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Orientation tuning of cytochrome oxidase patches in macaque primary visual cortex

Nature Neuroscience volume 14, pages 1574–1580 (2011)Cite this article

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Abstract

The abundant concentration of cytochrome oxidase in patches or blobs of primate striate cortex has never been explained. Patches are thought to contain unoriented, color-opponent neurons. Lacking orientation selectivity, these cells might endow patches with high metabolic activity because they respond to all contours in visual scenes. To test this idea, we measured orientation tuning in layer 2/3 of macaque cortical area V1 using acutely implanted 100-electrode arrays. Each electrode recording site was identified and assigned to the patch or interpatch compartment. The mean orientation bandwidth of cells was 28.4° in patches and 25.8° in interpatches. Neurons in patches were indeed less orientation selective, but the difference was subtle, indicating that the processing of form and color is not strictly segregated in V1. The most conspicuous finding was that patch cells had a 49% greater overall firing rate. This global difference in neuronal responsiveness, rather than an absence of orientation tuning, may account for the rich mitochondrial enzyme activity that defines patches.

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Figure 1: Recovery of microelectrode penetrations.
Figure 2: Identification of electrode tip laminar locations.
Figure 3: Orientation tuning in an interpatch (top row) and patch (bottom row).
Figure 4: Electrode array orientation tuning.
Figure 5: Orientation selectivity of patches versus interpatches.
Figure 6: Orientation selectivity versus cytochrome oxidase density.
Figure 7: Population mean tuning curves for patch versus interpatch neurons.

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References

  1. Heywood, C.A. & Kentridge, R.W. Achromatopsia, color vision, and cortex. Neurol. Clin. 21, 483–500 (2003).

    Article  Google Scholar 

  2. Horton, J.C. & Hubel, D.H. Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762–764 (1981).

    Article  CAS  Google Scholar 

  3. Wong-Riley, M. & Carroll, E.W. Effect of impulse blockage on cytochrome oxidase activity in monkey visual system. Nature 307, 262–264 (1984).

    Article  CAS  Google Scholar 

  4. 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 

  5. Martin, K.A.C. From enzymes to perception: a bridge too far? Trends Neurosci. 11, 380–387 (1988).

    Article  CAS  Google Scholar 

  6. Kelly, R.C. et al. Comparison of recordings from microelectrode arrays and single electrodes in the visual cortex. J. Neurosci. 27, 261–264 (2007).

    Article  CAS  Google Scholar 

  7. Smith, M.A. & Kohn, A. Spatial and temporal scales of neuronal correlation in primary visual cortex. J. Neurosci. 28, 12591–12603 (2008).

    Article  CAS  Google Scholar 

  8. Nauhaus, I., Benucci, A., Carandini, M. & Ringach, D.L. Neuronal selectivity and local map structure in visual cortex. Neuron 57, 673–679 (2008).

    Article  CAS  Google Scholar 

  9. Nordhausen, C.T., Maynard, E.M. & Normann, R.A. Single unit recording capabilities of a 100 microelectrode array. Brain Res. 726, 129–140 (1996).

    Article  CAS  Google Scholar 

  10. Henze, D.A. et al. Intracellular features predicted by extracellular recordings in the hippocampus in vivo. J. Neurophysiol. 84, 390–400 (2000).

    Article  CAS  Google Scholar 

  11. Kaufman, L. & Rousseeuw, P.J. Finding Groups In Data: An Introduction to Cluster Analysis (Wiley & Sons, New York, 1990).

  12. Ringach, D.L., Shapley, R.M. & Hawken, M.J. Orientation selectivity in macaque V1: diversity and laminar dependence. J. Neurosci. 22, 5639–5651 (2002).

    Article  CAS  Google Scholar 

  13. Swindale, N.V. Orientation tuning curves: empirical description and estimation of parameters. Biol. Cybern. 78, 45–56 (1998).

    Article  CAS  Google Scholar 

  14. Eliades, S.J. & Wang, X. Chronic multi-electrode neural recording in free-roaming monkeys. J. Neurosci. Methods 172, 201–214 (2008).

    Article  Google Scholar 

  15. Nordhausen, C.T., Rousche, P.J. & Normann, R.A. Optimizing recording capabilities of the Utah Intracortical Electrode Array. Brain Res. 637, 27–36 (1994).

    Article  CAS  Google Scholar 

  16. Kim, S.J., Manyam, S.C., Warren, D.J. & Normann, R.A. Electrophysiological mapping of cat primary auditory cortex with multielectrode arrays. Ann. Biomed. Eng. 34, 300–309 (2006).

    Article  Google Scholar 

  17. Purves, D. & LaMantia, A. Development of blobs in the visual cortex of macaques. J. Comp. Neurol. 334, 169–175 (1993).

    Article  CAS  Google Scholar 

  18. Farias, M.F., Gattass, R., Piñón, M.C. & Ungerleider, L.G. Tangential distribution of cytochrome oxidase-rich blobs in the primary visual cortex of macaque monkeys. J. Comp. Neurol. 386, 217–228 (1997).

    Article  CAS  Google Scholar 

  19. 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 

  20. Lennie, P., Krauskopf, J. & Sclar, G. Chromatic mechanisms in striate cortex of macaque. J. Neurosci. 10, 649–669 (1990).

    Article  CAS  Google Scholar 

  21. O'Keefe, L.P., Levitt, J.B., Kiper, D.C., Shapley, R.M. & Movshon, J.A. Functional organization of owl monkey lateral geniculate nucleus and visual cortex. J. Neurophysiol. 80, 594–609 (1998).

    Article  CAS  Google Scholar 

  22. Friedman, H.S., Zhou, H. & von der Heydt, R. The coding of uniform colour figures in monkey visual cortex. J. Physiol. (Lond.) 548, 593–613 (2003).

    Article  CAS  Google Scholar 

  23. Schiller, P.H., Finlay, B.L. & Volman, S.F. Quantitative studies of single-cell properties in monkey striate cortex. II. Orientation specificity and ocular dominance. J. Neurophysiol. 39, 1320–1333 (1976).

    Article  CAS  Google Scholar 

  24. Nauhaus, I. & Ringach, D.L. Precise alignment of micromachined electrode arrays with V1 functional maps. J. Neurophysiol. 97, 3781–3789 (2007).

    Article  Google Scholar 

  25. Blasdel, G.G. & Salama, G. Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321, 579–585 (1986).

    Article  CAS  Google Scholar 

  26. 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 

  27. Polimeni, J.R., Granquist-Fraser, D., Wood, R.J. & Schwartz, E.L. Physical limits to spatial resolution of optical recording: clarifying the spatial structure of cortical hypercolumns. Proc. Natl. Acad. Sci. USA 102, 4158–4163 (2005).

    Article  CAS  Google Scholar 

  28. Blasdel, G.G. Orientation selectivity, preference, and continuity in monkey striate cortex. J. Neurosci. 12, 3139–3161 (1992).

    Article  CAS  Google Scholar 

  29. Bartfeld, E. & Grinvald, A. 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).

    Article  CAS  Google Scholar 

  30. Landisman, C.E. & Ts'o, D.Y. Color processing in macaque striate cortex: electrophysiological properties. J. Neurophysiol. 87, 3138–3151 (2002).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  32. Sincich, L.C. & Horton, J.C. Divided by cytochrome oxidase: a map of the projections from V1 to V2 in macaques. Science 295, 1734–1737 (2002).

    Article  CAS  Google Scholar 

  33. Sincich, L.C. & Horton, J.C. Input to V2 thin stripes arises from V1 cytochrome oxidase patches. J. Neurosci. 25, 10087–10093 (2005).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  35. Landisman, C.E. & Ts'o, D.Y. Color processing in macaque striate cortex: relationships to ocular dominance, cytochrome oxidase, and orientation. J. Neurophysiol. 87, 3126–3137 (2002).

    Article  CAS  Google Scholar 

  36. 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 

  37. Chatterjee, S. & Callaway, E.M. Parallel colour-opponent pathways to primary visual cortex. Nature 426, 668–671 (2003).

    Article  CAS  Google Scholar 

  38. 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 

  39. Johnson, E.N., Hawken, M.J. & Shapley, R. The spatial transformation of color in the primary visual cortex of the macaque monkey. Nat. Neurosci. 4, 409–416 (2001).

    Article  CAS  Google Scholar 

  40. Yoshioka, T. & Dow, B.M. Color, orientation and cytochrome oxidase reactivity in areas V1, V2 and V4 of macaque monkey visual cortex. Behav. Brain Res. 76, 71–88 (1996).

    Article  CAS  Google Scholar 

  41. Horwitz, G.D., Chichilnisky, E.J. & Albright, T.D. Cone inputs to simple and complex cells in V1 of awake macaque. J. Neurophysiol. 97, 3070–3081 (2007).

    Article  Google Scholar 

  42. Johnson, E.N., Hawken, M.J. & Shapley, R. The orientation selectivity of color-responsive neurons in macaque V1. J. Neurosci. 28, 8096–8106 (2008).

    Article  CAS  Google Scholar 

  43. Sumner, P., Anderson, E.J., Sylvester, R., Haynes, J.D. & Rees, G. Combined orientation and colour information in human V1 for both L-M and S-cone chromatic axes. Neuroimage 39, 814–824 (2008).

    Article  Google Scholar 

  44. Engel, S.A. Adaptation of oriented and unoriented color-selective neurons in human visual areas. Neuron 45, 613–623 (2005).

    Article  CAS  Google Scholar 

  45. McDonald, J.S., Mannion, D.J., Goddard, E. & Clifford, C.W. Orientation-selective chromatic mechanisms in human visual cortex. J. Vis. 10, 34 (2010).

    Article  Google Scholar 

  46. Seymour, K., Clifford, C.W., Logothetis, N.K. & Bartels, A. Coding and binding of color and form in visual cortex. Cereb. Cortex 20, 1946–1954 (2010).

    Article  Google Scholar 

  47. DeYoe, E.A., Trusk, T.C. & Wong-Riley, M.T. Activity correlates of cytochrome oxidase-defined compartments in granular and supragranular layers of primary visual cortex of the macaque monkey. Vis. Neurosci. 12, 629–639 (1995).

    Article  CAS  Google Scholar 

  48. Kennedy, C., Des Rosiers, M.H. & Sakurada, O. Metabolic mapping of the primary visual system of the monkey by means of the autoradiographic 14[C] deoxyglucose technique. Proc. Natl. Acad. Sci. USA 73, 4230–4234 (1976).

    Article  CAS  Google Scholar 

  49. Tootell, R.B., Hamilton, S.L., Silverman, M.S. & Switkes, E. Functional anatomy of macaque striate cortex. I. Ocular dominance, binocular interactions, and baseline conditions. J. Neurosci. 8, 1500–1530 (1988).

    Article  CAS  Google Scholar 

  50. Horton, J.C. Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex. Phil. Trans. R. Soc. Lond. B 304, 199–253 (1984).

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by grants EY10217, EY10217-16A1S1 (J.C.H.), EY13676 (L.C.S.) and EY02162 (Beckman Vision Center) from the US National Eye Institute and by Research to Prevent Blindness. The California Regional Primate Research Center is supported by US National Institutes of Health Base Grant RR00169. C.M. Jocson provided technical assistance and M.K. Feusner assisted with computer programming.

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Author notes

  1. John R Economides and Lawrence C Sincich: These authors contributed equally to this work.

Authors and Affiliations

  1. Beckman Vision Center, University of California, San Francisco, San Francisco, California, USA.,

    John R Economides, Daniel L Adams & Jonathan C Horton

  2. Department of Visual Sciences, University of Alabama at Birmingham, Birmingham, Alabama, USA

    Lawrence C Sincich

  3. Center for Mind/Brain Sciences, University of Trento, Rovereto, Italy

    Daniel L Adams

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  1. John R Economides
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All authors participated in the physiological recording experiments, data analysis, and preparation of this paper.

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Correspondence to Jonathan C Horton.

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Economides, J., Sincich, L., Adams, D. et al. Orientation tuning of cytochrome oxidase patches in macaque primary visual cortex. Nat Neurosci 14, 1574–1580 (2011). https://doi.org/10.1038/nn.2958

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