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A micro-architecture for binocular disparity and ocular dominance in visual cortex

Abstract

In invertebrate predators such as the praying mantis and vertebrate predators such as wild cats the ability to detect small differences in inter-ocular retinal disparities is a critical means for accurately determining the depth of moving objects such as prey1. In mammals, the first neurons along the visual pathway that encode binocular disparities are found in the visual cortex. However, a precise functional architecture for binocular disparity has never been demonstrated in any species, and coarse maps for disparity have been found in only one primate species2,3. Moreover, the dominant approach for assaying the developmental plasticity of binocular cortical neurons used monocular tests of ocular dominance to infer binocular function4. The few studies that examined the relationship between ocular dominance and binocular disparity of individual cells used single-unit recordings and have provided conflicting results regarding whether ocular dominance can predict the selectivity or sensitivity to binocular disparity5,6,7,8,9. We used two-photon calcium imaging to sample the response to monocular and binocular visual stimuli from nearly every adjacent neuron in a small region of the cat visual cortex, area 18. Here we show that local circuits for ocular dominance always have smooth and graded transitions from one apparently monocular functional domain to an adjacent binocular region. Most unexpectedly, we discovered a new map in the cat visual cortex that had a precise functional micro-architecture for binocular disparity selectivity. At the level of single cells, ocular dominance was unrelated to binocular disparity selectivity or sensitivity. When the local maps for ocular dominance and binocular disparity both had measurable gradients at a given cortical site, the two gradient directions were orthogonal to each other. Together, these results indicate that, from the perspective of the spiking activity of individual neurons, ocular dominance cannot predict binocular disparity tuning. However, the precise local arrangement of ocular dominance and binocular disparity maps provide new clues regarding how monocular and binocular depth cues may be combined and decoded.

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Figure 1: Single-cell responses and functional maps from two experiments.
Figure 2: Orthogonal maps for binocular disparity and ocular dominance when gradients were evident in both maps.
Figure 3: Relationship between disparity sensitivity and the response to monocular stimuli.
Figure 4: Stable functional micro-architecture for binocular disparity.

References

  1. Rossel, S. Binocular stereopsis in an insect. Nature 302, 821–822 (1983)

    ADS  Article  Google Scholar 

  2. DeAngelis, G. C. & Newsome, W. T. Organization of disparity-selective neurons in macaque area MT. J. Neurosci. 19, 1398–1415 (1999)

    CAS  Article  Google Scholar 

  3. Chen, G., Lu, H. D. & Roe, A. W. A map for horizontal disparity in monkey V2. Neuron 58, 442–450 (2008)

    CAS  Article  Google Scholar 

  4. Hubel, D. H. & Wiesel, T. N. Early exploration of the visual cortex. Neuron 20, 401–412 (1998)

    CAS  Article  Google Scholar 

  5. Poggio, G. F. & Fischer, B. Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey. J. Neurophysiol. 40, 1392–1405 (1977)

    CAS  Article  Google Scholar 

  6. Ferster, D. A comparison of binocular depth mechanisms in areas 17 and 18 of the cat visual cortex. J. Physiol. (Lond.) 311, 623–655 (1981)

    CAS  Article  Google Scholar 

  7. Gardner, J. C. & Raiten, E. J. Ocular dominance and disparity-sensitivity: why there are cells in the visual cortex driven unequally by the two eyes. Exp. Brain Res. 64, 505–514 (1986)

    CAS  Article  Google Scholar 

  8. LeVay, S. & Voigt, T. Ocular dominance and disparity coding in cat visual cortex. Vis. Neurosci. 1, 395–414 (1988)

    CAS  Article  Google Scholar 

  9. Read, J. C. & Cumming, B. G. Ocular dominance predicts neither strength nor class of disparity selectivity with random-dot stimuli in primate V1. J. Neurophysiol. 91, 1271–1281 (2004)

    Article  Google Scholar 

  10. Parker, A. In the Blink of an Eye: How Vision Sparked the Big Bang of Evolution (Basic Books, 2003)

    Google Scholar 

  11. Barlow, H. B., Blakemore, C. & Pettigrew, J. D. The neural mechanism of binocular depth discrimination. J. Physiol. (Lond.) 193, 327–342 (1967)

    CAS  Article  Google Scholar 

  12. DeAngelis, G. C., Ohzawa, I. & Freeman, R. D. Depth is encoded in the visual cortex by a specialized receptive field structure. Nature 352, 156–159 (1991)

    ADS  CAS  Article  Google Scholar 

  13. Anzai, A., Ohzawa, I. & Freeman, R. D. Neural mechanisms underlying binocular fusion and stereopsis: position vs. phase. Proc. Natl Acad. Sci. USA 94, 5438–5443 (1997)

    ADS  CAS  Article  Google Scholar 

  14. Prince, S. J., Pointon, A. D., Cumming, B. G. & Parker, A. J. Quantitative analysis of the responses of V1 neurons to horizontal disparity in dynamic random-dot stereograms. J. Neurophysiol. 87, 191–208 (2002)

    CAS  Article  Google Scholar 

  15. Haefner, R. M. & Cumming, B. G. Adaptation to natural binocular disparities in primate V1 explained by a generalized energy model. Neuron 57, 147–158 (2008)

    CAS  Article  Google Scholar 

  16. Hubel, D. H. & Wiesel, T. N. Binocular interaction in striate cortex of kittens reared with artificial squint. J. Neurophysiol. 28, 1041–1059 (1965)

    CAS  Article  Google Scholar 

  17. Mitchell, D. in The Visual Neurosciencs (eds Chalupa, L. M & Werner, J. S.) 189–204 (MIT Press, 2004)

    Google Scholar 

  18. Ohzawa, I. & Freeman, R. D. The binocular organization of simple cells in the cat’s visual cortex. J. Neurophysiol. 56, 221–242 (1986)

    CAS  Article  Google Scholar 

  19. Freeman, R. D. & Ohzawa, I. Development of binocular vision in the kitten’s striate cortex. J. Neurosci. 12, 4721–4736 (1992)

    CAS  Article  Google Scholar 

  20. Chino, Y. M., Smith, E. L., Hatta, S. & Cheng, H. Postnatal development of binocular disparity sensitivity in neurons of the primate visual cortex. J. Neurosci. 17, 296–307 (1997)

    CAS  Article  Google Scholar 

  21. Maruko, I. et al. Postnatal development of disparity sensitivity in visual area 2 (V2) of macaque monkeys. J. Neurophysiol. 100, 2486–2495 (2008)

    CAS  Article  Google Scholar 

  22. Ohki, K., Chung, S., Ch'ng, Y. H., Kara, P. & Reid, R. C. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433, 597–603 (2005)

    ADS  CAS  Article  Google Scholar 

  23. Ohzawa, I., DeAngelis, G. C. & Freeman, R. D. Stereoscopic depth discrimination in the visual cortex: neurons ideally suited as disparity detectors. Science 249, 1037–1041 (1990)

    ADS  CAS  Article  Google Scholar 

  24. Bonhoeffer, T., Kim, D. S., Malonek, D., Shoham, D. & Grinvald, A. Optical imaging of the layout of functional domains in area 17 and across the area 17/18 border in cat visual cortex. Eur. J. Neurosci. 7, 1973–1988 (1995)

    CAS  Article  Google Scholar 

  25. Ringach, D. L. On the origin of the functional architecture of the cortex. PLoS ONE 2, e251 (2007)

    ADS  Article  Google Scholar 

  26. Shimojo, S., Silverman, G. H. & Nakayama, K. An occlusion-related mechanism of depth perception based on motion and interocular sequence. Nature 333, 265–268 (1988)

    ADS  CAS  Article  Google Scholar 

  27. Obermayer, K., Blasdel, G. G. & Schulten, K. Statistical–mechanical analysis of self-organization and pattern formation during the development of visual maps. Phys. Rev. A 45, 7568–7589 (1992)

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  29. 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)

    CAS  Article  Google Scholar 

  30. 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)

    ADS  CAS  Article  Google Scholar 

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Acknowledgements

We thank B. Cumming and N. Swindale for discussions. We thank B. Shi, Z. Shen, Z. Lu and J. Schnellmann for comments on the manuscript. This work was supported by grants from the NIH, Whitehall and Dana Foundations to P.K.

Author Contributions P.K. conceived the project, designed the experiments and set up the laboratory. P.K. and J.D.B. performed the experiments. P.K. analysed the data and wrote the paper. Both authors discussed the results and commented on the manuscript.

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Correspondence to Prakash Kara.

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Kara, P., Boyd, J. A micro-architecture for binocular disparity and ocular dominance in visual cortex. Nature 458, 627–631 (2009). https://doi.org/10.1038/nature07721

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