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fMRI evidence for objects as the units of attentional selection

Abstract

Contrasting theories of visual attention emphasize selection by spatial location1, visual features (such as motion or colour)2,3,4 or whole objects5,6. Here we used functional magnetic resonance imaging (fMRI) to test key predictions of the object-based theory, which proposes that pre-attentive mechanisms segment the visual array into discrete objects, groups, or surfaces, which serve as targets for visual attention5,6,7,8,9. Subjects viewed stimuli consisting of a face transparently superimposed on a house, with one moving and the other stationary. In different conditions, subjects attended to the face, the house or the motion. The magnetic resonance signal from each subject's fusiform face area10, parahippocampal place area11 and area MT/MST12 provided a measure of the processing of faces, houses and visual motion, respectively. Although all three attributes occupied the same location, attending to one attribute of an object (such as the motion of a moving face) enhanced the neural representation not only of that attribute but also of the other attribute of the same object (for example, the face), compared with attributes of the other object (for example, the house). These results cannot be explained by models in which attention selects locations or features, and provide physiological evidence that whole objects are selected even when only one visual attribute is relevant.

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Figure 1: Sample stimuli.
Figure 2: Design and results of Experiment 1.
Figure 3: Means of the peak evoked responses from Experiment 2 in the FFA and PPA as a function of task (attend moving or attend static) and stimulus (face moving or house moving).

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References

  1. Posner,M. I. Orienting of attention. Q. J. Exp. Psychol. 32, 3–25 (1980).

    Article  CAS  Google Scholar 

  2. Treisman,A. M. Strategies and models of selective attention. Psychol. Rev. 76, 282–299 (1969).

    Article  CAS  Google Scholar 

  3. Corbetta,M. et al. Attentional modulation of neural processing of shape, color, and velocity in humans. Science 248, 1556–1559 (1990).

    Article  ADS  CAS  Google Scholar 

  4. Wolfe,J. M., Cave,K. R. & Franzel,S. L. Guided search: an alternative to the feature integration model for visual search. J. Exp. Psychol. Hum. Percept. Perf. 15, 419–433 (1989).

    Article  CAS  Google Scholar 

  5. Duncan,J. Selective attention and the organization of visual information. J. Exp. Psychol. Gen. 113, 501–517 (1984).

    Article  CAS  Google Scholar 

  6. He,Z. J. & Nakayama,K. Visual attention to surfaces in three-dimensional space. Proc. Natl Acad. Sci. USA 24, 11155–11159 (1995).

    Article  ADS  Google Scholar 

  7. Vandenberghe,R. et al. Attention to one or two features in left or right visual field: a positron emission tomography study. J. Neurosci. 17, 3739–3750 (1997).

    Article  CAS  Google Scholar 

  8. Roelfsema,P. R., Lamme,V. A. & Spekreijse,H. Object-based attention in the primary visual cortex of the macaque monkey. Nature 395, 376–381 (1998).

    Article  ADS  CAS  Google Scholar 

  9. Driver,J., Baylis,G. C., Goodrich,S. J. & Rafal,R. D. Axis-based neglect of visual shapes. Neuropsychologia 32, 1353–1365 (1994).

    Article  CAS  Google Scholar 

  10. Kanwisher,N., McDermott,J. & Chun,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 

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

    Article  ADS  CAS  Google Scholar 

  12. 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  Google Scholar 

  13. Eriksen,B. A. & Eriksen,C. W. Effects of noise letters upon the identification of target letters in a nonsearch task. Percept. Psychophys. 16, 143–149 (1974).

    Article  Google Scholar 

  14. Driver,J. & Baylis,G. C. Movement and visual attention: The spotlight metaphor breaks down. J. Exp. Psychol. Hum. Percept. Perf. 15, 448–456 (1989).

    Article  CAS  Google Scholar 

  15. Rosen,B. R., Buckner,R. L. & Dale,A. M. Event-related functional MRI: Past, present, and future. Proc. Natl Acad. Sci. USA 95, 773–780 (1998).

    Article  ADS  CAS  Google Scholar 

  16. O'Craven,K. M., Rosen,B. R., Kwong,K. K., Treisman,A. & Savoy,R. L. Voluntary attention modulates fMRI activity in human MT-MST Neuron 18, 591–598 (1997).

    Article  CAS  Google Scholar 

  17. Beauchamp,M. S., Cox,R. W. & DeYoe,E. A. Graded effects of spatial and featural attention on human area MT and associated motion processing areas. J. Neurophys. 78, 516–520 (1997).

    Article  CAS  Google Scholar 

  18. Treue,S. & Trujillo,J. C. M. Feature-based attention influences motion processing in macaque visual cortex. Nature 399, 575–579 (1999).

    Article  ADS  CAS  Google Scholar 

  19. Hillyard,S. A. & Munte,T. F. Selective attention to color and location: An analysis with event-related brain potentials. Percept. Psychophys. 36, 185–198 (1984).

    Article  CAS  Google Scholar 

  20. Courtney,S. M., Ungerleider,L. G., Keil,K. & Haxby,J. V. Transient and sustained activity in a distributed neural system for human working memory. Nature 386, 608–611 (1997).

    Article  ADS  CAS  Google Scholar 

  21. Salzman,C. D. & Newsome,W. T. Neural mechanisms for forming a perceptual decision. Science 264, 231–237 (1994).

    Article  ADS  CAS  Google Scholar 

  22. Mangun,G. & Hillyard,S. A. Allocation of visual attention to spatial location: Tradeoff functions for event related brain potentials and detection performance. Percept. Psychophys. 47, 532–550 (1990).

    Article  CAS  Google Scholar 

  23. Brefczynski,J. A. & DeYoe,E. A. A physiological correlate of the ‘spotlight’ of visual attention. Nature Neurosci. 4, 370–374 (1999).

    Article  Google Scholar 

  24. Somers,D. C., Dale,A. M., Seiffert,A. E. & Tootell,R. B. Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. Proc. Natl Acad. Sci. USA 96, 1663–1668 (1999).

    Article  ADS  CAS  Google Scholar 

  25. Gandhi,S. P., Heeger,D. J. & Boynton,G. M. Spatial attention affects brain activity in human primary visual cortex. Proc. Natl Acad. Sci. USA 96, 3314–3319 (1999).

    Article  ADS  CAS  Google Scholar 

  26. Valdes-Sosa,M., Bobes,M., Rodriguez,V. & Pinilla,T. Switching attention without shifting the spotlight: Object-based attentional modulation of brain potentials. J. Cogn. Neurosci. 10, 137–151 (1998).

    Article  CAS  Google Scholar 

  27. Desimone,R. & Duncan,J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193–222 (1995).

    Article  CAS  Google Scholar 

  28. Kastner,S., Pinsk,M. A., De Weerd,P., Desimone,R. & Ungerleider,L. G. Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. Neuron 22, 751–761 (1999).

    Article  CAS  Google Scholar 

  29. Treisman,A. M. & Gelade,G. A feature-integration theory of attention. Cogn. Psychol. 12, 97–136 (1980).

    Article  CAS  Google Scholar 

  30. Qian,N., Andersen,R. A. & Adelson,E. H. Transparent motion perception as detection of unbalanced motion signals. I. Psychophysics. J. Neurosci. 14, 7357–7566 (1994).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank B. Rosen and others at the MGH-NMR Center for support; H. Wyatt for consultation on eye movements; and B. Anderson, J. Driver, R. Epstein, J. Mausell, M. Potter, G.Rainer, F. Tong, A. Wagner and members of our lab for comments on the manuscript.

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Correspondence to Nancy Kanwisher.

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O'Craven, K., Downing, P. & Kanwisher, N. fMRI evidence for objects as the units of attentional selection. Nature 401, 584–587 (1999). https://doi.org/10.1038/44134

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