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Contrast dependence of contextual effects in primate visual cortex

Abstract

The responses of neurons in the visual cortex to stimuli presented within their receptive fields can be markedly modulated by stimuli presented in surrounding regions that do not themselves evoke responses1–7. This modulation depends on the relative orientation and direction of motion of the centre and surround stimuli, and it has been suggested that local cortical circuits linking cells with similar stimulus selectivities underlie these phenomena 8–16. However, the functional relevance and nature of these integrative processes remain unclear. Here we investigate how such integration depends on the relative activity levels of neurons at different points across the cortex by varying the relative contrast of stimuli over the receptive field and surrounding regions. We show that simply altering the balance of the excitation driving centre and surround regions can dramatically change the sign and stimulus selectivity of these contextual effects. Thus, the way that single neurons integrate information across the visual field depends not only on the precise form of stimuli at different locations, but also crucially on their relative contrasts. We suggest that these effects reflect a complex gaincontrol mechanism that regulates cortical neuron responsiveness, which permits dynamic modification of response properties of cortical neurons.

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References

  1. Nelson, J. I. & Frost, B. J. Orientation-selective inhibition from beyond the classical visual receptive field. Brain Res. 139, 359–365 (1978).

    Article  CAS  Google Scholar 

  2. Allman, J., Miezin, F. & McGuinness, E. Stimulus specific responses from beyond the classical receptive field—neurophysiological mechanisms for local global comparisons in visual neurons Annu. Rev. Neurosci. 8, 407–430 (1985).

    Article  CAS  Google Scholar 

  3. Gilbert, C. D. & Wiesel, T. N. The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat. Visual Res. 30, 1689–1701 (1990).

    CAS  Google Scholar 

  4. Knierim, J. J. & Van Essen, D. C. Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. J. Neurophysiol 67, 961–980 (1992).

    Article  CAS  Google Scholar 

  5. Li, C. Y. & Li, W. Extensive integration field beyond the classical receptive field of cat striate cortical neurons—classification and tuning properties. Vision Res. 34, 2337–2355 (1994).

    Article  CAS  Google Scholar 

  6. DeAngelis, G. C., Freeman,R. D. & Ohzawa, I. Length and width tuning of neurons in the cat's primary visual cortex. J. Neurophysiol. 71, 347–374 (1994).

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  8. Rockland, K. S. & Lund, J. L. Intrinsic laminar lattice connections in primate visual cortex. J. Comp. Neurol. 216, 303–318 (1983).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  10. Lund, J. S., Yoshioka, T. & Levitt, J. B. Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. Cereb. Cortex 3, 148–162 (1993).

    Article  CAS  Google Scholar 

  11. Amir, Y., Harel, M. Malach, R. Cortical Hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex. J. Comp. Neurol. 334, 19–46 (1993).

    Article  CAS  Google Scholar 

  12. Yoshioka, T., Blasdel, G. G., Levitt, J. B. & Lund, J. S. Relation between patterns of intrinsic lateral connectivity, ocular dominance, and cytochrorne-oxidase reactive regions in macaque monkey striate cortex. Cereb. Cortex 6, 297–310 (1996).

    Article  CAS  Google Scholar 

  13. Rockland, K. S., Lund, J. S. & Humphrey, A. L. Anatomical banding of intrinsic connections in striate cortex of three shrews (Tupaia glis). J. Comp. Neurol. 209, 41–58 (1982).

    Article  CAS  Google Scholar 

  14. Ts'o, D. Y., Gilbert, C. D. & Wiesel, T. N. Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. J. Neurosci. 6, 1160–11170 (1986).

    Article  CAS  Google Scholar 

  15. 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 

  16. 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 

  17. Lamme, V. A. F. The neurophysiology of figure-ground segregation in primary -ual cortex J. Neurosci. 15, 1605–1615 (1995).

    Article  CAS  Google Scholar 

  18. Zipser, K., Lamme, V. A. F. & Schiller, P. H. Contextual modulation in primary visual cortex. J. Neurosci 16, 7376–7389 (1996).

    Article  CAS  Google Scholar 

  19. Toth, L. J., Rao, S. C., Kim, D.-S., Somers, D. & Sur,M. Subthreshold facilitation and suppression in primary visual cortex revealed by intrinsic signal imaging. Proc. Natl Acad. Sci. USA 93, 9869–9874 (1996).

    Article  ADS  CAS  Google Scholar 

  20. Douglas, R. J., Koch, C., Majowald, M., Martin, K. A. C. Suarez, H. H. Recurrent excitation in neucortical circuits. Science 269, 981–985 (1995).

    Article  ADS  CAS  Google Scholar 

  21. Heeger, D. J. Normalization of cell responses in cat striate cortex. Vis. Neurosci. 9, 181–197 (1992).

    Article  CAS  Google Scholar 

  22. Somers, D. C., Nelson, S. B. & Sur, M. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 15, 5448–5465(1995).

    Article  CAS  Google Scholar 

  23. Stuart, G. & Sakmann, B. Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15, 1065–1076 (1995).

    Article  CAS  Google Scholar 

  24. Markram, H., Helm, P. J. & Sakmann, B. Dendritic calcium transients evoked by single backpropagating action potentials in rat neocortical pyramidal neurons. J. Physiol.(Lond.) 485, 1–20 (1995).

    Article  CAS  Google Scholar 

  25. Thomson, A. M. Deuchars, J. D. Temporal and spatial properties of local circuits in neocortex. Trends Neurosci. 17, 119–126 (1994).

    Article  CAS  Google Scholar 

  26. Deuchars, J. D., West, D. C. & Thomson, A. M. Relationships between morphology and physiology of pyramid-pyramid single axon connections in rat neocortex In vitro. J. Physiol. (Lond.) 478, 423–435 (1994).

    Article  Google Scholar 

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Levitt, J., Lund, J. Contrast dependence of contextual effects in primate visual cortex. Nature 387, 73–76 (1997). https://doi.org/10.1038/387073a0

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