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Predicting the orientation of invisible stimuli from activity in human primary visual cortex

Nature Neuroscience volume 8, pages 686691 (2005) | Download Citation

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Abstract

Humans can experience aftereffects from oriented stimuli that are not consciously perceived, suggesting that such stimuli receive cortical processing. Determining the physiological substrate of such effects has proven elusive owing to the low spatial resolution of conventional human neuroimaging techniques compared to the size of orientation columns in visual cortex. Here we show that even at conventional resolutions it is possible to use fMRI to obtain a direct measure of orientation-selective processing in V1. We found that many parts of V1 show subtle but reproducible biases to oriented stimuli, and that we could accumulate this information across the whole of V1 using multivariate pattern recognition. Using this information, we could then successfully predict which one of two oriented stimuli a participant was viewing, even when masking rendered that stimulus invisible. Our findings show that conventional fMRI can be used to reveal feature-selective processing in human cortex, even for invisible stimuli.

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References

  1. 1.

    , & Attentional resolution and the locus of visual awareness. Nature 383, 334–337 (1996).

  2. 2.

    & Orientation-selective adaptation and tilt after-effect from invisible patterns. Nature 411, 473–476 (2001).

  3. 3.

    Unconscious orientation processing. Neuron 41, 663–673 (2004).

  4. 4.

    & Relationships between orientation-preference pinwheels, cytochrome oxidase blobs, and ocular-dominance columns in primate striate cortex. Proc. Natl. Acad. Sci. USA 89, 11905–11909 (1992).

  5. 5.

    & Geometry of orientation and ocular dominance columns in monkey striate cortex. J. Neurosci. 13, 4114–4129 (1993).

  6. 6.

    et al. Functional analysis of primary visual cortex (V1) in humans. Proc. Natl. Acad. Sci. USA 95, 811–817 (1998).

  7. 7.

    & Orientation-specific adaptation in human visual cortex. J. Neurosci. 23, 8781–8787 (2003).

  8. 8.

    , & Pattern Classification (Wiley, New York, 2001).

  9. 9.

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

  10. 10.

    & Functional magnetic resonance imaging (fMRI) 'brain reading': detecting and classifying distributed patterns of fMRI activity in human visual cortex. Neuroimage 19, 261–270 (2003).

  11. 11.

    , & Patterns of activity in the categorical representation of objects. J. Cogn. Neurosci. 15, 704–717 (2003).

  12. 12.

    et al. Inferring behavior from functional brain images. Nat. Neurosci. 1, 549–550 (1998).

  13. 13.

    & Neuronal correlates of visibility and invisibility in the primate visual system. Nat. Neurosci. 1, 144–149 (1998).

  14. 14.

    & An oblique effect in human primary visual cortex. Nat. Neurosci. 3, 535–536 (2000).

  15. 15.

    The distribution of preferred orientations in the peripheral visual field. Vision Res. 43, 53–57 (2003).

  16. 16.

    et al. An fMRI study of the selective activation of human extrastriate form vision areas by radial and concentric gratings. Curr. Biol. 10, 1455–1458 (2000).

  17. 17.

    & Are we aware of neural activity in primary visual cortex? Nature 375, 121–123 (1995).

  18. 18.

    Primary visual cortex and visual awareness. Nat. Rev. Neurosci. 4, 219–229 (2003).

  19. 19.

    & Neuronal correlates of perception in early visual cortex. Nat. Neurosci. 6, 414–420 (2003).

  20. 20.

    , , & Neuronal activity in human primary visual cortex correlates with perception during binocular rivalry. Nat. Neurosci. 3, 1153–1159 (2000).

  21. 21.

    & Interocular rivalry revealed in the human cortical blind-spot representation. Nature 411, 195–199 (2001).

  22. 22.

    , & Two distinct modes of sensory processing observed in monkey primary visual cortex (V1). Nat. Neurosci. 4, 304–310 (2001).

  23. 23.

    & A dissociation between brain activity and perception: chromatically opponent cortical neurons signal chromatic flicker that is not perceived. Vision Res. 37, 377–382 (1997).

  24. 24.

    & Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry. Nature 379, 549–553 (1996).

  25. 25.

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

  26. 26.

    et al. Unconscious activation of visual cortex in the damaged right hemisphere of a parietal patient with extinction. Brain 123, 1624–1633 (2000).

  27. 27.

    et al. Neural fate of seen and unseen faces in visuospatial neglect: a combined event-related functional MRI and event-related potential study. Proc. Natl. Acad. Sci. USA 98, 3495–3500 (2001).

  28. 28.

    et al. Imaging unconscious semantic priming. Nature 395, 597–600 (1998).

  29. 29.

    , & Word meanings can be accessed but not reported during the attentional blink. Nature 383, 616–618 (1996).

  30. 30.

    & Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys. J. Comp. Neurol. 201, 81–97 (1981).

  31. 31.

    , , , & Sustained extrastriate cortical activation without visual awareness revealed by fMRI studies of hemianopic patients. Vision Res. 41, 1459–1474 (2001).

  32. 32.

    , & Imaging implicit perception: promise and pitfalls. Nat. Rev. Neurosci. 6, 247–255 (2005).

  33. 33.

    et al. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 2, 189–210 (1995).

  34. 34.

    et al. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268, 889–893 (1995).

  35. 35.

    , & Creating connected representations of cortical gray matter for functional MRI visualization. IEEE Trans. Med. Imaging 16, 852–863 (1997).

  36. 36.

    , & Visualization and measurement of the cortical surface. J. Cogn. Neurosci. 12, 739–752 (2000).

  37. 37.

    & Applied Multivariate Data Analysis (Edward Arnold, London, 1991).

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Acknowledgements

We thank K. Friston and J. Driver for comments on the manuscript. The Wellcome Trust funded this work.

Author information

Affiliations

  1. Wellcome Department of Imaging Neuroscience, Institute of Neurology, University College London, 12 Queen Square, London WC1N 3BG, UK.

    • John-Dylan Haynes
    •  & Geraint Rees
  2. Institute of Cognitive Neuroscience, University College London, Alexandra House, 17 Queen Square, London WC1N 3AR, UK.

    • John-Dylan Haynes
    •  & Geraint Rees

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Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to John-Dylan Haynes.

Supplementary information

PDF files

  1. 1.

    Supplementary Fig. 1

    Simulation of expected orientation bias.

  2. 2.

    Supplementary Fig. 2

    Spatial distribution of orientation biases of voxels entering into the discriminant analysis.

  3. 3.

    Supplementary Fig. 4

    Details of pattern classification for experiment 1.

  4. 4.

    Supplementary Fig. 5

    Comparison of prediction using conventional and pattern signals.

Image files

  1. 1.

    Supplementary Fig. 3

    Analysis of radial and tangential contributions to orientation bias in V1.

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DOI

https://doi.org/10.1038/nn1445

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