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Collinear stimuli regulate visual responses depending on cell's contrast threshold

Abstract

Neurons in the primary visual cortex are selective for the size, orientation and direction of motion of patterns falling within a restricted region of visual space known as the receptive field1. The response to stimuli presented within the receptive field can be facilitated or suppressed by other stimuli falling outside the receptive field which, when presented in isolation, fail to activate the cell2,3,4,5,6,7,8. Whether this interaction is facilitative3,4,7,9,10,11,12 or suppressive2,3,5,6,8,9,10,11,12,13,14 depends on the relative orientation of pattern elements inside and outside the receptive field. Here we show that neuronal facilitation preferentially occurs when a near-threshold stimulus inside the receptive field is flanked by higher-contrast, collinear elements located in surrounding regions of visual space. Collinear flanks and orthogonally oriented flanks, however, both act to reduce the response to high-contrast stimuli presented within the receptive field. The observed pattern of facilitation and suppression may be the cellular basis for the observation in humans that the detectability of an oriented pattern is enhanced by collinear flanking elements15,16,17. Modulation of neuronal responses by stimuli falling outside their receptive fields may thus represent an early neural mechanism for encoding objects and enhancing their perceptual saliency.

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Figure 1: The stimuli were Gabor patches (Gaussian-weighted sinusoids) presented singly or in combination.
Figure 2: The comparison of contrast–response functions between target alone (filled circles) and target plus two collinear flanks (open circles) is exemplified in two single cells.
Figure 3: Population summary of contrast-dependent modulation for 325 data points, all of which satisfied the additivity test (see Methods), obtained from the 83 cells tested with three contrasts or more per cell.

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References

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

    Article  CAS  Google Scholar 

  2. Blakemore, C. & Tobin, E. A. Lateral inhibition between orientation detectors in the cat's visual cortex. Exp. Brain Res. 15, 439–440 (1972).

    Article  CAS  Google Scholar 

  3. Maffei, L. & Fiorentini, A. The unresponsive regions of visual cortical receptive fields. Vision Res. 16, 1131–1139 (1976).

    Article  CAS  Google Scholar 

  4. Nelson, J. I. & Frost, B. J. Intracortical facilitation among co-oriented, co-axially aligned simple cells in cat striate cortex. Exp. Brain Res. 61, 54–61 (1985).

    Article  CAS  Google Scholar 

  5. 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 

  6. 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 

  7. 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 

  8. 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 

  9. Mizobe, K., Polat, U., Kasamatsu, T. & Norcia, A. M. Lateral masking reveals facilitation and suppression from the same single cells in cat area 17. Assoc. Res. Vis. Ophthal. Abstr. 37, S493 (1996).

    Google Scholar 

  10. 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 

  11. Stemmler, M., Usher, M. & Niebur, E. Lateral interactions in primary visual cortex: a model bridging physiology and psychophysics. Science 269, 1877–1880 (1995).

    Article  ADS  CAS  Google Scholar 

  12. Somers, D. C., Nelson, S. & Sur, M. Effects of long-range connections on gain control in an emergent model of visual cortical orientation selectivity. Soc. Neurosci. Abstr. 20, 1577 (1994).

    Google Scholar 

  13. Kitano, M., Niiyama, K., Kasamatsu, T., Norcia, A. M. & Sutter, E. E. Retinotopic and nonretinotopic field potentials in cat visual cortex. Vis. Neurosci. 11, 953–977 (1994).

    Article  CAS  Google Scholar 

  14. Levitt, J. B. & Lund, J. S. Contrast dependence of contextual effects in primate visual cortex. Nature 387, 73–76 (1997).

    Article  ADS  CAS  Google Scholar 

  15. Polat, U. & Sagi, D. Lateral interactions between spatial channels: suppression and facilitation revealed by lateral masking experiments. Vision Res. 33, 993–999 (1993).

    Article  CAS  Google Scholar 

  16. Polat, U. & Sagi, D. The architecture of perceptual spatial interactions. Vision Res. 34, 73–78 (1994).

    Article  CAS  Google Scholar 

  17. Polat, U. & Norcia, A. M. Neurophysiological evidence for contrast dependent long-range facilitation and suppression in the human visual cortex. Vision Res. 36, 2099–2109 (1996).

    Article  CAS  Google Scholar 

  18. Albrecht, D. G. & Hamliton, D. B. Striate cortex of monkey and cat: contrast response function. J. Neurophysiol. 48, 217–236 (1982).

    Article  CAS  Google Scholar 

  19. Somers, D. C., Todorov, E. V., Siapas, A. G., Toth, L. J., Kim, D.-S. & Sur, M. Alocal circuit integration approach to understanding visual cortical receptive fields. Cerebr. Cort. (in the press).

  20. Douglas, R. J., Martin, K. A. C. & Whitteridge, D. An intracellular analysis of the visual responses of neurones in cat visual cortex. J. Physiol. 440, 659–696 (1991).

    Article  CAS  Google Scholar 

  21. Hirsch, J. A. & Gilbert, C. D. Synaptic physiology of horizontal connections in the cat visual cortex. J. Neurosci. 11, 1800–1809 (1991).

    Article  CAS  Google Scholar 

  22. Douglas, R. J., Martin, K. A. C. & Whitteridge, D. Acanonical microcircuit for neocortex. J. Neur. Comp. 1, 480–488 (1989).

    Article  Google Scholar 

  23. McCormick, D. A., Connors, B. W., Lighthall, J. M. & Prince, D. A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of neorcortex. J. Neurophysiol. 54, 782–806 (1985).

    Article  CAS  Google Scholar 

  24. Cannon, M. W. & Fullenkamp, S. C. Spatial interactions in apparent contrast: inhibitory effects among grating patterns of different spatial frequencies, spatial patterns and orientations. Vis. Res. 31, 1985–1998 (1991).

    Article  CAS  Google Scholar 

  25. Cannon, M. W. & Fullenkamp, S. C. Spatial interactions in apparent contrast: individual differences in enhancement and suppression effects. Vis. Res. 33, 1685–1695 (1993).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Fitzpatrick, D. The functional organization of local circuits in visual cortex: insight from the study of tree shrew striate cortex. Cerebr. Cort. 6, 329–341 (1996).

    Article  CAS  Google Scholar 

  28. 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 

  29. Victor, J. D. & Mast, J. Anew statistic for steady-state evoked potentials. Electroenceph. Clin. Neurophysiol. 78, 378–388 (1991).

    Article  CAS  Google Scholar 

  30. Norcia, A. M., Clarke, M. & Tyler, C. W. Digital filtering and robust regression techniques for estimating sensory thresholds from the evoked potential. IEEE Eng. Med. Biol. 4, 26–32 (1985).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank S. P. McKee, D. Sagi, C. W. Tyler and M. Usher for helpful comments, E.Schmidt for technical support, and K. Swenson and V. Vildavski for software development. This work was supported by the National Eye Institute, the SKERI and Kyoto Prefectural University of Medicine.

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Correspondence to Takuji Kasamatsu.

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Polat, U., Mizobe, K., Pettet, M. et al. Collinear stimuli regulate visual responses depending on cell's contrast threshold. Nature 391, 580–584 (1998). https://doi.org/10.1038/35372

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