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Functional organization for color and orientation in macaque V4

Nature Neuroscience volume 13, pages 1542–1548 (2010)Cite this article

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Abstract

Visual area V4 in the macaque monkey is a cortical area that is strongly involved in color and shape perception. However, fundamental questions about V4 are still debated. V4 was initially characterized as a color-processing area, but subsequent studies revealed that it contains a diverse complement of cells, including those with preference for color, orientation, disparity and higher-order feature preferences. This has led to disputes and uncertainty about the role of V4 in vision. Using intrinsic signal optical imaging methods in awake, behaving monkeys, we found that different feature preferences are functionally organized in V4. Optical images revealed that regions with preferential response to color were largely separate from orientation-selective regions. Our results help to resolve long-standing controversies regarding functional diversity and retinotopy in V4 and indicate the presence of spatially biased distribution of featural representation in V4 in the ventral visual pathway.

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Figure 1: Examples of time course of stimulus-evoked reflectance change in V4.
Figure 2: Functional maps of color and orientation sensitivity in foveal V4.
Figure 3: Functional maps of color and orientation sensitivity in parafoveal V4.
Figure 4: Overall spatial pattern of modulation by the stimulus at different locations in the visual field.
Figure 5: Functional maps of orientation preference in V4.
Figure 6: Functional map of hue preference in V4.
Figure 7: Luminance invariance in responses of hue-preferring region.

References

  1. Livingstone, M.S. & Hubel, D.H. Anatomy and physiology of a color system in the primate visual cortex. J. Neurosci. 4, 309–356 (1984).

    Article  CAS  Google Scholar 

  2. Hubel, D.H. & Livingstone, M.S. Segregation of form, color, and stereopsis in primate area 18. J. Neurosci. 7, 3378–3415 (1987).

    Article  CAS  Google Scholar 

  3. Leventhal, A.G., Thompson, K.G., Liu, D., Zhou, Y. & Ault, S.J. Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex. J. Neurosci. 15, 1808–1818 (1995).

    Article  CAS  Google Scholar 

  4. Levitt, J.B., Kiper, D.C. & Movshon, J.A. Receptive field and functional architecture of macaque V2. J. Neurophysiol. 71, 2517–2542 (1994).

    Article  CAS  Google Scholar 

  5. Sincich, L.C. & Horton, J.C. The circuitry of V1 and V2: integration of color, form, and motion. Annu. Rev. Neurosci. 28, 303–326 (2005).

    Article  CAS  Google Scholar 

  6. Zeki, S.M. Colour coding in rhesus monkey prestriate cortex. Brain Res. 53, 422–427 (1973).

    Article  CAS  Google Scholar 

  7. Krüger, J. & Gouras, P. Spectral selectivity of cells and its dependence on slit length in monkey visual cortex. J. Neurophysiol. 43, 1055–1069 (1980).

    Article  Google Scholar 

  8. Schein, S.J., Marrocco, R.T. & de Monasterio, F.M. Is there a high concentration of color-selective cells in area V4 of monkey visual cortex? J. Neurophysiol. 47, 193–213 (1982).

    Article  CAS  Google Scholar 

  9. Tanaka, M., Weber, H. & Creutzfeldt, O.D. Visual properties and spatial distribution of neurones in the visual association area on the prelunate gyrus of the awake monkey. Exp. Brain Res. 65, 11–37 (1986).

    Article  CAS  Google Scholar 

  10. Ghose, G.M. & Ts'o, D.Y. Form processing modules in primate area V4. J. Neurophysiol. 77, 2191–2196 (1997).

    Article  CAS  Google Scholar 

  11. Maunsell, J.H. & Treue, S. Feature-based attention in visual cortex. Trends Neurosci. 29, 317–322 (2006).

    Article  CAS  Google Scholar 

  12. Xiao, Y., Wang, Y. & Felleman, D.J. A spatially organized representation of colour in macaque cortical area V2. Nature 421, 535–539 (2003).

    Article  CAS  Google Scholar 

  13. Vanzetta, I., Slovin, H., Omer, D.B. & Grinvald, A. Columnar resolution of blood volume and oximetry functional maps in the behaving monkey; implications for fMRI. Neuron 42, 843–854 (2004).

    Article  CAS  Google Scholar 

  14. Lu, H.D. & Roe, A.W. Functional organization of color domains in V1 and V2 of macaque monkey revealed by optical imaging. Cereb. Cortex 18, 516–533 (2008).

    Article  Google Scholar 

  15. Gattass, R., Sousa, A.P. & Gross, C.G. Visuotopic organization and extent of V3 and V4 of the macaque. J. Neurosci. 8, 1831–1845 (1988).

    Article  CAS  Google Scholar 

  16. Roe, A.W. & Ts'o, D.Y. Visual topography in primate V2: multiple representation across functional stripes. J. Neurosci. 15, 3689–3715 (1995).

    Article  CAS  Google Scholar 

  17. Hubel, D.H. & Wiesel, T.N. Sequence regularity and geometry of orientation columns in the monkey striate cortex. J. Comp. Neurol. 158, 267–293 (1974).

    Article  CAS  Google Scholar 

  18. Bonhoeffer, T. & Grinvald, A. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature 353, 429–431 (1991).

    Article  CAS  Google Scholar 

  19. Xiao, Y., Casti, A., Xiao, J. & Kaplan, E. Hue maps in primate striate cortex. Neuroimage 35, 771–786 (2007).

    Article  Google Scholar 

  20. Kotake, Y., Morimoto, H., Okazaki, Y., Fujita, I. & Tamura, H. Organization of color-selective neurons in macaque visual area V4. J. Neurophysiol. 102, 15–27 (2009).

    Article  Google Scholar 

  21. Wang, Y., Xiao, Y. & Felleman, D.J. V2 thin stripes contain spatially organized representations of achromatic luminance change. Cereb. Cortex 17, 116–129 (2007).

    Article  Google Scholar 

  22. Dobkins, K.R., Thiele, A. & Albright, T.D. Comparison of red-green equiluminance points in humans and macaques: evidence for different L:M cone ratios between species. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 17, 545–556 (2000).

    Article  CAS  Google Scholar 

  23. Livingstone, M. & Hubel, D. Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240, 740–749 (1988).

    Article  CAS  Google Scholar 

  24. Gallant, J.L., Braun, J. & Van Essen, D.C. Selectivity for polar, hyperbolic and Cartesian gratings in macaque visual cortex. Science 259, 100–103 (1993).

    Article  CAS  Google Scholar 

  25. Pasupathy, A. & Connor, C.E. Responses to contour features in macaque area V4. J. Neurophysiol. 82, 2490–2502 (1999).

    Article  CAS  Google Scholar 

  26. Kobatake, E. & Tanaka, K. Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. J. Neurophysiol. 71, 856–867 (1994).

    Article  CAS  Google Scholar 

  27. Zeki, S. The distribution of wavelength and orientation selective cells in different areas of monkey visual cortex. Proc. R. Soc. Lond. B Biol. Sci. 217, 449–470 (1983).

    Article  CAS  Google Scholar 

  28. Conway, B.R., Moeller, S. & Tsao, D.Y. Specialized color modules in macaque extrastriate cortex. Neuron 56, 560–573 (2007).

    Article  CAS  Google Scholar 

  29. Zeki, S.M. Cortical projections from two prestriate areas in the monkey. Brain Res. 34, 19–35 (1971).

    Article  CAS  Google Scholar 

  30. Stepniewska, I., Collins, C.E. & Kaas, J.H. Reappraisal of DL/V4 boundaries based on connectivity patterns of dorsolateral visual cortex in macaques. Cereb. Cortex 15, 809–822 (2005).

    Article  Google Scholar 

  31. Xiao, Y., Zych, A. & Felleman, D.J. Segregation and convergence of functionally defined V2 thin stripe and interstripe compartment projections to area V4 of macaques. Cereb. Cortex 9, 792–804 (1999).

    Article  CAS  Google Scholar 

  32. Xu, X. et al. Functional organization of visual cortex in the owl monkey. J. Neurosci. 24, 6237–6247 (2004).

    Article  CAS  Google Scholar 

  33. Van Essen, D.C. & Zeki, S.M. The topographic organization of rhesus monkey prestriate cortex. J. Physiol. (Lond.) 277, 193–226 (1978).

    Article  Google Scholar 

  34. Maguire, W.M. & Baizer, J.S. Visuotopic organization of the prelunate gyrus in rhesus monkey. J. Neurosci. 4, 1690–1704 (1984).

    Article  CAS  Google Scholar 

  35. Fize, D. et al. The retinotopic organization of primate dorsal V4 and surrounding areas: a functional magnetic resonance imaging study in awake monkeys. J. Neurosci. 23, 7395–7406 (2003).

    Article  CAS  Google Scholar 

  36. Hubel, D.H. & Wiesel, T.N. Functional architecture of macaque monkey visual cortex. Proc. R. Soc. Lond. B Biol. Sci. 198, 1–59 (1977).

    Article  CAS  Google Scholar 

  37. Vanduffel, W., Tootell, R.B., Schoups, A.A. & Orban, G.A. The organization of orientation selectivity throughout macaque visual cortex. Cereb. Cortex 12, 647–662 (2002).

    Article  Google Scholar 

  38. Tootell, R.B., Nelissen, K., Vanduffel, W. & Orban, G.A. Search for color 'center(s)' in macaque visual cortex. Cereb. Cortex 14, 353–363 (2004).

    Article  Google Scholar 

  39. Desimone, R. & Schein, S.J. Visual properties of neurons in area V4 of the macaque: sensitivity to stimulus form. J. Neurophysiol. 57, 835–868 (1987).

    Article  CAS  Google Scholar 

  40. Harada, T. et al. Distribution of colour-selective activity in the monkey inferior temporal cortex revealed by functional magnetic resonance imaging. Eur. J. Neurosci. 30, 1960–1970 (2009).

    Article  Google Scholar 

  41. Moore, T. & Armstrong, K.M. Selective gating of visual signals by microstimulation of frontal cortex. Nature 421, 370–373 (2003).

    Article  CAS  Google Scholar 

  42. Hayden, B.Y. & Gallant, J.L. Time course of attention reveals different mechanisms for spatial and feature-based attention in area V4. Neuron 47, 637–643 (2005).

    Article  CAS  Google Scholar 

  43. Koida, K. & Komatsu, H. Effects of task demands on the responses of color-selective neurons in the inferior temporal cortex. Nat. Neurosci. 10, 108–116 (2007).

    Article  CAS  Google Scholar 

  44. Chen, L.M. et al. A chamber and artificial dura method for long-term optical imaging in the monkey. J. Neurosci. Methods 113, 41–49 (2002).

    Article  Google Scholar 

  45. Huettel, S.A., Song, A.W. & McCarthy, G. Functional Magnetic Resonance Imaging (Sinauer Associates, Sunderland, Massachusetts, 2004).

  46. Bonhoeffer, T. & Grinvald, A. Optical imaging based on intrinsic signals: the methodology. in Brain Mapping: the Methods (eds. Toga, A.W. & Mazziotta, J.C.) 55–97 (Academic Press, New York, 1996).

  47. Zhan, C.A. & Baker, C.L. Jr. Boundary cue invariance in cortical orientation maps. Cereb. Cortex 16, 896–906 (2006).

    Article  Google Scholar 

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Acknowledgements

We thank J.H. Kaas and G. Chen for comments on the manuscript and Y. Chu for technical assistance. This work was supported by grants from the US National Institutes of Health, Vanderbilt Vision Research Center and Vanderbilt University Center for Integrative & Cognitive Neuroscience to A.W.R.

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  1. Haidong D Lu

    Present address: Present address: Institute of Neuroscience, Chinese Academy of Sciences, Shanghai, China.,

Authors and Affiliations

  1. Department of Psychology, Vanderbilt University, Nashville, Tennessee, USA

    Hisashi Tanigawa, Haidong D Lu & Anna W Roe

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  1. Hisashi Tanigawa
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Contributions

H.T. and A.W.R. designed the experiments. H.T. performed the experiments and analyzed the data. H.L. assisted H.T. with experimental procedures. H.T. and A.W.R. discussed the results and wrote the paper.

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Correspondence to Anna W Roe.

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Supplementary Figures 1–7, Supplementary Table 1 and Supplementary Note (PDF 2518 kb)

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Tanigawa, H., Lu, H. & Roe, A. Functional organization for color and orientation in macaque V4. Nat Neurosci 13, 1542–1548 (2010). https://doi.org/10.1038/nn.2676

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