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.

  • Letter
  • Published:

Colour tuning in human visual cortex measured with functional magnetic resonance imaging

Abstract

The primate retina contains three classes of cones, the L, M and S cones, which respond preferentially to long-, middle- and short-wavelength visible light, respectively. Colour appearance results from neural processing of these cone signals within the retina and the brain. Perceptual experiments have identified three types of neural pathways that represent colour: a red–green pathway that signals differences between L- and M-cone responses; a blue–yellow pathway that signals differences between S-cone responses and a sum of L- and M-cone responses; and a luminance pathway that signals a sum of L- and M-cone responses1,2,3. It might be expected that there are neurons in the primary visual cortex with response properties that resemble these three perceptual pathways, but attempts to find them have led to inconsistent results4,5,6,7. We have therefore used functional magnetic resonance imaging (fMRI) to examine responses in the human brain to a large number of colours. In visual cortical areas V1 and V2, the strongest response is to red–green stimuli, and much of this activity is from neurons receiving opposing inputs from L and M cones. A strong response is also seen with blue–yellow stimuli, and this response declines rapidly as the temporal frequency of the stimulus is increased. These responses resemble psychophysical measurements, suggesting that colour signals relevant for perception are encoded in a large population of neurons in areas V1 and V2.

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: Experimental protocol.
Figure 2: Colour tuning in a red–green plane measured in human cortical area V1.
Figure 3: Colour tuning in a blue–yellow plane measured in human cortical area V2.
Figure 4: Psychophysical detection contours of the stimuli used in the fMRI experiments for observer B.W.

Similar content being viewed by others

References

  1. Hurvich, L. & Jameson, D. An opponent-process theory of color vision. Psychol. Rev. 64, 384–404 (1957).

    Article  Google Scholar 

  2. Boynton, R. et al. Interactions among chromatic mechanisms as inferred from positive and negative increment thresholds. Vis. Res. 4, 87–117 (1964).

    Article  CAS  Google Scholar 

  3. Thornton, J. & Pugh, E. Red/green color opponency at detection threshold. Science 219, 191–183 (1983).

    Article  ADS  CAS  Google Scholar 

  4. Thorell, L. et al. Spatial mapping of monkey V1 cells with pure color and luminance stimuli. Vis. Res. 24, 751–769 (1984).

    Article  CAS  Google Scholar 

  5. Livingstone, M. & Hubel, D. Anatomy and physiology of a colour system in the primate visual cortex. J. Neurosci. 4, 2830–2835 (1984).

    Article  CAS  Google Scholar 

  6. Vautin, R. & Dow, B. Color cell groups in foveal striate cortex of the behaving macaque. J. Neurophysiol. 54, 273–292 (1985).

    Article  CAS  Google Scholar 

  7. Lennie, P. et al. Chromatic mechanisms in striate cortex of macaque. J. Neurosci. 10, 649–669 (1990).

    Article  CAS  Google Scholar 

  8. DeValois, R. L. Analysis and coding of color vision in the primate visual system. Cold Spring Harb. Symp. Quant. Biol. 30, 567–579 (1965).

    Article  CAS  Google Scholar 

  9. Wiesel, T. & Hubel, D. S. Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. J. Neurophysiol. 29, 1115–1156 (1966).

    Article  CAS  Google Scholar 

  10. Derrington, A. et al. Chromatic mechanisms in lateral geniculate nucleus of macaque. J. Physiol. (Lond.) 357, 241–265 (1984).

    Article  CAS  Google Scholar 

  11. Mullen, K. The contrast sensitivity of human colour vision to red–green and blue–yellow chromatic gratings. J. Physiol. (Lond.) 359, 381–400 (1985).

    Article  ADS  CAS  Google Scholar 

  12. Poirson, A. & Wandell, B. Appearance of colored patterns: Pattern-color separability. J. Opt. Soc. Am. 12, 2458–2471 (1993).

    Article  Google Scholar 

  13. Ts'o, C. & Gilbert, C. The organization of chromatic and spatial interactions in the primate striate cortex. J. Neurosci. 8, 1712–1727 (1988).

    Article  CAS  Google Scholar 

  14. Wandell, B. Color measurement and discrimination. J. Opt. Soc. Am. A 2, 62–71 (1985).

    Article  ADS  CAS  Google Scholar 

  15. Cole, G. et al. Detection of mechanisms in L-, M-, and S-cone contrast space. J. Opt. Soc. Am. A 10, 38–51 (1993).

    Article  ADS  CAS  Google Scholar 

  16. Curcio, C. A. et al. Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. J. Comp. Neurol. 312, 610–624 (1991).

    Article  CAS  Google Scholar 

  17. Dacey, D. M. & Lee, B. B. The ‘blue-on’ opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367, 731–735 (1994).

    Article  ADS  CAS  Google Scholar 

  18. Kelly, D. Theory of flicker and transient responses: I. Uniform fields. J. Opt. Soc. Am. 61, 537–546 (1971).

    Article  ADS  CAS  Google Scholar 

  19. Stockman, A. The temporal properties of the human short-wave photoreceptors and their associated pathways. Vis. Res. 31, 189–208 (1991).

    Article  CAS  Google Scholar 

  20. Cottaris, N. P. et al. Spatio-temporal luminance and chromatic receptive field profiles of macaque striate cortex simple cells. Soc. Neurosci. Abstr. 22, 951 (1996).

    Google Scholar 

  21. Gur, M. & Snodderly, D. M. Adissociation between brain activity and perception: Chromatically opponent cortical neurons signal chromatic flicker that is not perceived. Vis. Res. 37, 377–382 (1997).

    Article  CAS  Google Scholar 

  22. Regan, D. Evoked potentials specific to spatial patterns of luminance and colour. Vis. Res. 13, 2381–2402 (1973).

    Article  CAS  Google Scholar 

  23. Rabin, J. et al. Visual evoked potentials in three-dimensional color space: Correlates of spatio-chromatic processing. Vis. Res. 34, 2657–2671 (1994).

    Article  CAS  Google Scholar 

  24. Kleinschmidt, A. et al. Functional mapping of color processing by magnetic resonance imaging of responses to selective P- and M-pathway stimulation. Exp. Brain Res. 110, 279–288 (1996).

    Article  CAS  Google Scholar 

  25. Rodieck, R. W. in From Pigments to Perception(eds Valberg, A. & Lee, B. B.) 83–93 (Plenum, New York, (1991)).

    Book  Google Scholar 

  26. Calkins, D. J. & Sterling, P. Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina. Nature 381, 613–615 (1996).

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  29. DeYoe, E. et al. Mapping striate and extrastriate visual areas in human cerebral cortex. Proc. Natl Acad. Sci. USA 93, 2382–2386 (1996).

    Article  ADS  CAS  Google Scholar 

  30. Engel, S. A. et al. Retinotropic organization in human visual cortex and the spatial precision of functional MRI. Cereb. Cort. 7, 181–192 (1997).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank G. Glover for technical help, and H. Baseler, G. Boynton, E. J. Chichilnisky, E. Markman, W. Newsome, A. Poirson and J. Wine for comments on the manuscript. This work was funded by the National Eye Institute and the McDonnel-Pew Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephen Engel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Engel, S., Zhang, X. & Wandell, B. Colour tuning in human visual cortex measured with functional magnetic resonance imaging. Nature 388, 68–71 (1997). https://doi.org/10.1038/40398

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/40398

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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