Neuroscience and Behavioral Physiology

, Volume 30, Issue 5, pp 599–609 | Cite as

Image features selected by neurons of the cat primary visual cortex

  • I. A. Shevelev


The sensitivity of neurons in field 17 of the visual cortex in cats to cross-shaped, Y-shaped, and star-shaped figures flashing in the receptive field was studied. About 40% of the neurons studied (114 of 289) were found to generate large responses (with an average response factor of 3.06±0.32) to one of the figures flashing in the center of the receptive field, as compared with the responses produced to a single bar in the optimal orientation. Most of these neurons (72%) were selectively sensitive to the shape and orientation of figures; the remainder demonstrated some degree of tuning invariance to these properties. The latent periods of responses to figures were usually shorter than those of responses to bars. Tuning parameters for bars and figures were generally related: neurons with acute orientational tuning to a bar were usually highly selective to both the configuration and the orientation people figures. Separate or combined stimulation with crosses in the center and near periphery of the receptive fields demonstrated summation, antagonism, or the lack of any interaction between these zones in producing sensitivity to crosses. Local blockade of intracortical GABAergic inhibition by microiontophoretic application of bicuculline showed that in one third of the neurons studied, sensitivity to figures was generated or enhanced by inhibition in normal conditions, while one third of cells showed suppression by inhibition, and sensitivity in the remainder was independent of inhibition. These data show that reconsideration of existing concepts of the role of field 17 in selecting only first-order shape features of images (i.e., the orientations of single lines) is needed, since almost half the neurons in the cat primary visual cortex can efficiently detect second-order features (angles and line intersections).

Key Words

Bicuculline GABA visual cortex selectivity invariance cat cross tuning neuron orientation image features receptive field inhibition angle figure shape sensitivity 


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  1. 1.
    G. M. Zenkin and A. P. Petrov, “A system for image analysis and the recognition of objects on complex backgrounds,”Biofizika,12, 493–501 (1967).PubMedGoogle Scholar
  2. 2.
    N. A. Lazareva, I. A. Shevelev, R. V. Novikova, A. S. Tikhomirova, and G. A. Sharaev, “Double orientational tuning of neurons in the primary visual cortex of the cat at different levels of consciousness,”Neirofiziologiya,24, 260–269 (1992).Google Scholar
  3. 3.
    N. A. Lazareva, I. A. Shevelev, U. Eysel, and G. A. Garaev, “Bicuculline and orientational tuning of neurons in the visual cortex,”Neirofiziologiya,27, 54–63 (1995).Google Scholar
  4. 4.
    N. A. Lazareva, I. A. Sheveleva, R. V. Novikova, A. S. Tikhomirov, and G. A. Sharaev, “The selective sensitivity of striate neurons in the cat to cross-like and angular figures of different orientations,”Neirofiziologiya,27, 403–412 (1995).Google Scholar
  5. 5.
    N. A. Lazareva, I. A. Shevelev, G. A. Sharaev, R. V. Novikova, and A. S. Tikhomirov, “The sensitivity of neurons in the cat visual cortex to cross-like figures in conditions of stimulation of the center or periphery of the receptive field,”Zh. Vyssh. Nerv.Deyat.,48, 485–495 (1998).Google Scholar
  6. 6.
    I. A. Shevelev,Visual Cortex Neurons: Adaptivity and Dynamics of Receptive Fields [in Russian], Nauka, Moscow (1984).Google Scholar
  7. 7.
    I. A. Shevelev, U. T. Eysel, K.-U. Irmann, and G. A. Sharaev, “Responses of visual cortex neurons to cross-like figures in conditions of local blockade of inhibition,”Dokl. Ross.Akad. Nauk,363, 137–140 (1998).Google Scholar
  8. 8.
    I. A. Shevelev, U. T. Eysel, K. U. Irmann, and G. A. Sharaev, “Tuning of striate neurons to cross-like figures in conditions of local blockade of intracortical inhibition,”Zh. Vyssh. Nerv. Deyat.,49, 271–278 (1999).Google Scholar
  9. 9.
    I. A. Shevelev, N. A. Lazareva, R. V. Novikova, A. S. Tikhomirov, and G. A. Sharaev, “Tuning of cat visual cortex neurons to the extraction of cross-like figures,”Neirofiziologiya,1, 362–265 (1993).Google Scholar
  10. 10.
    I. A. Shevelev, G. A. Sharaev, N. A. Lazareva R. V. Novikova, and A. S. Tikhomirov, “Double orientational tuning of cat visual cortex neurons,”Neirofiziologiya,15, 459–466 (1983).Google Scholar
  11. 11.
    B. D. Burns and R. Pritchard, “Geometrical illusions and the response of neurones in the cat's visual cortex to angle patterns,”J. Physiol. (London),213, 599–616 (1971).Google Scholar
  12. 12.
    R. H. S. Carpenter and C. Blakemore, “Interactions between orientations in human vision,”Exp. Brain Res.,18, 287–303 (1973).PubMedCrossRefGoogle Scholar
  13. 13.
    S. Chen and D. M. Levi, “Angle judgment. Is the whole the sum of its parts?,”Vision Res.,36, 1721–1735 (1996).PubMedCrossRefGoogle Scholar
  14. 14.
    J. Cudeiro and A. M. Sillito, “Spatial frequency tuning of orientation-discontinuity-sensitive corticofugal feedback to the cat lateral geniculate nucleus,”J. Physiol. (London),490, 481–492 (1996).Google Scholar
  15. 15.
    G. C. DeAngelis, J. G. Robson, I. Ohzawa, and R. D. Freeman, “Organization of suppression in receptive fields of neurons in cat visual cortex,”J. Neurophysiol. 68, 144–163 (1992).PubMedGoogle Scholar
  16. 16.
    R. J. Douglas and K. A. Martin, “A functional microcircuit for cat visual cortex,”J. Physiol. (London),440, 735–769 (1991).Google Scholar
  17. 17.
    E. S. Eriksson, “A field theory of visual illusions,”Brit. J. Psychol.,61, 451–466 (1970).PubMedGoogle Scholar
  18. 18.
    U. T. Eysel, “Lateral inhibitory interactions in area 17 and 18 of the cat visual cortex,”Progr. Brain Res.,90, 407–422 (1992).Google Scholar
  19. 19.
    U. T. Eysel, J. M. Crook, and H. F. Machemer, “GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex,”Exp. Brain Res. 80, 626–630 (1990).PubMedCrossRefGoogle Scholar
  20. 20.
    U. T. Eysel and I. A. Shevelev, “Time-slice analysis of inhibition in cat striate cortex neurones,”NeuroReport,5, 2033–2036 (1994).PubMedGoogle Scholar
  21. 21.
    I. Fujita, K. Tanaka, M. Ito, and K. Cheng, “Columns for visual features of objects in monkey inferotemporal cortex,”Nature,360, 343–346 (1992).PubMedCrossRefGoogle Scholar
  22. 22.
    M. Georgeson, “Human vision combines oriented filters to compute edges,”Proc. Roy. Soc. Lond.,B249, 235–245 (1992).Google Scholar
  23. 23.
    C. D. Gilbert and T. N. Wiesel, “The influence of contextual stimuli on the orientational selectivity of cells in primary visual cortex of the cat,”Vision Res.,30, 1689–1701 (1990).PubMedCrossRefGoogle Scholar
  24. 24.
    M. S. Gizzi, E. Katz, R. A. Schumer, and J. A. Movshon, “Selectivity for orientation and direction of motion of single neurons in cat striate and extrastriate visual cortex,”J. Neurophysiol.,63, 1529–1543 (1990).PubMedGoogle Scholar
  25. 25.
    R. Gray and S. J. Hamstra, “Evidence for a neuronal mechanism that encodes angles,”Vision Res.,36, 323–330 (1996).PubMedCrossRefGoogle Scholar
  26. 26.
    K. L. Grieve and A. M. Sillito, “Length summation in layer VI cells of cat visual cortex and hypercomplex cell inhibitory end zones in the anesthetized cat,”J. Physiol. (London),416, 21–37 (1989).Google Scholar
  27. 27.
    P. Hammond and D. P. Andrews, “Orientation tuning of cells in areas 17 and 18 of the cat's visual cortex,”Exp. Brain Res.,31, 341–351 (1978).PubMedGoogle Scholar
  28. 28.
    D. W. Heeley and H. H. Buchanan-Smith, “Recognition of stimulus orientation,”Vision Res.,30, 1429–1437 (1990).PubMedCrossRefGoogle Scholar
  29. 29.
    P. Heggelund and K. Albus, “Orientation selectivity of single cells of striate cortex of cat: the shape of orientation tuning curves,”Vision Res.,18, 1067–1071 (1978).PubMedCrossRefGoogle Scholar
  30. 30.
    G. H. Henry, “Receptive field classes of cells in the striate cortex of the cat,”Brain Res.,133, 1–28 (1977).PubMedCrossRefGoogle Scholar
  31. 31.
    G. H. Henry, B. Dreher, and P. O. Bishop, “Orientation specificity of cells in cat striate cortex,”J. Neurophysiol.,37, 1394–1409 (1974).PubMedGoogle Scholar
  32. 32.
    D. H. Hubel and T. N. Wiesel, “Receptive fields, binocular interaction and functional architecture in the cat's visual cortex,”J. Physiol. (London),160, 106–154 (1962).Google Scholar
  33. 33.
    D. H. Hubel and T. N. Wiesel, “Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat,”J. Neurophysiol.,28, 229–289 (1965).PubMedCrossRefGoogle Scholar
  34. 34.
    E. Kobatake and K. Tanaka, “Neuronal selectivities to complex objects features in the ventral visual pathway of the macaque cerebral cortex,”J. Neurophysiol.,71, 856–867 (1994).PubMedGoogle Scholar
  35. 35.
    L. Lagae, H. Maes, S. Raiguel, D. K. Xiao, and G. A. Orban, “Responses of macaque STS neurons to optic flow components: a comparison of areas MT and mST,”J. Neurophysiol.,71, 1597–1626 (1994).PubMedGoogle Scholar
  36. 36.
    J. B. Levitt and J. S. Lund, “Contrast dependence of contextual effects in primate visual cortex,”Nature,387, 73–76 (1997).PubMedCrossRefGoogle Scholar
  37. 37.
    D. Marr, “A theory for the cerebral cortex,”Proc. Roy. Soc. Lond.,B176, 161–234 (1970).Google Scholar
  38. 38.
    D. Marr and C. E. Hildreth, “A theory of edge detection,”Proc. Roy. Soc. Lond.,B204, 301–328 (1980).Google Scholar
  39. 39.
    R. Maske, S. Yamane, and P. O. Bishop, “End-stopped cells and binocular depth discrimination in the striate cortex of cats,”Proc. Roy. Soc. Lond.,B229, 257–276 (1986).CrossRefGoogle Scholar
  40. 40.
    M. C. Morrone, D. C. Burr, and H. D. Speed, “Cross-orientation inhibition in cat is GABA mediated,”Exp. Brain Res.,67, 635–644 (1987).PubMedCrossRefGoogle Scholar
  41. 41.
    J. I. Nelson and B. J. Frost, “Orientation-selective inhibition from beyond the classical visual receptive field,”Brain Res.,139, 359–365 (1978).PubMedCrossRefGoogle Scholar
  42. 42.
    J. I. Nelson and B. J. Frost, “Intracortical facilitation among co-oriented, co-axially aligned simple cells in cat striate cortex,”Exp. Brain Res.,61, 54–61 (1985).PubMedCrossRefGoogle Scholar
  43. 43.
    K. Sakai and Y. Miyashita, “Neural organization for the long-term memory of paired associates,”Nature,354, 152–155 (1991).PubMedCrossRefGoogle Scholar
  44. 44.
    I. A. Shevelev, K. U. Jimann, G. A. Sharaev, and U. T. Eysel, “Contribution of GABAergic inhibition to sensitivity to cross-like figures in striate cortex,”NeuroReport,9, 3153–3157.Google Scholar
  45. 45.
    I. A. Shevelev, N. A. Lazareva, R. V. Novikova, A. S. Tikhomirov, and G. A. Sharaev, “Bimodal orientation tuning and detection of crosses and angles in cat visual cortex,”Perception,22S, 138 (1993).Google Scholar
  46. 46.
    I. A. Shevelev, N. A. Lazareva, R. V. Novikova, A. S. Tikhomirov, and G. A. Sharaev, “Double orientation tuning of units in cat visual cortex,”Neurosci.,61, 965–973 (1994).CrossRefGoogle Scholar
  47. 47.
    I. A. Shevelev, N. A. Lazareva, G. A. Sharaev, R. V. Novikova, and A. S. Tikhomirov, “Selective and invariant sensitivity to crosses and corners in cat striate neurons,”Neurosci.,84, 713–721 (1998).CrossRefGoogle Scholar
  48. 48.
    I. A. Shevelev, N. A. Lazareva, G. A. Sharaev, R. V. Novikova, and A. S. Tikhomirov, “Interrelation of tuning characteristics to bar, cross and corner in striate neurons,”Neurosci.,88, 17–25 (1999).CrossRefGoogle Scholar
  49. 49.
    I. A. Shevelev, R. V. Novikova, N. A. Lazareva, A. S. Tikhomirov, and G. A. Sharaev, “Sensitivity to cross-like figures in the cat striate neurons,”Neurosci.,69, 51–57 (1995).CrossRefGoogle Scholar
  50. 50.
    A. M. Sillito, K. L. Grieve, H. E. Jones, J. Cudeiro, and J. Davis, “Visual cortical mechanisms detecting focal orientation discontinuities,”Nature,378, 492–496 (1995).PubMedCrossRefGoogle Scholar
  51. 51.
    T. Tsumoto, W. Eckert, and O. D. Creutzfeldt, “Modification of orientation sensitivity of cat visual cortex neurones by removal of GABA-mediated inhibition,”Exp. Brain Res.,34, 351–363 (1979).PubMedCrossRefGoogle Scholar
  52. 52.
    G. Wallis and E. T. Rolls, “Invariant face and object recognition in the visual system,”Progr. Neurobiol.,51, 167–194 (1997).PubMedCrossRefGoogle Scholar
  53. 53.
    G. Wang, K. Tanaka, and M. Tanifuji, “Optical imaging of functional organization in the monkey inferotemporal cortex,”Science,272, 1665–1668 (1996).PubMedGoogle Scholar

Copyright information

© Kluwer Academic/Plenum Publishers 2000

Authors and Affiliations

  • I. A. Shevelev
    • 1
  1. 1.Laboratory for Analyzer Physiology, Institute of Higher Nervous Activity and NeurophysiologyRussian Academy of SciencesMoscowRussia

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