a holistic representation in the brain. Neurally, spatial patterns of activation in the FFA were more similar among correct than incorrect trials only when face parts were presented in a veridical face configuration. In contrast, spatial patterns of activation in the occipital face area, as well as the object-selective lateral occipital complex, were more similar among correct than incorrect trials regardless of the presence of veridical face configurations. This finding suggests that in the FFA faces are represented not on the basis of individual parts but in terms of the whole that emerges from the parts.

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

[2]  Daniel D. Dilks,et al.  Resting-State Neural Activity across Face-Selective Cortical Regions Is Behaviorally Relevant , 2011, The Journal of Neuroscience.

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

[4]  Z Kourtzi,et al.  Representation of Perceived Object Shape by the Human Lateral Occipital Complex , 2001, Science.

[5]  N D Haig,et al.  The Effect of Feature Displacement on the Perception of Well-Known Faces , 1988, Perception.

[6]  Keiji Tanaka,et al.  Inferotemporal cortex and object vision. , 1996, Annual review of neuroscience.

[7]  R. Goebel,et al.  Holistic perception of individual faces in the right middle fusiform gyrus as evidenced by the composite face illusion. , 2010, Journal of vision.

[8]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[9]  G. Rhodes Looking at Faces: First-Order and Second-Order Features as Determinants of Facial Appearance , 2013, Perception.

[10]  K. Nakayama,et al.  Categorical perception of face identity in noise isolates configural processing. , 2001, Journal of experimental psychology. Human perception and performance.

[11]  Bruno Rossion,et al.  Hemispheric Asymmetries for Whole-Based and Part-Based Face Processing in the Human Fusiform Gyrus , 2000, Journal of Cognitive Neuroscience.

[12]  Bruno Rossion,et al.  Faces are represented holistically in the human occipito-temporal cortex , 2006, NeuroImage.

[13]  A. Young,et al.  Configurational Information in Face Perception , 1987, Perception.

[14]  V. Bruce,et al.  The Quarterly Journal of Experimental Psychology Section A: Human Experimental Psychology When Inverted Faces Are Recognized: the Role of Configural Information in Face Recognition , 2022 .

[15]  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.

[16]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[17]  Jennifer L. Campos,et al.  Bayesian integration of visual and vestibular signals for heading. , 2009, Journal of vision.

[18]  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.

[19]  David D. Cox,et al.  Functional magnetic resonance imaging (fMRI) “brain reading”: detecting and classifying distributed patterns of fMRI activity in human visual cortex , 2003, NeuroImage.

[20]  Jia Liu,et al.  The Part Task of the Part-Spacing Paradigm Is Not a Pure Measurement of Part-Based Information of Faces , 2009, PloS one.

[21]  D. Maurer,et al.  Impairment in Holistic Face Processing Following Early Visual Deprivation , 2004, Psychological science.

[22]  N. Kanwisher,et al.  The Neural Basis of the Behavioral Face-Inversion Effect , 2005, Current Biology.

[23]  A. Freire,et al.  The Face-Inversion Effect as a Deficit in the Encoding of Configural Information: Direct Evidence , 2000, Perception.

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

[25]  H B Barlow,et al.  Single units and sensation: a neuron doctrine for perceptual psychology? , 1972, Perception.

[26]  M. Farah,et al.  Parts and Wholes in Face Recognition , 1993, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[27]  M. Riesenhuber,et al.  Face processing in humans is compatible with a simple shape–based model of vision , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[29]  D. Maurer,et al.  Neural correlates of processing facial identity based on features versus their spacing , 2007, Neuropsychologia.

[30]  Roberto Cabeza,et al.  Features are Also Important: Contributions of Featural and Configural Processing to Face Recognition , 2000, Psychological science.

[31]  N. Kanwisher,et al.  Only some spatial patterns of fMRI response are read out in task performance , 2007, Nature Neuroscience.

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

[33]  Stephen D. Mayhew,et al.  Article Learning Shapes the Representation of Behavioral Choice in the Human Brain , 2022 .

[34]  Jia Liu,et al.  Perception of Face Parts and Face Configurations: An fMRI Study , 2010, Journal of Cognitive Neuroscience.

[35]  J. Keenan,et al.  Discrimination of spatial relations and features in faces: Effects of inversion and viewing duration. , 2001, British journal of psychology.

[36]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[37]  J. Sergent An investigation into component and configural processes underlying face perception. , 1984, British journal of psychology.

[38]  Nancy Kanwisher,et al.  Face Perception Engages a Domain-Specific System for Processing both Configural and Part-Based Information about Faces , 2004 .

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

[40]  Nancy Kanwisher,et al.  The representations of spacing and part-based information are associated for upright faces but dissociated for objects: Evidence from individual differences , 2008, Psychonomic bulletin & review.

[41]  G. Rhodes,et al.  The fusiform face area and occipital face area show sensitivity to spatial relations in faces , 2009, The European journal of neuroscience.

[42]  M. Farah,et al.  What is "special" about face perception? , 1998, Psychological review.

[43]  Yasushi Miyashita,et al.  Dynamically Modulated Spike Correlation in Monkey Inferior Temporal Cortex Depending on the Feature Configuration within a Whole Object , 2005, The Journal of Neuroscience.

[44]  Raymond J. Dolan,et al.  Role of Features and Second-order Spatial Relations in Face Discrimination, Face Recognition, and Individual Face Skills: Behavioral and Functional Magnetic Resonance Imaging Data , 2007, Journal of Cognitive Neuroscience.

[45]  J. Mumford,et al.  Greater Neural Pattern Similarity Across Repetitions Is Associated with Better Memory , 2010, Science.

[46]  R. Raizada,et al.  Quantifying the adequacy of neural representations for a cross-language phonetic discrimination task: prediction of individual differences. , 2010, Cerebral cortex.

[47]  Gillian Rhodes,et al.  What's lost in inverted faces? , 1993, Cognition.

[48]  N. Kanwisher,et al.  Face perception: domain specific, not process specific. , 2004, Neuron.

[49]  T. Allison,et al.  Electrophysiological studies of human face perception. II: Response properties of face-specific potentials generated in occipitotemporal cortex. , 1999, Cerebral cortex.

[50]  H. Barlow,et al.  Single Units and Sensation: A Neuron Doctrine for Perceptual Psychology? , 1972, Perception.

[51]  Kenneth F. Valyear,et al.  The fusiform face area is not sufficient for face recognition: Evidence from a patient with dense prosopagnosia and no occipital face area , 2006, Neuropsychologia.

[52]  T. Hendler,et al.  A hierarchical axis of object processing stages in the human visual cortex. , 2001, Cerebral cortex.

[53]  Paul E. Downing,et al.  Using multi-voxel pattern analysis of fMRI data to interpret overlapping functional activations , 2007, Trends in Cognitive Sciences.

[54]  J. Keenan,et al.  Lesions of the fusiform face area impair perception of facial configuration in prosopagnosia , 2002, Neurology.

[55]  Jonathan D. Cohen,et al.  Reproducibility Distinguishes Conscious from Nonconscious Neural Representations , 2010, Science.

[56]  G. Rees,et al.  Neuroimaging: Decoding mental states from brain activity in humans , 2006, Nature Reviews Neuroscience.

[57]  Alison Harris,et al.  The Representation of Parts and Wholes in Face-selective Cortex , 2008, Journal of Cognitive Neuroscience.

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

[59]  K. Grill-Spector,et al.  The dynamics of object-selective activation correlate with recognition performance in humans , 2000, Nature Neuroscience.

[60]  J. Tanaka,et al.  Features and their configuration in face recognition , 1997, Memory & cognition.

[61]  Alison Harris,et al.  Neural tuning for face wholes and parts in human fusiform gyrus revealed by FMRI adaptation. , 2010, Journal of neurophysiology.