Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects

Abstract

The cognitive and neural mechanisms underlying category-specific knowledge remain controversial. Here we report that, across multiple tasks (viewing, delayed match to sample, naming), pictures of animals and tools were associated with highly consistent, category-related patterns of activation in ventral (fusiform gyrus) and lateral (superior and middle temporal gyri) regions of the posterior temporal lobes. In addition, similar patterns of category-related activity occurred when subjects read the names of, and answered questions about, animals and tools. These findings suggest that semantic object information is represented in distributed networks that include sites for storing information about specific object attributes such as form (ventral temporal cortex) and motion (lateral temporal cortex).

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Examples of category-related activations in three representative subjects.
Figure 2: Amplitude and time course of category-related modulation.
Figure 3: Category-related activations during tool and house perception in voxels that responded to both stimuli in the medial fusiform region.
Figure 4: Pictures and words elicit common category-related activations.

Similar content being viewed by others

References

  1. Caramazza, A. & Shelton, J. R. Domain-specific knowledge systems in the brain: the animate-inanimate distinction. J. Cogn. Neurosci. 10, 1–34 (1998 ).

    Article  CAS  Google Scholar 

  2. Forde, E. M. E. & Humphreys, G. W. Category-specific recognition impairments: a review of important case studies and influential theories. Aphasiology 13, 169– 193 (1999).

    Article  Google Scholar 

  3. Perani, D. et al. Different neural systems for recognition of animals and man-made tools. Neuroreport 6, 1637– 1641 (1995).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Damasio, H., Grabowski, T. J., Tranel, D., Hichwa, R. D. & Damasio, A. R. A neural basis for lexical retrieval. Nature 380, 499–505 (1996).

    Article  CAS  Google Scholar 

  6. Tranel, D., Damasio, H. & Damasio, A. R. A neural basis for the retrieval of conceptual knowledge. Neuropsychologia 35, 1319– 1327 (1997).

    Article  CAS  Google Scholar 

  7. Pietrini, V. et al. Recovery from herpes simplex encephalitis: selective impairment of specific semantic categories with neuroradiological correlation. J. Neurol. Neurosurg. Psychiatry 51, 1284– 1293 (1988).

    Article  CAS  Google Scholar 

  8. Sartori, G., Miozzo, M. & Job, R. Category specific naming impairments? Yes. Q. J. Exp. Psychol. A 46, 489–509 ( 1993).

    Article  CAS  Google Scholar 

  9. Gainotti, G., Silveri, M. C., Daniele, A. & Giustolisi, L. Neuroanatomical correlates of category-specific impairments: a critical survey. Memory 3, 247–264 (1995).

    Article  CAS  Google Scholar 

  10. Bookheimer, S. Y., Zeffiro, T. A., Blaxton, T., Gaillard, W. & Theodore, W. Regional cerebral blood flow during object naming and word reading. Hum. Brain Mapp. 3, 93–106 (1995).

    Article  Google Scholar 

  11. Price, C. J., Moore, C. J., Humphreys, G. W., Frackowiak, R. S. & Friston, K. J. The neural regions sustaining object recognition and naming. Proc. R. Soc. Lond. B Biol. Sci. 263, 1501–1507 ( 1996).

    Article  CAS  Google Scholar 

  12. Büchel, C., Price, C. & Friston, K. A multimodal language region in the ventral visual pathway. Nature 394, 274–277 (1998).

    Article  Google Scholar 

  13. Vandenberghe, R., Price, C. J., Wise, R., Josephs, O. & Frackowiak, R. S. J. Functional anatomy of a common semantic system for words and pictures. Nature 383, 254– 256 (1996).

    Article  CAS  Google Scholar 

  14. Ricci, P. T. et al. Functional neuroanatomy of semantic memory: Recognition of semantic associations. Neuroimage 9, 88– 96 (1999).

    Article  CAS  Google Scholar 

  15. Mummery, C. J., Patterson, K., Hodges, J. R. & Wise, R. Retrieving "tiger" as an animal name or a word beginning with T: Differences in brain activation. Proc. R. Soc. Lond. B Biol. Sci. 263, 989–995 (1996).

    Article  CAS  Google Scholar 

  16. Mummery, C. J., Patterson, K., Hodges, J. R. & Price, C. J. Functional neuroanatomy of the semantic system: divisible by what? J. Cogn. Neurosci. 10, 766–777 (1998).

    Article  CAS  Google Scholar 

  17. Cappa, S. F., Perani, D., Schnur, T., Tettamanti, M. & Fazio, F. The effects of semantic category and knowledge type on lexical-semantic access: A PET study. Neuroimage 8, 350–359 (1998).

    Article  CAS  Google Scholar 

  18. Perani, D. et al. Word and picture matching: a PET study of semantic category effects. Neuropsychologia 37, 293– 306 (1999).

    Article  CAS  Google Scholar 

  19. Moore, C. J. & Price, C. J. A functional neuroimaging study of the variables that generate category-specific object processing differences. Brain 122, 943–962 (1999).

    Article  Google Scholar 

  20. Puce, A., Allison, T., Asgari, M., Gore, J. C. & McCarthy, G. Differential sensitivity of human visual cortex to faces, letter strings, and textures: a functional magnetic resonance imaging study. J. Neurosci. 16, 5205– 5215 (1996).

    Article  CAS  Google Scholar 

  21. Clark, V. P. et al. Functional magnetic resonance imaging (fMRI) of human visual cortex during face matching: a comparison with positron emission tomography (PET). Neuroimage 4, 1– 15. (1996).

    Article  CAS  Google Scholar 

  22. Kanwisher, N., McDermott, J. & Chun, M. M. The fusiform face area: a module in human extrastriate cortex specialized for the perception of faces. J. Neurosci. 17, 4302–4311 (1997).

    Article  CAS  Google Scholar 

  23. McCarthy, G., Puce, A., Gore, J. C. & Allison, T. Face-specific processing in the human fusiform gyrus. J. Cogn. Neurosci. 9, 605–610 (1997).

    Article  CAS  Google Scholar 

  24. Haxby, J. V. et al. The effect of face inversion on activity in human neural systems for face and object perception. Neuron 22, 189–199 (1999).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  26. Aguirre, G. K., Zarahn, E. & D'Esposito, M. An area within human ventral cortex sensitive to "building" stimuli: evidence and implications. Neuron 21, 373–383 (1998).

    Article  CAS  Google Scholar 

  27. Polk, T. A. & Farah, M. J. The neural development and organization of letter recognition: Evidence from functional neuroimaging, computational modeling, and behavioral studies. Proc. Natl. Acad. Sci. USA 95, 847–852 (1998 ).

    Article  CAS  Google Scholar 

  28. Ishai, A., Ungerleider, L. G., Martin, A., Schouten, J. L. & Haxby, J. V. Distributed representation of object form in the human ventral visual pathway. Proc. Natl. Acad. Sci. USA 96, 9379–9384 ( 1999).

    Article  CAS  Google Scholar 

  29. Martin, A., Ungerleider, L. G. & Haxby, J. V. in The Cognitive Neurosciences (ed. Gazzaniga, M. S.) (MIT Press, Cambridge, Massachusetts, in press).

  30. Ungerleider, L. G. & Haxby, J. V. 'What' and 'Where' in the human brain? Curr. Opin. Neurobiol. 4, 157–165 (1994).

    Article  CAS  Google Scholar 

  31. McNeil, J. E. & Warrington, E. K. Prosopagnosia: A face-specific disorder. Q. J. Exp. Psychol. A. 46A, 1– 10 (1993).

    Article  Google Scholar 

  32. Farah, M. J. Patterns of co-occurrence among the associative agnosia: Implications for visual object representation. Cognit. Neuropsychol. 3, 25–41 (1991).

    Google Scholar 

  33. Bonda, E., Petrides, M., Ostry, D. & Evans, A. Specific involvement of human parietal systems and the amygdala in the perception of biological motion. J. Neurosci. 16, 3737– 3744 (1996).

    Article  CAS  Google Scholar 

  34. Puce, A., Allison, T., Bentin, S., Gore, J. C. & McCarthy, G. Temporal cortex activation in humans viewing eye and mouth movements. J. Neurosci. 18, 2188– 2199 (1998).

    Article  CAS  Google Scholar 

  35. Perrett, D. I. et al. Social signals analyzed at the cell level: someone is looking at me, something touched me, something moved! Int. J. Comp. Psychol. 4, 25–54 ( 1990).

    Google Scholar 

  36. Oram, M. W. & Perrett, D. I. Responses of anterior superior temporal polysensory (STPa) neurons to "biological motion" stimuli. J. Cogn. Neurosci. 6, 99–116 (1994).

    Article  CAS  Google Scholar 

  37. Zeki, S. et al. A direct demonstration of functional specialization in human visual cortex. J. Neurosci. 11, 641– 649 (1991).

    Article  CAS  Google Scholar 

  38. Wise, R. et al. Distribution of cortical neural networks involved in word comprehension and word retrieval. Brain 114, 1803– 1817 (1991).

    Article  Google Scholar 

  39. Fiez, J. A., Raichle, M. E., Balota, D. A., Tallal, P. & Petersen, S. E. PET activation of posterior temporal regions during auditory word presentation and verb generation. Cereb. Cortex 6, 1–10 ( 1996).

    Article  CAS  Google Scholar 

  40. Martin, A., Haxby, J. V., Lalonde, F. M., Wiggs, C. L. & Ungerleider, L. G. Discrete cortical regions associated with knowledge of color and knowledge of action. Science 270, 102–105 ( 1995).

    Article  CAS  Google Scholar 

  41. Sheridan, J. & Humphreys, G. W. A verbal-semantic category-specific recognition impairment. Cognit. Neuropsychol. 10, 143–184 (1993).

    Article  Google Scholar 

  42. Laiacona, M., Capitani, E. & Barbarotto, R. Semantic category dissociation: a longitudinal study of two cases. Cortex 33, 441– 461 (1997).

    Article  CAS  Google Scholar 

  43. Funnell, E. & De Mornay Davies, P. JBR: A reassessment of concept familiarity and a category-specific disorder for living things. Neurocase 2, 461–474 ( 1997).

    Article  Google Scholar 

  44. Samson, D., Pillon, A. & De Wilde, V. Impaired knowledge of visual and non-visual attributes in a patient with a semantic impairment for living entities: a case of true category-specific deficit. Neurocase 4, 273–290 (1998).

    Article  Google Scholar 

  45. Thompson-Schill, S. L., Aguirre, G. K., D'Esposito, M. & Farah, M. J. A neural basis for category and modality specificity of semantic knowledge. Neuropsychologia 37, 671– 676 (1999).

    Article  CAS  Google Scholar 

  46. Grabowski, T. J., Damasio, H. & Damasio, A. R. Premotor and prefrontal correlates of category-related lexical retrieval. Neuroimage 7, 232– 243 (1998).

    Article  CAS  Google Scholar 

  47. Grafton, S. T., Fadiga, L., Arbib, M. A. & Rizzolatti, G. Premotor cortex activation during observation and naming of familiar tools. Neuroimage 6, 231–236 ( 1997).

    Article  CAS  Google Scholar 

  48. Friston, K. J. et al. Analysis of fMRI time-series revisited. Neuroimage 2, 45–53 (1995 ).

    Article  CAS  Google Scholar 

  49. Haxby, J. V., Maisog, J. M. & Courtney, S. M. in Mapping and Modeling the Human Brain (eds. Lancaster, J., Fox, P. & Friston, K.) (Wiley, New York, in press).

  50. Talairach, J. & Tournoux, P. Co-Planar Stereotaxic Atlas of the Human Brain (Thieme, New York, 1988).

    Google Scholar 

Download references

Acknowledgements

We thank Leslie Ungerleider for comments and Jill Weisberg and François Lalonde for technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alex Martin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chao, L., Haxby, J. & Martin, A. Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nat Neurosci 2, 913–919 (1999). https://doi.org/10.1038/13217

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/13217

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing