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Attention during natural vision warps semantic representation across the human brain

Nature Neuroscience volume 16, pages 763–770 (2013)Cite this article

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Abstract

Little is known about how attention changes the cortical representation of sensory information in humans. On the basis of neurophysiological evidence, we hypothesized that attention causes tuning changes to expand the representation of attended stimuli at the cost of unattended stimuli. To investigate this issue, we used functional magnetic resonance imaging to measure how semantic representation changed during visual search for different object categories in natural movies. We found that many voxels across occipito-temporal and fronto-parietal cortex shifted their tuning toward the attended category. These tuning shifts expanded the representation of the attended category and of semantically related, but unattended, categories, and compressed the representation of categories that were semantically dissimilar to the target. Attentional warping of semantic representation occurred even when the attended category was not present in the movie; thus, the effect was not a target-detection artifact. These results suggest that attention dynamically alters visual representation to optimize processing of behaviorally relevant objects during natural vision.

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Figure 1: Tuning-shift hypothesis predicts that attention warps semantic representation.
Figure 2: Voxel-wise tuning vectors are measured from BOLD responses evoked by natural movies.
Figure 3: Attentional tuning changes for a single voxel in lateral occipital complex.
Figure 4: Attention causes tuning shifts in single voxels.
Figure 5: Attention causes different degrees of tuning shifts in functional ROIs.
Figure 6: Semantic tuning for unattended categories shifts toward the attended category even when no targets are present.
Figure 7: Attention expands the representation of unattended categories that are semantically similar to the attended category.

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Acknowledgements

We thank D. Whitney for discussions regarding this manuscript. We also thank J. Gao, N. Bilenko, T. Naselaris, A. Vu and M. Oliver for their help in various aspects of this research. This work was supported by the National Eye Institute (EY019684 and EY022454) and the Center for Science of Information, a National Science Foundation Science and Technology Center, under grant agreement CCF-0939370.

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Author notes

  1. Shinji Nishimoto

    Present address: Present address: Center for Information and Neural Networks, National Institute of Information and Communications Technology, Suita, Osaka, Japan.,

Authors and Affiliations

  1. Helen Wills Neuroscience Institute, University of California, Berkeley, California, USA

    Tolga Çukur, Shinji Nishimoto, Alexander G Huth & Jack L Gallant

  2. Program in Bioengineering, University of California, Berkeley, California, USA

    Jack L Gallant

  3. Department of Psychology, University of California, Berkeley, California, USA

    Jack L Gallant

Authors
  1. Tolga Çukur
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  2. Shinji Nishimoto
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  4. Jack L Gallant
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Contributions

T.Ç. and S.N. designed the experiments. T.Ç. and A.G.H. operated the scanner. T.Ç. conducted the experiments and analyzed the data. T.Ç. and J.L.G. wrote the manuscript. J.L.G. provided guidance on all aspects of the project.

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Correspondence to Jack L Gallant.

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The authors declare no competing financial interests.

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Supplementary Figures 1–13 and Supplementary Tables 1 and 2 (PDF 23321 kb)

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Çukur, T., Nishimoto, S., Huth, A. et al. Attention during natural vision warps semantic representation across the human brain. Nat Neurosci 16, 763–770 (2013). https://doi.org/10.1038/nn.3381

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