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.

Orthogonal micro-organization of orientation and spatial frequency in primate primary visual cortex

An Erratum to this article was published on 22 November 2013

A Corrigendum to this article was published on 22 November 2013

An Erratum to this article was published on 22 November 2013

This article has been updated

Abstract

Orientation and spatial frequency tuning are highly salient properties of neurons in primary visual cortex (V1). The combined organization of these particular tuning properties in the cortical space will strongly shape the V1 population response to different visual inputs, yet it is poorly understood. In this study, we used two-photon imaging in macaque monkey V1 to demonstrate the three-dimensional cell-by-cell layout of both spatial frequency and orientation tuning. We first found that spatial frequency tuning was organized into highly structured maps that remained consistent across the depth of layer II/III, similarly to orientation tuning. Next, we found that orientation and spatial frequency maps were intimately related at the fine spatial scale observed with two-photon imaging. Not only did the map gradients tend notably toward orthogonality, but they also co-varied negatively from cell to cell at the spatial scale of cortical columns.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Two experimental two-photon imaging procedures.
Figure 2: Large-scale imaging of orientation and spatial frequency maps at different depths of layer II/III for two cortical locations.
Figure 3: Micro-maps of orientation and spatial frequency for three example regions (one per row), each 150 μm deep.
Figure 4: Bootstrap analysis to examine clustering of micro-maps.
Figure 5: Relationship between orientation and spatial frequency maps.
Figure 6: Measuring the angle of intersection between micro-maps of orientation and spatial frequency.
Figure 7: Measuring orthogonality based on tuning curves of single neurons.

Change history

  • 03 December 2012

    In the version of this article initially published, the scale bar length for Figure 1e was misstated as 500 μm. The correct length is 50 μm. The error has been corrected in the HTML and PDF versions of the article.

  • 09 January 2013

    In the version of this article initially published, the computation performed to yield the values on the x axis of Figure 6c was incorrectly defined in the text and on the axis label as the absolute difference between Aθ and Aϕ (mod 90°). The correct computation is 90° − || Aθ − Aϕ | − 90°|, which yields values near 0° for parallel gradients and values near 90° for perpendicular gradients. The error has been corrected in the HTML and PDF versions of the article.

  • 11 January 2013

    In the version of this article initially published, in the equation for Aθ on p. 5, the subscript to the variable f was given as an e. The correct character is θ. The error has been corrected in the HTML and PDF versions of the article.

References

  1. Hubel, D.H. & Wiesel, T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 (1962).

    Article  CAS  Google Scholar 

  2. Hubel, D.H. & Wiesel, T.N. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. (Lond.) 195, 215–243 (1968).

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  4. Ts'o, D.Y., Frostig, R., Lieke, E. & Grinvald, A. Functional organization of primate visual cortex revealed by high resolution optical imaging. Science 249, 417–420 (1990).

    Article  CAS  PubMed  Google Scholar 

  5. Horton, J.C. & Adams, D.L. The cortical column: a structure without a function. Phil. Trans. R. Soc. Lond. B 360, 837–862 (2005).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 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  PubMed  PubMed Central  Google Scholar 

  9. Crair, M.C., Ruthazer, E.S., Gillespie, D.C. & Stryker, M.P. Ocular dominance peaks at pinwheel center singularities of the orientation map in cat visual cortex. J. Neurophysiol. 77, 3381–3385 (1997).

    Article  CAS  PubMed  Google Scholar 

  10. Blasdel, G. & Campbell, D. Functional retinotopy of monkey visual cortex. J. Neurosci. 21, 8286–8301 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Hübener, M., Shoham, D., Grinvald, A. & Bonhoeffer, T. Spatial relationships among three columnar systems in cat area 17. J. Neurosci. 17, 9270–9284 (1997).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Issa, N.P., Trepel, C. & Stryker, M.P. Spatial frequency maps in cat visual cortex. J. Neurosci. 20, 8504–8514 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Yu, H., Farley, B.J., Jin, D.Z. & Sur, M. The coordinated mapping of visual space and response features in visual cortex. Neuron 47, 267–280 (2005).

    Article  CAS  PubMed  Google Scholar 

  14. Sirovich, L. & Uglesich, R. The organization of orientation and spatial frequency in primary visual cortex. Proc. Natl. Acad. Sci. USA 101, 16941–16946 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kim, D.S., Matsuda, Y., Ohki, K., Ajima, A. & Tanaka, S. Geometrical and topological relationships between multiple functional maps in cat primary visual cortex. Neuroreport 10, 2515–2522 (1999).

    Article  CAS  PubMed  Google Scholar 

  16. Edwards, D.P., Purpura, K.P. & Kaplan, E. Contrast sensitivity and spatial frequency response of primate cortical neurons in and around the cytochrome oxidase blobs. Vision Res. 35, 1501–1523 (1995).

    Article  CAS  PubMed  Google Scholar 

  17. Born, R.T. & Tootell, R.B. Spatial frequency tuning of single units in macaque supragranular striate cortex. Proc. Natl. Acad. Sci. USA 88, 7066–7070 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Silverman, M.S., Grosof, D.H., De Valois, R.L. & Elfar, S.D. Spatial-frequency organization in primate striate cortex. Proc. Natl. Acad. Sci. USA 86, 711–715 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Tootell, R.B., Silverman, M.S., Hamilton, S.L., Switkes, E. & De Valois, R.L. Functional anatomy of macaque striate cortex. V. Spatial frequency. J. Neurosci. 8, 1610–1624 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 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 

  21. Stosiek, C., Garaschuk, O., Holthoff, K. & Konnerth, A. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl. Acad. Sci. USA 100, 7319–7324 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ohki, K. et al. Highly ordered arrangement of single neurons in orientation pinwheels. Nature 442, 925–928 (2006).

    Article  CAS  PubMed  Google Scholar 

  23. Ringach, D.L., Sapiro, G. & Shapley, R. A subspace reverse-correlation technique for the study of visual neurons. Vision Res. 37, 2455–2464 (1997).

    Article  CAS  PubMed  Google Scholar 

  24. Nauhaus, I., Nielsen, K.J. & Callaway, E.M. Nonlinearity of two-photon Ca2+ imaging yields distorted measurements of tuning for V1 neuronal populations. J. Neurophysiol. 107, 923–936 (2012).

    Article  CAS  PubMed  Google Scholar 

  25. Maffei, L. & Fiorentini, A. Spatial frequency rows in the striate visual cortex. Vision Res. 17, 257–264 (1977).

    Article  CAS  PubMed  Google Scholar 

  26. Berardi, N., Bisti, S., Cattaneo, A., Fiorentini, A. & Maffei, L. Correlation between the preferred orientation and spatial frequency of neurones in visual areas 17 and 18 of the cat. J. Physiol. (Lond.) 323, 603–618 (1982).

    Article  CAS  Google Scholar 

  27. Tootell, R.B., Silverman, M.S. & De Valois, R.L. Spatial frequency columns in primary visual cortex. Science 214, 813–815 (1981).

    Article  CAS  PubMed  Google Scholar 

  28. Tolhurst, D.J. & Thompson, I. Organization of neurones preferring similar spatial frequencies in cat striate cortex. Exp. Brain Res. 48, 217–227 (1982).

    Article  CAS  PubMed  Google Scholar 

  29. DeAngelis, G.C., Ghose, G.M., Ohzawa, I. & Freeman, R.D. Functional micro-organization of primary visual cortex: receptive field analysis of nearby neurons. J. Neurosci. 19, 4046–4064 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Molotchnikoff, S., Gillet, P.-C., Shumikhina, S. & Bouchard, M. Spatial frequency characteristics of nearby neurons in cats' visual cortex. Neurosci. Lett. 418, 242–247 (2007).

    Article  CAS  PubMed  Google Scholar 

  31. Shoham, D., Huebener, M., Schulze, S., Grinvald, A. & Bonhoeffer, T. Spatio-temporal frequency domains and their relation to cytochrome oxidase staining in cat visual cortex. Nature 385, 529–33 (1997).

    Article  CAS  PubMed  Google Scholar 

  32. Everson, R.M. et al. Representation of spatial frequency and orientation in the visual cortex. Proc. Natl. Acad. Sci. USA 95, 8334–8338 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Xu, X., Anderson, T.J. & Casagrande, V.A. How do functional maps in primary visual cortex vary with eccentricity? J. Comp. Neurol. 501, 741–755 (2007).

    Article  PubMed  Google Scholar 

  34. Gilbert, C.D. Microcircuitry of the visual cortex. Annu. Rev. Neurosci. 6, 217–247 (1983).

    Article  CAS  PubMed  Google Scholar 

  35. Martin, K.A.C. Neuronal circuits in cat striate cortex. in Cerebral Cortex (eds. Jones, E.G. & Peters, A.) 2:241–2:284 (Plenum, New York, 1984).

  36. Callaway, E.M. Local circuits in primary visual cortex of the macaque monkey. Annu. Rev. Neurosci. 21, 47–74 (1998).

    Article  CAS  PubMed  Google Scholar 

  37. Nassi, J.J. & Callaway, E.M. Parallel processing strategies of the primate visual system. Nat. Rev. Neurosci. 10, 360–372 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Boyd, J.D. & Matsubara, J.A. Laminar and columnar patterns of geniculocortical projections in the cat: relationship to cytochrome oxidase. J. Comp. Neurol. 365, 659–682 (1996).

    Article  CAS  PubMed  Google Scholar 

  39. Swindale, N.V., Shoham, D., Grinvald, A., Bonhoeffer, T. & Hübener, M. Visual cortex maps are optimized for uniform coverage. Nat. Neurosci. 3, 822–826 (2000).

    Article  CAS  PubMed  Google Scholar 

  40. Issa, N.P., Trachtenberg, J.T., Chapman, B., Zahs, K.R. & Stryker, M.P. The critical period for ocular dominance plasticity in the ferret's visual cortex. J. Neurosci. 19, 6965–6978 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. White, L.E., Bosking, W. & Fitzpatrick, D. Consistent mapping of orientation preference across irregular functional domains in ferret visual cortex. Vis. Neurosci. 18, 65–76 (2001).

    Article  CAS  PubMed  Google Scholar 

  42. Durbin, R. & Mitchison, G. A dimension reduction framework for understanding cortical maps. Nature 343, 644–647 (1990).

    Article  CAS  PubMed  Google Scholar 

  43. Koulakov, A.A. & Chklovskii, D. Orientation preference patterns in mammalian visual cortex: a wire length minimization approach. Neuron 29, 519–527 (2001).

    Article  CAS  PubMed  Google Scholar 

  44. Swindale, N.V. The development of topography in the visual cortex: a review of models. Network 7, 161–247 (1996).

    Article  CAS  PubMed  Google Scholar 

  45. Ferster, D. & Miller, K. Neural mechanisms of orientation selectivity in the visual cortex. Annu. Rev. Neurosci. 23, 441–471 (2000).

    Article  CAS  PubMed  Google Scholar 

  46. McLaughlin, D., Shapley, R. & Shelley, M. Large-scale modeling of the primary visual cortex: influence of cortical architecture upon neuronal response. J. Physiol. Paris 97, 237–252 (2003).

    Article  PubMed  Google Scholar 

  47. Paik, S.-B. & Ringach, D.L. Retinal origin of orientation maps in visual cortex. Nat. Neurosci. 14, 919–925 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Kaschube, M. et al. Universality in the evolution of orientation columns in the visual cortex. Science 330, 1113–1116 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Li, Y., Van Hooser, S.D., Mazurek, M., White, L.E. & Fitzpatrick, D. Experience with moving visual stimuli drives the early development of cortical direction selectivity. Nature 456, 952–956 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Kara, P. & Boyd, J.D. A micro-architecture for binocular disparity and ocular dominance in visual cortex. Nature 458, 627–631 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Nimmerjahn, A., Kirchhoff, F., Kerr, J.N.D. & Helmchen, F. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat. Methods 1, 31–37 (2004).

    Article  CAS  PubMed  Google Scholar 

  52. Pologruto, T.A., Sabatini, B.L. & Svoboda, K. ScanImage: flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2, 13 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Brainard, D.H. The psychophysics toolbox. Spat. Vis. 10, 433–436 (1997).

    CAS  PubMed  Google Scholar 

  54. Pelli, D.G. The VideoToolbox software for visual psychophysics: transforming numbers to movies. Spat. Vis. 10, 437–442 (1997).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to S. Chatterjee, K. Ohki and C. Reid for preliminary designs of the imaging chamber and for graciously helping us to get started with monkey two-photon imaging. We also thank D. Ringach for comments on an earlier version of the manuscript. Finally, we thank M. De La Parra for technical assistance with the experiments. This work was supported by US National Eye Institute grants EY-010742 to E.M.C., EY-019821 to I.N and MH093567 to A.A.D.

Author information

Authors and Affiliations

Authors

Contributions

I.N., K.J.N. and E.M.C. designed the research. I.N., K.J.N., A.A.D. and E.M.C. performed experiments. I.N. analyzed the data. I.N., K.J.N. and E.M.C. wrote the paper.

Corresponding author

Correspondence to Edward M Callaway.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–8 (PDF 860 kb)

Supplementary Video 1

The acquired images during a flashed grating stimulus, played at 2x the actual speed, are shown on the left. The movie begins about 8 sec after the start of the trial, as depicted by the "progress bar" along the x-axis in each of the two panels on the right. The stimulus begins 2 s after the start of the timecourse, and lasts for 60 s. The right panels also contain the measured (black) and predicted (blue/red) response of the two circled neurons in the movie. The red and blue circles move with the measured location of each neuron as determined by the movement correction algorithm. The dominant movement in this trial is coupled to the animal's breathing. The heartbeat can be seen as well, but is more subtle. This difference between the two motion sources was typical, although this is not always the case, as demonstrated by the trial from Supp. Fig. 6b. (AVI 34564 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nauhaus, I., Nielsen, K., Disney, A. et al. Orthogonal micro-organization of orientation and spatial frequency in primate primary visual cortex. Nat Neurosci 15, 1683–1690 (2012). https://doi.org/10.1038/nn.3255

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3255

This article is cited by

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