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Topography of contextual modulations mediated by short-range interactions in primary visual cortex

Nature volume 399, pages 655–661 (1999)Cite this article

Abstract

Neurons in primary visual cortex (V1) respond differently to a simple visual element presented in isolation from when it is embedded withina complex image. This difference, a specific modulation by surrounding elements in the image, is mediated by short- and long-range connections within V1 and by feedback from other areas. Here we study the role of short-range connections in this process, and relate it to the layout of local inhomogeneities in the cortical maps of orientation and space. By measuring correlation between neuron pairs located in optically imaged maps of V1 orientation columns we show that the strength of local connections between cells is a graded function of lateral separation across cortex, largely radially symmetrical and relatively independent of orientation preferences. We then show the contextual influence of flanking visual elements on neuronal responses varies systematically with a neuron's position within the cortical orientation map. The strength of this contextual influence on a neuron can be predicted from a model of local connections based on simple overlap with particular features of the orientation map. This indicates that local intracortical circuitry could endow neurons with a graded specialization for processing angular visual features such as corners and T junctions, and this specialization could have its own functional cortical map, linked with the orientation map.

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Figure 1: V1 neurons have strong local interconnections, independent of relative orientation difference.
Figure 2: Normalized cross-correlation peak height (left) and peak area (right) for receptive field pairs as a function of inter-site separation on cortex.
Figure 3: Specific suppressive influence of perpendicular flank stimuli.
Figure 4: Comparing suppression strength with arborization overlap calculated using geometric model.
Figure 5: Flanks originating from nearer cortical loci lead to stronger suppression.

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References

  1. Gilbert, C. D. Adult cortical dynamics Physiol. Rev. 78, 467–485 (1998).

    Article  ADS  CAS  Google Scholar 

  2. Kapadia, M. K., Ito, M., Gilbert, C. D. & Westheimer, G. Improvement in visual sensitivity by changes in local context: parallel studies in human observers and in V1 of alert monkeys. Neuron 15, 843–856 (1995).

    Article  CAS  Google Scholar 

  3. Gilbert, C. D. Horizontal integration and cortical dynamics. Neuron 9, 1–13 (1992).

    Article  CAS  Google Scholar 

  4. Polat, U., Mizobe, K., Pettet, M. W., Kasamatsu, T. & Norcia, A. M. Collinear stimuli regulate visual responses depending on cell's contrast threshold. Nature 391, 580–584 (1998).

    Article  ADS  CAS  Google Scholar 

  5. Wertheimer, M. Laws of Organization in Perceptual Forms(Harcourt, Brace and Jovanovich, London, 1938).

    Book  Google Scholar 

  6. Ullman, S. Three-dimensional object recognition. Cold Spring Harbor Symp. Quant. Biol. 55, 889–898 (1990).

    Article  CAS  Google Scholar 

  7. Field, D. J., Hayes, A. & Hess, R. F. Contour integration by the human visual systems: evidence for a local “association field”. Vision Res. 33, 173–193 (1993).

    Article  CAS  Google Scholar 

  8. Hubel, D. H. & Wiesel, T. N. Sequence regularity and geometry of orientation columns in the monkey striate cortex. J. Comp. Neurol. 158, 267–294 ( 1974).

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  12. Das, A. & Gilbert, C. D. Distortions of visuotopic map match orientation singularities in primary visual cortex. Nature 387, 594–598 ( 1997).

    Article  ADS  CAS  Google Scholar 

  13. Malach, R., Amir, Y., Harel, M. & Grinvald, A. Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. Proc. Natl Acad. Sci. USA 90, 10469– 10473 (1993).

    Article  ADS  CAS  Google Scholar 

  14. Malach, R. Dendritic sampling across processing streams in monkey striate cortex. J. Comp. Neurol. 315, 303–312 (1992).

    Article  CAS  Google Scholar 

  15. Hubener, M. & Bolz, J. Relationships between dendritic morphology and cytochrome oxidase compartments in monkey striate cortex. J. Comp. Neurol. 324, 67–80 (1992).

    Article  CAS  Google Scholar 

  16. Katz, L. C., Gilbert, C. D. & Wiesel, T. N. Local circuits and ocular dominance columns in monkey striate cortex. J. Neurosci. 9, 1389– 1399 (1989).

    Article  CAS  Google Scholar 

  17. Bosking, W. H., Zhang, Y., Schofield, B. & Fitzpatrick, D. Orientation selectivity and arrangement of horizontal connections in tree shrew striate cortex. J. Neurosci. 17, 2112– 2127 (1997).

    Article  CAS  Google Scholar 

  18. Sillito, A. M., Grieve, K. L., Jones, H. L., Cuderio, J. & Davis, J. Visual cortical mechanisms detecting focal orientation discontinuities. Nature 378, 492–496 (1995).

    Article  ADS  CAS  Google Scholar 

  19. Shevelev, I. A., Novikova, R. V., Lazareva, N. A., Tikhomirov, A. S. & Sharaev, G. A. Sensitivity to cross-like figures in the cat striate neurons. Neuroscience 69, 51–57 ( 1995).

    Article  CAS  Google Scholar 

  20. Shevelev, I. A., Lazareva, N. A., Sharaev, G. A., Novikova, R. V. & Tikhomirov, A. S. Selective and invariant sensitivity to crosses and corners in cat striate cortex neurons. Neuroscience 84, 713–721 (1998).

    Article  CAS  Google Scholar 

  21. Gilbert, C. D. & Wiesel, T. N. Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex. Nature 280, 120– 125 (1979).

    Article  ADS  CAS  Google Scholar 

  22. Gilbert, C. D. & Wiesel, T. N. Clustered intrinsic connections in cat visual cortex. J. Neurosci. 3, 1116–1133 (1983).

    Article  CAS  Google Scholar 

  23. Ts'o, D. Y., Gilbert, C. D. & Wiesel, T. N. Relationships between horizontal corticocortical connections in cat visual cortex. J. Neurosci. 9, 2432–2442 (1989).

    Article  Google Scholar 

  24. Gilbert, C. D. & Wiesel, T. N. Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J. Neurosci. 9, 2432–2442 (1989).

    Article  CAS  Google Scholar 

  25. Grinvald, A., Lieke, E. E., Frostig, R. D., Gilbert, C. D. & Wiesel, T. N. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324, 361–364 (1986).

    Article  ADS  CAS  Google Scholar 

  26. Frostig, R. D., Lieke, E. E., Ts'o, D. Y. & Grinvald, A. Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high resolution optical imaging of intrinsic signals. Proc. Natl Acad. Sci. USA 6082 –6086 (1990).

  27. Das, A. & Gilbert, C. D. Receptive field expansion in adult visual cortex is linked to dynamic changes in strength of cortical connections. J. Neurophysiol. 74, 779– 792 (1995).

    Article  CAS  Google Scholar 

  28. Aertsen, A. M. H. J. & Gerstein, G. L. Evaluation of neuronal connectivity: sensitivity of crosscorrelation. Brain Res. 340, 341–354 ( 1985).

    Article  CAS  Google Scholar 

  29. Perkel, D. H., Gerstein, G. L. & Moore, G. P. Neuronal spike trains and stochastic point processes. I Thesingle spike train. Biophys. J. 7, 391–418 (1967).

    Article  CAS  Google Scholar 

  30. Perkel, D. H., Gerstein, G. L. & Moore, G. P. Neuronal spike trains and stochastic point processes. II Simultaneous spike trains. Biophys. J. 7, 419–440 (1967).

    Article  CAS  Google Scholar 

  31. Melssen, W. J. & Epping, W. J. M. Detection and estimation of neuronal connectivity based on crosscorrelation analysis. Biol. Cybern. 57, 403– 414 (1987).

    Article  CAS  Google Scholar 

  32. Hata, Y., Tsumoto, T., Sato, H. & Tamura, H. Horizontal interactions between visual cortical neurones studied by cross-correlation analysis in the cat. J. Physiol. 441, 593– 614 (1991).

    Article  CAS  Google Scholar 

  33. Kisvarday, Z. F. et al . Synaptic targets of HRP-filled layer III pyramidal cells in the cat striate cortex. Exp. Brain Res. 64, 541–552 (1986).

    Article  CAS  Google Scholar 

  34. McGuire, B. A., Gilbert, C. D., Rivlin, P. K. & Wiesel, T. N. Targets of horizontal connections in macaque primary visual cortex. J. Comp. Neurol. 305, 370–392 (1991).

    Article  CAS  Google Scholar 

  35. Hirsch, J. & Gilbert, C. D. Synaptic physiology of horizontal connections in the cat's visual cortex. J. Neurosci. 11, 1800–1908 (1991).

    Article  CAS  Google Scholar 

  36. Malach, R. Cortical columns as devices for maximizing neuronal diversity. Trends Neurosci. 17, 101–104 (1994).

    Article  CAS  Google Scholar 

  37. Bauer, U., Scholz, M., Levitt, J. B., Obermayer, K. & Lund, J. S. Amodel for the depth-dependence of receptive field size and contrast sensitivity of cells in layer 4C of macaque striate cortex. Vision Res. 39, 613– 629 (1999).

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  39. Ito, M. & Gilbert, C. D. Attention modulates contextual influences in the primary visual cortex of alert monkeys. Neuron 22, 593–604 ( 1999).

    Article  CAS  Google Scholar 

  40. Crist, R. E., Ito, M., Westheimer, G. & Gilbert, C. D. Task dependent contextual interactions in the primary visual cortex of primates trained in hyperacuity discrimination. Abstr. Soc. Neurosci. 23 , 1543 (1997).

    Google Scholar 

  41. Ito, M., Westheimer, G. & Gilbert, C. D. Attention and perceptual learning modulate contextual influences on visual perception. Neuron 20, 1191–1197 (1998).

    Article  CAS  Google Scholar 

  42. Sompolinsky, H. & Shapley, R. New perspectives on the mechanism for orientation selectivity. Curr. Opin. Neurobiol. 7, 514–522 ( 1997).

    Article  CAS  Google Scholar 

  43. Crook, J. M., Kisvárday, Z. F. & Eysel, U. T. GABA-induced inactivation of functionally characterized sites in cat striate cortex: effects on orientation tuning and direction selectivity. Vis. Neurosci. 14, 141– 158 (1997).

    Article  CAS  Google Scholar 

  44. Crook, J. M., Kisvárday, Z. F. & Eysel, U. T. Evidence for a contribution of lateral inhibition to orientation tuning and direction selectivity in cat visual cortex: reversible inactivation of functionally characterized sites combined with neuroanatomical tracing techniques. Eur. J. Neurosci. 10, 2056–2075 (1998).

    Article  CAS  Google Scholar 

  45. Gawne, T. J., Kjaer, T. W., Hertz, J. A. & Richmond, B. J. Adjacent visual cortical complex cells share about 20% of their stimulus-related information. Cerebral Cortex 6, 482– 489 (1996).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank A. Glatz and J. Lopez for expert technical assistance. The work was supported by the National Science Foundation.

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  1. The Rockefeller University, 1230 York Avenue, New York, 10021, New York, USA

    Aniruddha Das & Charles D. Gilbert

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  1. Aniruddha Das
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Correspondence to Charles D. Gilbert.

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Das, A., Gilbert, C. Topography of contextual modulations mediated by short-range interactions in primary visual cortex. Nature 399, 655–661 (1999). https://doi.org/10.1038/21371

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