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  • Review Article
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The functional architecture of the ventral temporal cortex and its role in categorization

Nature Reviews Neuroscience volume 15, pages 536–548 (2014)Cite this article

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Key Points

  • Understanding information processing in the visual system requires an understanding of the interplay among the system's computational goals and representations, and their physical implementation in the brain.

  • Recent results indicate a consistent topology of functional representations relative to each other and anatomical landmarks in high-level visual cortex.

  • The consistent topology of functional representations reveals that axes of representational spaces are physically implemented as axes in cortical space.

  • Anatomical constraints might determine the topology of functional representations in the brain, which would explain the correspondence between representational and anatomical axes in the ventral temporal cortex (VTC).

  • Superimposition and topology generate predictable spatial convergences and divergences among functional representations, which in turn enable information integration and parallel processing, respectively.

  • Superimposition and topological organization in the VTC generates a series of nested functional representations, the arrangements of which generate a spatial hierarchy of category information.

  • The spatial scale of functional representations may be tied to the level of category abstractness in which more abstract information is represented in larger spatial scales across the VTC.

Abstract

Visual categorization is thought to occur in the human ventral temporal cortex (VTC), but how this categorization is achieved is still largely unknown. In this Review, we consider the computations and representations that are necessary for categorization and examine how the microanatomical and macroanatomical layout of the VTC might optimize them to achieve rapid and flexible visual categorization. We propose that efficient categorization is achieved by organizing representations in a nested spatial hierarchy in the VTC. This spatial hierarchy serves as a neural infrastructure for the representational hierarchy of visual information in the VTC and thereby enables flexible access to category information at several levels of abstraction.

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Figure 1: Computational goals of a visual categorization system.
Figure 2: Properties of the ventral temporal cortex representations.
Figure 3: Three implementational features of the ventral temporal cortex: clustering, topological organization and superimposition.
Figure 4: Linking anatomical features to large-scale functional maps in the ventral temporal cortex.
Figure 5: The spatial structure of nested functional representations in the ventral temporal cortex supports the hierarchical information structure.

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References

  1. Thorpe, S., Fize, D. & Marlot, C. Speed of processing in the human visual system. Nature 381, 520–522 (1996).

    Article  CAS  PubMed  Google Scholar 

  2. Grill-Spector, K. & Kanwisher, N. Visual recognition: as soon as you know it is there, you know what it is. Psychol. Sci. 16, 152–160 (2005).

    Article  PubMed  Google Scholar 

  3. Ungerleider, L. G. & Mishkin, M. in Analysis of Visual Behaviour (eds Ingle, D. J., Goodale, M. A. & Mansfield, R. J. W.) 549–586 (MIT Press, 1982).

    Google Scholar 

  4. Tong, F., Nakayama, K., Vaughan, J. T. & Kanwisher, N. Binocular rivalry and visual awareness in human extrastriate cortex. Neuron 21, 753–759 (1998).

    Article  CAS  PubMed  Google Scholar 

  5. Grill-Spector, K., Kushnir, T., Hendler, T. & Malach, R. The dynamics of object-selective activation correlate with recognition performance in humans. Nature Neurosci. 3, 837–843 (2000).

    Article  CAS  PubMed  Google Scholar 

  6. Moutoussis, K. & Zeki, S. The relationship between cortical activation and perception investigated with invisible stimuli. Proc. Natl Acad. Sci. USA 99, 9527–9532 (2002).

    Article  CAS  PubMed  Google Scholar 

  7. Farah, M. J. Visual Agnoisa: Disorders of Object Recognition and What They Tell Us About Normal Vision (MIT Press, 1990).

    Google Scholar 

  8. Konen, C. S., Behrmann, M., Nishimura, M. & Kastner, S. The functional neuroanatomy of object agnosia: a case study. Neuron 71, 49–60 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Schiltz, C. et al. Impaired face discrimination in acquired prosopagnosia is associated with abnormal response to individual faces in the right middle fusiform gyrus. Cereb. Cortex 16, 574–586 (2006).

    Article  PubMed  Google Scholar 

  10. Rossion, B. et al. A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 126, 2381–2395 (2003).

    Article  PubMed  Google Scholar 

  11. Brewer, A. A., Liu, J., Wade, A. R. & Wandell, B. A. Visual field maps and stimulus selectivity in human ventral occipital cortex. Nature Neurosci. 8, 1102–1109 (2005).

    Article  CAS  PubMed  Google Scholar 

  12. Beauchamp, M. S., Haxby, J. V., Jennings, J. E. & DeYoe, E. A. An fMRI version of the Farnsworth–Munsell 100-Hue test reveals multiple colour-selective areas in human ventral occipitotemporal cortex. Cereb. Cortex 9, 257–263 (1999).

    Article  CAS  PubMed  Google Scholar 

  13. Murphey, D. K., Yoshor, D. & Beauchamp, M. S. Perception matches selectivity in the human anterior colour center. Curr. Biol. 18, 216–220 (2008).

    Article  CAS  PubMed  Google Scholar 

  14. Bouvier, S. E. & Engel, S. A. Behavioural deficits and cortical damage loci in cerebral achromatopsia. Cereb. Cortex 16, 183–191 (2006).

    Article  PubMed  Google Scholar 

  15. Hasson, U., Levy, I., Behrmann, M., Hendler, T. & Malach, R. Eccentricity bias as an organizing principle for human high-order object areas. Neuron 34, 479–490 (2002).

    Article  CAS  PubMed  Google Scholar 

  16. Behrmann, M. & Plaut, D. C. Distributed circuits, not circumscribed centers, mediate visual recognition. Trends Cogn. Sci. 17, 210–219 (2013).

    Article  PubMed  Google Scholar 

  17. Weiner, K. S. et al. The mid-fusiform sulcus: a landmark identifying both cytoarchitectonic and functional divisions of human ventral temporal cortex. Neuroimage 84, 453–465 (2014). This study provides crucial evidence for how representational axes are mapped to cortical axes in the VTC. Results show that the MFS predicts both transitions in the functional maps and boundaries between cytoarchitectonic areas. These findings underscore the importance of the MFS, which is not even mentioned in neuroanatomical atlases.

    Article  PubMed  Google Scholar 

  18. Arcaro, M. J., McMains, S. A., Singer, B. D. & Kastner, S. Retinotopic organization of human ventral visual cortex. J. Neurosci. 29, 10638–10652 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. 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).

    Article  CAS  PubMed  Google Scholar 

  20. Epstein, R. & Kanwisher, N. A cortical representation of the local visual environment. Nature 392, 598–601 (1998).

    Article  CAS  PubMed  Google Scholar 

  21. McGugin, R. W., Gatenby, J. C., Gore, J. C. & Gauthier, I. High-resolution imaging of expertise reveals reliable object selectivity in the fusiform face area related to perceptual performance. Proc. Natl Acad. Sci. USA 109, 17063–17068 (2012).

    Article  PubMed  Google Scholar 

  22. Haxby, J. V. et al. Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293, 2425–2430 (2001).

    Article  CAS  PubMed  Google Scholar 

  23. Kriegeskorte, N. et al. Matching categorical object representations in inferior temporal cortex of man and monkey. Neuron 60, 1126–1141 (2008). A study in which a data-driven representational similarity approach is used to show that the representational hierarchy of object categories is similar in the human VTC and monkey IT.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Chao, L. L., Haxby, J. V. & Martin, A. Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nature Neurosci. 2, 913–919 (1999).

    Article  CAS  PubMed  Google Scholar 

  25. Cukur, T., Huth, A. G., Nishimoto, S. & Gallant, J. L. Functional subdomains within human FFA. J. Neurosci. 33, 16748–16766 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Huth, A. G., Nishimoto, S., Vu, A. T. & Gallant, J. L. A continuous semantic space describes the representation of thousands of object and action categories across the human brain. Neuron 76, 1210–1224 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Konkle, T. & Oliva, A. A real-world size organization of object responses in occipitotemporal cortex. Neuron 74, 1114–1124 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Caspers, J. et al. Cytoarchitectonical analysis and probabilistic mapping of two extrastriate areas of the human posterior fusiform gyrus. Brain Struct. Funct. 218, 511–526 (2013).

    Article  PubMed  Google Scholar 

  29. Caspers, J. et al. Receptor architecture of visual areas in the face and word-form recognition region of the posterior fusiform gyrus. Brain Struct. Funct. http://dx.doi.org/10.1007/s00429-013-0646-z (2013).

  30. Saygin, Z. M. et al. Anatomical connectivity patterns predict face selectivity in the fusiform gyrus. Nature Neurosci. 15, 321–327 (2012). The authors use a novel methodology to show that functionally defined regions in the VTC can be defined from their fingerprint of white-matter connections to the rest of the brain. They show that structure–function relationships in the VTC are so consistent that connectivity in one group of subjects can predict the functional organization of the VTC in a separate group of subjects.

    Article  CAS  Google Scholar 

  31. Pyles, J. A., Verstynen, T. D., Schneider, W. & Tarr, M. J. Explicating the face perception network with white matter connectivity. PLoS ONE 8, e61611 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Gschwind, M., Pourtois, G., Schwartz, S., Van De Ville, D. & Vuilleumier, P. White-matter connectivity between face-responsive regions in the human brain. Cereb. Cortex 22, 1564–1576 (2012).

    Article  PubMed  Google Scholar 

  33. Nasr, S. et al. Scene-selective cortical regions in human and nonhuman primates. J. Neurosci. 31, 13771–13785 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Witthoft, N. et al. Where is human V4? Predicting the location of hV4 and VO1 from cortical folding. Cereb. Cortex http://dx.doi.org/10.1093/cercor/bht092 (2013).

  35. Marr, D. Vision: A Computational Approach (Freeman & Co., 1982). In this book, published posthumously, David Marr established the field of computational vision.

    Google Scholar 

  36. Zeki, S. & Shipp, S. The functional logic of cortical connections. Nature 335, 311–317 (1988). A review linking the anatomical construction of the visual system to information processing. One of the many key insights is how divergent and convergent connections enable information segregation and integration, respectively.

    Article  CAS  PubMed  Google Scholar 

  37. Van Essen, D. C., Anderson, C. H. & Felleman, D. J. Information processing in the primate visual system: an integrated systems perspective. Science 255, 419–423 (1992). A review linking anatomical organization of the visual system to information processing through an integrated systems perspective. It discusses the definition of cortical areas and processing streams, as well as modularity, distributed hierarchies and computational flexibility.

    Article  CAS  PubMed  Google Scholar 

  38. Ullman, S. High-Level Vision: Object Recognition and Visual Cognition (Bradford Books, 1996).

    Book  Google Scholar 

  39. Selfridge, O. G. in Mechanisation of Thought Processes. Proceedings of a Symposium held at the National Physical Laboratory on 24th, 25th, 26th and 27th November 1958 Vol. 1 513–526 (H.M. Stationery Office, 1959).

    Google Scholar 

  40. Riesenhuber, M. & Poggio, T. Hierarchical models of object recognition in cortex. Nature Neurosci. 2, 1019–1025 (1999).

    Article  CAS  PubMed  Google Scholar 

  41. Serre, T., Oliva, A. & Poggio, T. A feedforward architecture accounts for rapid categorization. Proc. Natl Acad. Sci. USA 104, 6424–6429 (2007).

    Article  CAS  PubMed  Google Scholar 

  42. Fukushima, K. Neocognitron: a hierarchical neural network capable of visual pattern recognition. Neural Networks 1, 119–130 (1982).

    Article  Google Scholar 

  43. Epshtein, B., Lifshitz, I. & Ullman, S. Image interpretation by a single bottom-up top-down cycle. Proc. Natl Acad. Sci. USA 105, 14298–14303 (2008).

    Article  PubMed  Google Scholar 

  44. Rosenblatt, F. The perceptron: a probabilistic model for information storage and organization in the brain. Psychol. Rev. 65, 386–408 (1958).

    Article  CAS  PubMed  Google Scholar 

  45. Vandewalle, J. & Suykens, J. A. K. Least squares support vector machine classifiers. Neural Process. Lett. 9, 293–300 (1999).

    Article  Google Scholar 

  46. Edelman, S. & Duvdevani-Bar, S. A model of visual recognition and categorization. Phil. Trans. R. Soc. Lond. B 352, 1191–1202 (1997).

    Article  CAS  Google Scholar 

  47. Poggio, T. & Girosi, F. Regularization algorithms for learning that are equivalent to multilayer networks. Science 247, 978–982 (1990).

    Article  CAS  PubMed  Google Scholar 

  48. Rust, N. C. & Dicarlo, J. J. Selectivity and tolerance (“invariance”) both increase as visual information propagates from cortical area V4 to IT. J. Neurosci. 30, 12978–12995 (2010). An examination of information transformations across the ventral processing stream in macaques. Results show that as receptive fields increase in size from V4 to IT, neural responses become more selective to feature conjunctions and more tolerant to position and scale.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Rosch, E., Mervis, C. B., Gray, W. D., Johnson, D. M. & Boyes-Braem, P. Basic objects in natural categories. Cogn. Psychol. 8, 382–439 (1976).

    Article  Google Scholar 

  50. Peelen, M. V. & Downing, P. E. Selectivity for the human body in the fusiform gyrus. J. Neurophysiol. 93, 603–608 (2005).

    Article  PubMed  Google Scholar 

  51. Cohen, L. et al. The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. Brain 123, 291–307 (2000).

    Article  PubMed  Google Scholar 

  52. Edelman, S., Grill-Spector, K., Kusnir, T. & Malach, R. Towards direct visualization of the internal shape space by fMRI. Psychobiology 26, 309–321 (1998).

    Google Scholar 

  53. 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).

    Article  CAS  PubMed  Google Scholar 

  54. Mendola, J. D., Dale, A. M., Fischl, B., Liu, A. K. & Tootell, R. B. The representation of illusory and real contours in human cortical visual areas revealed by functional magnetic resonance imaging. J. Neurosci. 19, 8560–8572 (1999).

    Article  CAS  PubMed  Google Scholar 

  55. Kourtzi, Z. & Kanwisher, N. Representation of perceived object shape by the human lateral occipital complex. Science 293, 1506–1509 (2001).

    Article  CAS  PubMed  Google Scholar 

  56. Vinberg, J. & Grill-Spector, K. Representation of shapes, edges, and surfaces across multiple cues in the human visual cortex. J. Neurophysiol. 99, 1380–1393 (2008).

    Article  PubMed  Google Scholar 

  57. Avidan, G. et al. Contrast sensitivity in human visual areas and its relationship to object recognition. J. Neurophysiol. 87, 3102–3116 (2002).

    Article  PubMed  Google Scholar 

  58. Ishai, A., Ungerleider, L. G., Martin, A. & Haxby, J. V. The representation of objects in the human occipital and temporal cortex. J. Cogn. Neurosci. 12 (Suppl. 2), 35–51 (2000).

    Article  PubMed  Google Scholar 

  59. Spiridon, M. & Kanwisher, N. How distributed is visual category information in human occipito-temporal cortex? An fMRI study. Neuron 35, 1157–1165 (2002).

    Article  CAS  PubMed  Google Scholar 

  60. Walther, D. B., Chai, B., Caddigan, E., Beck, D. M. & Fei-Fei, L. Simple line drawings suffice for functional MRI decoding of natural scene categories. Proc. Natl Acad. Sci. USA 108, 9661–9666 (2011).

    Article  PubMed  Google Scholar 

  61. Grill-Spector, K., Knouf, N. & Kanwisher, N. The fusiform face area subserves face perception, not generic within-category identification. Nature Neurosci. 7, 555–562 (2004). This article shows that neural responses in face-selective regions on the fusiform gyrus are correlated with both the detection and identification of faces but not within-category identification of non-face objects.

    Article  CAS  PubMed  Google Scholar 

  62. Grill-Spector, K. et al. Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron 24, 187–203 (1999).

    Article  CAS  PubMed  Google Scholar 

  63. Schwarzlose, R. F., Swisher, J. D., Dang, S. & Kanwisher, N. The distribution of category and location information across object-selective regions in human visual cortex. Proc. Natl Acad. Sci. USA 105, 4447–4452 (2008).

    Article  PubMed  Google Scholar 

  64. Andrews, T. J. & Ewbank, M. P. Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe. Neuroimage 23, 905–913 (2004).

    Article  PubMed  Google Scholar 

  65. MacEvoy, S. P. & Epstein, R. A. Position selectivity in scene- and object-responsive occipitotemporal regions. J. Neurophysiol. 98, 2089–2098 (2007).

    Article  PubMed  Google Scholar 

  66. Liu, H., Agam, Y., Madsen, J. R. & Kreiman, G. Timing, timing, timing: fast decoding of object information from intracranial field potentials in human visual cortex. Neuron 62, 281–290 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Kravitz, D. J., Kriegeskorte, N. & Baker, C. I. High-level visual object representations are constrained by position. Cereb. Cortex 20, 2916–2925 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Eger, E., Schyns, P. G. & Kleinschmidt, A. Scale invariant adaptation in fusiform face-responsive regions. Neuroimage 22, 232–242 (2004).

    Article  PubMed  Google Scholar 

  69. Vuilleumier, P., Henson, R. N., Driver, J. & Dolan, R. J. Multiple levels of visual object constancy revealed by event-related fMRI of repetition priming. Nature Neurosci. 5, 491–499 (2002).

    Article  CAS  PubMed  Google Scholar 

  70. Axelrod, V. & Yovel, G. Hierarchical processing of face viewpoint in human visual cortex. J. Neurosci. 32, 2442–2452 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Kietzmann, T. C., Swisher, J. D., Konig, P. & Tong, F. Prevalence of selectivity for mirror-symmetric views of faces in the ventral and dorsal visual pathways. J. Neurosci. 32, 11763–11772 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Freiwald, W. A. & Tsao, D. Y. Functional compartmentalization and viewpoint generalization within the macaque face-processing system. Science 330, 845–851 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Epstein, R., Graham, K. S. & Downing, P. E. Viewpoint-specific scene representations in human parahippocampal cortex. Neuron 37, 865–876 (2003).

    Article  CAS  PubMed  Google Scholar 

  74. Downing, P. E., Chan, A. W., Peelen, M. V., Dodds, C. M. & Kanwisher, N. Domain specificity in visual cortex. Cereb. Cortex 16, 1453–1461 (2006).

    Article  CAS  PubMed  Google Scholar 

  75. Mur, M. et al. Categorical, yet graded—single-image activation profiles of human category-selective cortical regions. J. Neurosci. 32, 8649–8662 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. 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).

    Article  CAS  PubMed  Google Scholar 

  77. Davidesco, I. et al. Exemplar selectivity reflects perceptual similarities in the human fusiform cortex. Cereb. Cortex http://dx.doi.org/10.1093/cercor/bht038 (2013).

  78. Jacques, C. et al. Electrocorticography of category-selectivity in human ventral temporal cortex: spatial organization, responses to single images, and coupling with fMRI. J. Vision 13, 495 (2013).

    Article  Google Scholar 

  79. Bastin, J. et al. Temporal components in the parahippocampal place area revealed by human intracerebral recordings. J. Neurosci. 33, 10123–10131 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Weiner, K. S. & Grill-Spector, K. Sparsely-distributed organization of face and limb activations in human ventral temporal cortex. Neuroimage 52, 1559–1573 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  81. Sayres, R. & Grill-Spector, K. Relating retinotopic and object-selective responses in human lateral occipital cortex. J. Neurophysiol. 100, 249–267 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  82. Walther, D. B., Caddigan, E., Fei-Fei, L. & Beck, D. M. Natural scene categories revealed in distributed patterns of activity in the human brain. J. Neurosci. 29, 10573–10581 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Haushofer, J., Livingstone, M. S. & Kanwisher, N. Multivariate patterns in object-selective cortex dissociate perceptual and physical shape similarity. PLoS Biol. 6, e187 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Drucker, D. M. & Aguirre, G. K. Different spatial scales of shape similarity representation in lateral and ventral LOC. Cereb. Cortex 19, 2269–2280 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  85. Davidenko, N., Remus, D. A. & Grill-Spector, K. Face-likeness and image variability drive responses in human face-selective ventral regions. Hum. Brain Mapp. 33, 2234–2249 (2012).

    Article  Google Scholar 

  86. O'Toole, A. J., Jiang, F., Abdi, H. & Haxby, J. V. Partially distributed representations of objects and faces in ventral temporal cortex. J. Cogn. Neurosci. 17, 580–590 (2005).

    Article  PubMed  Google Scholar 

  87. Connolly, A. C. et al. The representation of biological classes in the human brain. J. Neurosci. 32, 2608–2618 (2012). This study examines distributed responses in the VTC and shows that there is a hierarchy of animate classes, ranging from insects, to birds, to mammals.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Op de Beeck, H. P., Brants, M., Baeck, A. & Wagemans, J. Distributed subordinate specificity for bodies, faces, and buildings in human ventral visual cortex. Neuroimage 49, 3414–3425 (2010).

    Article  PubMed  Google Scholar 

  89. Orlov, T., Makin, T. R. & Zohary, E. Topographic representation of the human body in the occipitotemporal cortex. Neuron 68, 586–600 (2010).

    Article  CAS  PubMed  Google Scholar 

  90. Fujita, I., Tanaka, K., Ito, M. & Cheng, K. Columns for visual features of objects in monkey inferotemporal cortex. Nature 360, 343–346 (1992).

    Article  CAS  PubMed  Google Scholar 

  91. Adams, D. L., Sincich, L. C. & Horton, J. C. Complete pattern of ocular dominance columns in human primary visual cortex. J. Neurosci. 27, 10391–10403 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Mountcastle, V. B. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J. Neurophysiol. 20, 408–434 (1957).

    Article  CAS  PubMed  Google Scholar 

  93. Tsao, D. Y., Freiwald, W. A., Tootell, R. B. & Livingstone, M. S. A cortical region consisting entirely of face-selective cells. Science 311, 670–674 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Engel, S. A. et al. fMRI of human visual cortex. Nature 369, 525 (1994).

    Article  CAS  PubMed  Google Scholar 

  95. Afraz, S. R., Kiani, R. & Esteky, H. Microstimulation of inferotemporal cortex influences face categorization. Nature 442, 692–695 (2006).

    Article  CAS  PubMed  Google Scholar 

  96. Parvizi, J. et al. Electrical stimulation of human fusiform face-selective regions distorts face perception. J. Neurosci. 32, 14915–14920 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Pinsk, M. A., DeSimone, K., Moore, T., Gross, C. G. & Kastner, S. Representations of faces and body parts in macaque temporal cortex: a functional MRI study. Proc. Natl Acad. Sci. USA 102, 6996–7001 (2005).

    Article  CAS  PubMed  Google Scholar 

  98. Bell, A. H. et al. Relationship between functional magnetic resonance imaging-identified regions and neuronal category selectivity. J. Neurosci. 31, 12229–12240 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Srihasam, K., Mandeville, J. B., Morocz, I. A., Sullivan, K. J. & Livingstone, M. S. Behavioural and anatomical consequences of early versus late symbol training in macaques. Neuron 73, 608–619 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Malach, R. et al. Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc. Natl Acad. Sci. USA 92, 8135–8139 (1995).

    Article  CAS  PubMed  Google Scholar 

  101. Grill-Spector, K., Kourtzi, Z. & Kanwisher, N. The lateral occipital complex and its role in object recognition. Vision Res. 41, 1409–1422 (2001).

    Article  CAS  PubMed  Google Scholar 

  102. Issa, E. B., Papanastassiou, A. M. & DiCarlo, J. J. Large-scale, high-resolution neurophysiological maps underlying fMRI of macaque temporal lobe. J. Neurosci. 33, 15207–15219 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Weiner, K. S. & Grill-Spector, K. Not one extrastriate body area: using anatomical landmarks, hMT+, and visual field maps to parcellate limb-selective activations in human lateral occipitotemporal cortex. Neuroimage 56, 2183–2199 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  104. Weiner, K. S., Sayres, R., Vinberg, J. & Grill-Spector, K. fMRI-adaptation and category selectivity in human ventral temporal cortex: regional differences across timescales. J. Neurophysiol. 103, 3349–3365 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  105. Witthoft, N., Golarai, G., Nguyen, M., Liberman, A. & Grill-Spector, K. Anatomy, retinotopy, & category selectivity in human ventral visual cortex. J. Vision 12, 1177 (2012).

    Article  Google Scholar 

  106. Hanson, S. J. & Schmidt, A. High-resolution imaging of the fusiform face area (FFA) using multivariate nonlinear classifiers shows diagnosticity for non-face categories. Neuroimage 54, 1715–1734 (2011).

    Article  PubMed  Google Scholar 

  107. Grill-Spector, K., Sayres, R. & Ress, D. High-resolution imaging reveals highly selective nonface clusters in the fusiform face area. Nature Neurosci. 9, 1177–1185 (2006).

    Article  CAS  PubMed  Google Scholar 

  108. Albright, T. D. Direction and orientation selectivity of neurons in visual area MT of the macaque. J. Neurophysiol. 52, 1106–1130 (1984).

    Article  CAS  PubMed  Google Scholar 

  109. Albright, T. D., Desimone, R. & Gross, C. G. Columnar organization of directionally selective cells in visual area MT of the macaque. J. Neurophysiol. 51, 16–31 (1984).

    Article  CAS  PubMed  Google Scholar 

  110. Huntgeburth, S. C. & Petrides, M. Morphological patterns of the collateral sulcus in the human brain. Eur. J. Neurosci. 35, 1295–1311 (2012).

    Article  PubMed  Google Scholar 

  111. Yeatman, J. D., Rauschecker, A. M. & Wandell, B. A. Anatomy of the visual word form area: adjacent cortical circuits and long-range white matter connections. Brain Lang. 125, 146–155 (2013).

    Article  PubMed  Google Scholar 

  112. Glezer, L. S. & Riesenhuber, M. Individual variability in location impacts orthographic selectivity in the “visual word form area”. J. Neurosci. 33, 11221–11226 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Weiner, K. S. & Grill-Spector, K. Neural representations of faces and limbs neighbour in human high-level visual cortex: evidence for a new organization principle. Psychol. Res. 77, 74–97 (2013).

    Article  PubMed  Google Scholar 

  114. Winawer, J., Horiguchi, H., Sayres, R. A., Amano, K. & Wandell, B. A. Mapping hV4 and ventral occipital cortex: the venous eclipse. J. Vis. 10, 1 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  115. Kohonen, T. Self-Organization and Associative Memory (Springer, 1983).

    Google Scholar 

  116. Haxby, J. V. et al. A common, high-dimensional model of the representational space in human ventral temporal cortex. Neuron 72, 404–416 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Martin, A., Wiggs, C. L., Ungerleider, L. G. & Haxby, J. V. Neural correlates of category-specific knowledge. Nature 379, 649–652 (1996).

    Article  CAS  PubMed  Google Scholar 

  118. Beauchamp, M. S., Lee, K. E., Haxby, J. V. & Martin, A. Parallel visual motion processing streams for manipulable objects and human movements. Neuron 34, 149–159 (2002).

    Article  CAS  PubMed  Google Scholar 

  119. Mahon, B. Z., Anzellotti, S., Schwarzbach, J., Zampini, M. & Caramazza, A. Category-specific organization in the human brain does not require visual experience. Neuron 63, 397–405 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Levy, I., Hasson, U., Avidan, G., Hendler, T. & Malach, R. Center-periphery organization of human object areas. Nature Neurosci. 4, 533–539 (2001).

    Article  CAS  PubMed  Google Scholar 

  121. Weiner, K. S. & Grill-Spector, K. Improbable simplicity of the fusiform face area. Trends Cogn. Sci. 16, 251–254 (2012).

    Article  PubMed  Google Scholar 

  122. Glasser, M. F. & Van Essen, D. C. Mapping human cortical areas in vivo based on myelin content as revealed by T1- and T2-weighted MRI. J. Neurosci. 31, 11597–11616 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Van Essen, D. C. et al. The WU-Minn Human Connectome Project: an overview. Neuroimage 80, 62–79 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  124. Malach, R. Cortical columns as devices for maximizing neuronal diversity. Trends Neurosci. 17, 101–104 (1994).

    Article  CAS  PubMed  Google Scholar 

  125. Moeller, S., Freiwald, W. A. & Tsao, D. Y. Patches with links: a unified system for processing faces in the macaque temporal lobe. Science 320, 1355–1359 (2008).

    Article  CAS  PubMed  Google Scholar 

  126. Kornblith, S., Cheng, X., Ohayon, S. & Tsao, D. Y. A network for scene processing in the macaque temporal lobe. Neuron 79, 766–781 (2013).

    Article  CAS  PubMed  Google Scholar 

  127. Van Essen, D. C. A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385, 313–318 (1997).

    Article  CAS  PubMed  Google Scholar 

  128. Issa, E. B. & DiCarlo, J. J. Precedence of the eye region in neural processing of faces. J. Neurosci. 32, 16666–16682 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Perrett, D. I., Hietanen, J. K., Oram, M. W. & Benson, P. J. Organization and functions of cells responsive to faces in the temporal cortex. Phil. Trans. R. Soc. Lond. B 335, 23–30 (1992).

    Article  CAS  Google Scholar 

  130. Wang, G., Tanaka, K. & Tanifuji, M. Optical imaging of functional organization in the monkey inferotemporal cortex. Science 272, 1665–1668 (1996).

    Article  CAS  PubMed  Google Scholar 

  131. Tsunoda, K., Yamane, Y., Nishizaki, M. & Tanifuji, M. Complex objects are represented in macaque inferotemporal cortex by the combination of feature columns. Nature Neurosci. 4, 832–838 (2001).

    Article  CAS  PubMed  Google Scholar 

  132. Jiang, X. et al. Categorization training results in shape- and category-selective human neural plasticity. Neuron 53, 891–903 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Tanaka, K. Inferotemporal cortex and object vision. Annu. Rev. Neurosci. 19, 109–139 (1996).

    Article  CAS  PubMed  Google Scholar 

  134. Kravitz, D. J., Saleem, K. S., Baker, C. I., Ungerleider, L. G. & Mishkin, M. The ventral visual pathway: an expanded neural framework for the processing of object quality. Trends Cogn. Sci. 17, 26–49 (2013). A review linking anatomical features to recurrent processing networks in the macaque ventral visual processing stream. Modern insights are incorporated into the classic understanding of the anatomical and functional construction of the ventral visual pathway across species.

    Article  PubMed  Google Scholar 

  135. Mezer, A. et al. Quantifying the local tissue volume and composition in individual brains with magnetic resonance imaging. Nature Med. 19, 1667–1672 (2013).

    Article  CAS  PubMed  Google Scholar 

  136. Holmes, G. Disturbances of vision by cerebral lesions. Br. J. Ophthalmol. 2, 353–384 (1918).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Hasnain, M. K., Fox, P. T. & Woldorff, M. G. Structure–function spatial covariance in the human visual cortex. Cereb. Cortex 11, 702–716 (2001).

    Article  CAS  PubMed  Google Scholar 

  138. Benson, N. C., Butt, O. H., Brainard, D. H. & Aguirre, G. K. Correction of distortion in flattened representations of the cortical surface allows prediction of V1-V3 functional organization from anatomy. PLoS Comput. Biol. 10, e1003538 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Tootell, R. B. et al. Functional analysis of V3A and related areas in human visual cortex. J. Neurosci. 17, 7060–7078 (1997).

    Article  CAS  PubMed  Google Scholar 

  140. Fischl, B. et al. Cortical folding patterns and predicting cytoarchitecture. Cereb. Cortex 18, 1973–1980 (2008).

    Article  PubMed  Google Scholar 

  141. Dumoulin, S. O. et al. A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. Cereb. Cortex 10, 454–463 (2000).

    Article  CAS  PubMed  Google Scholar 

  142. Braitenberg, V. & Schüz, A. Anatomy of the Cortex (Springer, 1991).

    Book  Google Scholar 

  143. Hubel, D. H. & Wiesel, T. N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. 160, 106–154 (1962).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I. & Moser, M. B. Path integration and the neural basis of the 'cognitive map'. Nature Rev. Neurosci. 7, 663–678 (2006).

    Article  CAS  Google Scholar 

  145. O'Toole, A. J., Roark, D. A. & Abdi, H. Recognizing moving faces: a psychological and neural synthesis. Trends Cogn. Sci. 6, 261–266 (2002).

    Article  PubMed  Google Scholar 

  146. Tootell, R. B. et al. Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J. Neurosci. 15, 3215–3230 (1995).

    Article  CAS  PubMed  Google Scholar 

  147. Stigliani, A., Weiner, K. S. & Grill-Spector, K. Differential rate of temporal processing across category-selective regions in human high-level visual cortex. Vision Sci. Soc. Abstr. 23.579 (2014).

  148. Gross, C. G., Bender, D. B. & Rocha-Miranda, C. E. Visual receptive fields of neurons in inferotemporal cortex of the monkey. Science 166, 1303–1306 (1969).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank C. Jacques for creating figure 2b, and N. Davidenko for creating figure 2a. The authors thank D. Van Essen, M. Glasser, J. Caspers, S. Nasr, T. Konkle and Z. M. Saygin for providing access to their data and contributing to figure 4. The authors thank A. Connolly, J. S. Guntupalli, J. V. Haxby, E. Issa and N. Kriegeskorte for permission to use their figures. This work was supported by the National Science Foundation, BCS grant 0920865 and National Eye Institute grant NIH 1 RO1 EY 02231801A1.

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  1. Department of Psychology, Stanford University, Stanford, 94305, California, USA

    Kalanit Grill-Spector & Kevin S. Weiner

  2. Stanford Neuroscience Institute, Stanford University, Stanford, 94305, California, USA

    Kalanit Grill-Spector

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  1. Kalanit Grill-Spector
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Correspondence to Kalanit Grill-Spector.

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FURTHER INFORMATION

Human Connectome Project

PowerPoint slides

Glossary

Visual categorization and recognition

Determining, from the visual input, what it is that we see. These processes involve multiple levels of abstraction: exemplar ('my car'); subordinate category ('Volkswagen Beetle'); basic category ('car') and superordinate category ('vehicle').

Ventral temporal cortex

(VTC). An anatomical section of the human temporal lobe that includes the fusiform gyrus, parahippocampal gyrus and their bounding sulci.

Agnosia

A condition characterized by a loss of the ability to recognize objects, people or shapes but in which basic visual acuity and memory are preserved.

Eccentricity bias

A preference for particular eccentricities, such as the centre or periphery.

Tolerance

The ability to generalize across a transformation (such as size, position, illumination or view) that affects the appearance of an exemplar.

Separable representations

Representations that can be divided by a linear boundary.

Basic-level

The mid-level (typically entry-level) of the category hierarchy; members have the most shared features and are most distinct from other categories (for example, car versus face).

Superordinate-level

The broadest level of the category hierarchy. It has a high degree of generality; members share fewer attributes than members of basic-level categories (for example, animate versus inanimate).

Subordinate-level

The most specific level of the category hierarchy; members share more features than members of basic-level categories (for example, Honda Civic versus Toyota Corolla).

Category hierarchies

A differentiation of superordinate, basic-level and subordinate categories.

Topological organization

An orderly spatial arrangement of functional representations across the cortex.

Eccentricity

Distance from the centre of gaze. It is measured in units of visual angle.

Inferotemporal cortex

(IT). An anatomical section in the inferior aspect of the temporal lobe in the macaque brain that is thought to be homologous to the ventral temporal cortex in humans.

Fusiform body area

(FBA). A region in the occipital temporal sulcus (OTS) that selectively responds to images of human bodies and body parts. It is also referred to as OTS-limbs.

Lateral occipital complex

(LOC). A constellation of object-selective regions in humans that includes a region (termed LO) in the lateral occipital cortex that overlaps with LO-2, and a region (named posterior fusiform/occipitotemporal sulcus (pFus/OTS)) in the ventral temporal cortex that overlaps with the posterior fusiform gyrus and OTS.

Retinotopy

A representation in which adjacent points on the retina are mapped to adjacent points in the cortex.

Voxel

Volume pixel.

Parahippocampal place area

(PPA). A region that responds selectively to scenes, places and houses over other visual stimuli. Recent studies show that place-selective activations are actually located in the collateral sulcus (CoS) rather than in the parahippocampal gyrus. This area is also referred to as CoS-places.

Fusiform face area

(FFA). A region in the lateral fusiform gyrus that selectively responds to faces compared to other animate or inanimate stimuli. Recent measurements indicate anatomically and functionally distinct divisions of the FFA, which are referred to as posterior fusiform face-selective region (pFus-Faces; also known as FFA-1) and mid-fusiform face-selective region (mFus-faces; also known as FFA-2).

Posterior transverse collateral sulcus

(ptCoS). A sulcus that is transverse to the posterior edge of the lateral branch of the CoS and separates the occipital lobe from the temporal lobes.

Mid-fusiform sulcus

(MFS). A longitudinal sulcus that bisects the fusiform gyrus.

Convergent representations

Superimposition of multiple functional representations on the same cortical location.

Divergent representations

Spatially distinct functional representations in the cortex.

Cytoarchitectonic

The arrangement (for example, columnar), properties (for example, density and cell size) and characteristic layout of neuronal cell bodies in the brain.

Intermediate complexity features

Visual features that contain more than one low-level feature: for example, a shape with an elaborated contour or a coloured shape.

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Grill-Spector, K., Weiner, K. The functional architecture of the ventral temporal cortex and its role in categorization. Nat Rev Neurosci 15, 536–548 (2014). https://doi.org/10.1038/nrn3747

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