Categorical, Yet Graded – Single-Image Activation Profiles of Human Category-Selective Cortical Regions

Human inferior temporal cortex contains category-selective visual regions, including the fusiform face area (FFA) and the parahippocampal place area (PPA). These regions are defined by their greater category-average activation to the preferred category (faces and places, respectively) relative to nonpreferred categories. The approach of investigating category-average activation has left unclear to what extent category selectivity holds for individual object images. Here we investigate single-image activation profiles to address (1) whether each image from the preferred category elicits greater activation than any image outside the preferred category (categorical ranking), (2) whether there are activation differences within and outside the preferred category (gradedness), and (3) whether the activation profile falls off continuously across the category boundary or exhibits a discontinuity at the boundary (category step). We used functional magnetic resonance imaging to measure the activation elicited in the FFA and PPA by each of 96 object images from a wide range of categories, including faces and places, but also humans and animals, and natural and manmade objects. Results suggest that responses in FFA and PPA exhibit almost perfect categorical ranking, are graded within and outside the preferred category, and exhibit a category step. The gradedness within the preferred category was more pronounced in FFA; the category step was more pronounced in PPA. These findings support the idea that these regions have category-specific functions, but are also consistent with a distributed object representation emphasizing categories while still distinguishing individual images.

[1]  M. Young,et al.  Sparse population coding of faces in the inferotemporal cortex. , 1992, Science.

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

[3]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[4]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

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

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

[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]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[9]  N. Kanwisher,et al.  Covert visual attention modulates face-specific activity in the human fusiform gyrus: fMRI study. , 1998, Journal of neurophysiology.

[10]  S. Edelman,et al.  Toward direct visualization of the internal shape representation space by fMRI , 1998, Psychobiology.

[11]  R. Dolan,et al.  Common effects of emotional valence, arousal and attention on neural activation during visual processing of pictures , 1999, Neuropsychologia.

[12]  N. Kanwisher,et al.  Brain Imaging , 2020, Encyclopedia of Behavioral Medicine.

[13]  R. Vogels Categorization of complex visual images by rhesus monkeys. Part 2: single‐cell study , 1999, The European journal of neuroscience.

[14]  Nancy Kanwisher,et al.  fMRI evidence for objects as the units of attentional selection , 1999, Nature.

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

[16]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[17]  N. Sigala,et al.  Visual categorization shapes feature selectivity in the primate temporal cortex , 2002, Nature.

[18]  Michel Vidal-Naquet,et al.  Visual features of intermediate complexity and their use in classification , 2002, Nature Neuroscience.

[19]  Doris Y. Tsao,et al.  Faces and objects in macaque cerebral cortex , 2003, Nature Neuroscience.

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

[21]  D. Perrett,et al.  Rapid serial visual presentation for the determination of neural selectivity in area STSa. , 2004, Progress in brain research.

[22]  M. Carrasco,et al.  Transient Attention Enhances Perceptual Performance and fMRI Response in Human Visual Cortex , 2005, Neuron.

[23]  Doris Y. Tsao,et al.  A Cortical Region Consisting Entirely of Face-Selective Cells , 2006, Science.

[24]  N. Kanwisher,et al.  Domain specificity in visual cortex. , 2006, Cerebral cortex.

[25]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[26]  G. Rhodes,et al.  Are you always on my mind? A review of how face perception and attention interact , 2007, Neuropsychologia.

[27]  Sharon L. Thompson-Schill,et al.  Item analysis in functional magnetic resonance imaging , 2007, NeuroImage.

[28]  R. Goebel,et al.  Individual faces elicit distinct response patterns in human anterior temporal cortex , 2007, Proceedings of the National Academy of Sciences.

[29]  David D. Cox,et al.  Untangling invariant object recognition , 2007, Trends in Cognitive Sciences.

[30]  Keiji Tanaka,et al.  Object category structure in response patterns of neuronal population in monkey inferior temporal cortex. , 2007, Journal of neurophysiology.

[31]  Geoffrey Karl Aguirre,et al.  Continuous carry-over designs for fMRI , 2007, NeuroImage.

[32]  Raymond J. Dolan,et al.  fMRI Activity Patterns in Human LOC Carry Information about Object Exemplars within Category , 2008, Journal of Cognitive Neuroscience.

[33]  Shimon Ullman,et al.  Class Information Predicts Activation by Object Fragments in Human Object Areas , 2008, Journal of Cognitive Neuroscience.

[34]  N. Kanwisher,et al.  Multivariate Patterns in Object-Selective Cortex Dissociate Perceptual and Physical Shape Similarity , 2008, PLoS biology.

[35]  Keiji Tanaka,et al.  Matching Categorical Object Representations in Inferior Temporal Cortex of Man and Monkey , 2008, Neuron.

[36]  Leslie G. Ungerleider,et al.  Object representations in the temporal cortex of monkeys and humans as revealed by functional magnetic resonance imaging. , 2009, Journal of neurophysiology.

[37]  Dwight J. Kravitz,et al.  Real-World Scene Representations in High-Level Visual Cortex: It's the Spaces More Than the Places , 2011, The Journal of Neuroscience.

[38]  Natalia Y. Bilenko,et al.  The “Parahippocampal Place Area” Responds Preferentially to High Spatial Frequencies in Humans and Monkeys , 2011, PLoS biology.