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Dynamics of neuronal sensitivity in visual cortex and local feature discrimination

Abstract

A striking aspect of natural scenes is that image features such as line orientation are strongly correlated at neighboring spatial locations but not at distant locations. Thus, during the viewing of a scene, eye movements are often accompanied by a change in the orientation structure of the image. How does this behavior influence the discrimination of local features and their encoding by visual cortical neurons? Here we examined the perceived changes in orientation induced by brief exposure to oriented image patterns in monkeys and humans, and then used reverse correlation to investigate dynamic changes in neuronal sensitivity in the primary visual cortex (V1) of behaving monkeys. Whereas brief adaptation to an oriented grating impaired identification of nearby orientations by broadening orientation selectivity and changing the preferred orientation of individual V1 neurons, it actually enhanced the identification of orthogonal orientations by sharpening neuronal selectivity. Hence, successive exposure to image patches of dissimilar spatial structure enhances both the ability to discriminate local features and the encoding of these features by V1 neurons.

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Figure 1: Correlational structure of natural scenes.
Figure 2: Psychophysics of orientation discrimination after brief adaptation.
Figure 3: Temporal dynamics of brief adaptation in V1 neurons.
Figure 4: Population analysis of adaptation-induced dynamics of orientation preference.
Figure 5: Population analysis of adaptation-induced dynamics of orientation selectivity.
Figure 6: Changes in orientation discrimination performance after adaptation.

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References

  1. Attneave, F. Informational aspects of visual processing. Psychol. Rev. 61, 183–193 (1954).

    Article  CAS  Google Scholar 

  2. Coppola, D.M., Purves, H.R., McCoy, A.N. & Purves, D. The distribution of oriented contours in the real world. Proc. Natl. Acad. Sci. USA 95, 4002–4006 (1998).

    Article  CAS  Google Scholar 

  3. van Hateren, J.H. & Ruderman, D.L. Independent component analysis of natural image sequences yields spatio-temporal filters similar to simple cells in primary visual cortex. Proc. R. Soc. Lond. B Biol. Sci. 265, 2315–2320 (1998).

    Article  CAS  Google Scholar 

  4. Simoncelli, E.P. & Olshausen, B.A. Natural image statistics and neural representation. Annu. Rev. Neurosci. 24, 1193–1216 (2001).

    Article  CAS  Google Scholar 

  5. Rossi, A.F., Rittenhouse, C.D. & Paradiso, M.A. The representation of brightness in primary visual cortex. Science 273, 1104–1107 (1996).

    Article  CAS  Google Scholar 

  6. Sceniak, M.P., Ringach, D.L., Hawken, M.J. & Shapley, R. Contrast's effect on spatial summation by macaque V1 neurons. Nat. Neurosci. 2, 733–739 (1999).

    Article  CAS  Google Scholar 

  7. Super, H., Spekreijse, H. & Lamme, V.A. A neural correlate of working memory in the monkey primary visual cortex. Science 293, 120–124 (2001).

    Article  CAS  Google Scholar 

  8. Schoups, A., Vogels, R., Qian, N. & Orban, G. Practising orientation identification improves orientation coding in V1 neurons. Nature 412, 549–553 (2001).

    Article  CAS  Google Scholar 

  9. Field, D.J. Relations between the statistics of natural images and the response properties of cortical cells. J. Opt. Soc. Am. A 4, 2379–2394 (1987).

    Article  CAS  Google Scholar 

  10. Vinje, W.E. & Gallant, J.L. Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287, 1273–1276 (2000).

    Article  CAS  Google Scholar 

  11. Dragoi, V., Turcu, C.M. & Sur, M. Stability of cortical responses and the statistics of natural scenes. Neuron 32, 1181–1192 (2001).

    Article  CAS  Google Scholar 

  12. Tolhurst, D.J., Tadmor, Y. & Chao, T. Amplitude spectra of natural images. Ophthalmic Physiol. Opt. 12, 229–232 (1992).

    Article  CAS  Google Scholar 

  13. Simoncelli, E.P. & Schwartz, O. in Advances in Neural Information Processing Systems Vol. 11 (eds. Kearns, M. S., Solla, S. A. & Cohn, D. A.) (MIT Press, Cambridge, Massachusetts, 1999).

    Google Scholar 

  14. Reinagel, P. & Zador, A.M. Natural scene statistics at the centre of gaze. Network 10, 341–350 (1999).

    Article  CAS  Google Scholar 

  15. Sigman, M., Cecchi, G.A., Gilbert, C.D. & Magnasco, M.O. On a common circle: natural scenes and Gestalt rules. Proc. Natl. Acad. Sci. USA 98, 1935–1940 (2001).

    Article  CAS  Google Scholar 

  16. Geisler, W.S., Perry, J.S., Super, B.J. & Gallogly, D.P. Edge co-occurrence in natural images predicts contour grouping performance. Vision Res. 41, 711–724 (2001).

    Article  CAS  Google Scholar 

  17. Yarbus, A.L. Eye Movement and Vision (Plenum, New York, 1967).

    Book  Google Scholar 

  18. Andrews, T.J. & Coppola, D.M. Idiosyncratic characteristics of saccadic eye movements when viewing different visual environments. Vision Res. 39, 2947–2953 (1999).

    Article  CAS  Google Scholar 

  19. Gallant, J.L., Connor, C.E. & Van Essen, D.C. Neural activity in areas V1, V2 and V4 during free viewing of natural scenes compared to controlled viewing. Neuroreport 9, 2153–2158 (1998).

    Article  CAS  Google Scholar 

  20. Muller, J.R., Metha, A.B., Krauskopf, J. & Lennie, P. Rapid adaptation in visual cortex to the structure of images. Science 285, 1405–1408 (1999).

    Article  CAS  Google Scholar 

  21. Dragoi, V., Sharma, J. & Sur, M. Adaptation-induced plasticity of orientation tuning in adult visual cortex. Neuron 28, 287–298 (2000).

    Article  CAS  Google Scholar 

  22. Barlow, H.B. in Vision: Coding and Efficiency (ed. Blakemore, C.) 363–375 (Cambridge Univ. Press, 1990).

    Google Scholar 

  23. Clifford, C.W., Wyatt, A.M., Arnold, D.H., Smith, S.T. & Wenderoth, P. Orthogonal adaptation improves orientation discrimination. Vision Res. 41, 151–159 (2001).

    Article  CAS  Google Scholar 

  24. Blakemore, C. & Campbell, F.W.J. Adaptation to spatial stimuli. J. Physiol. (Lond.) 200, 11P–13P (1969).

    CAS  Google Scholar 

  25. Carandini, M., Movshon, J.A. & Ferster, D. Pattern adaptation and cross-orientation interactions in the primary visual cortex. Neuropharmacology 37, 501–511 (1998).

    Article  CAS  Google Scholar 

  26. Nelson, S.B. Temporal interactions in the cat visual system. I. Orientation-selective suppression in the visual cortex. J. Neurosci. 11, 344–356 (1991).

    Article  CAS  Google Scholar 

  27. Theunissen, F.E. et al. Estimating spatio-temporal receptive fields of auditory and visual neurons from their responses to natural stimuli. Network 12, 289–316 (2001).

    Article  CAS  Google Scholar 

  28. de Boer, E. & Kuyper, P. IEEE Trans. Biomed. Eng. 15, 169–179 (1968).

    Article  CAS  Google Scholar 

  29. Ringach, D.L., Hawken, M.J. & Shapley, R. Dynamics of orientation tuning in macaque primary visual cortex. Nature 387, 281–284 (1997).

    Article  CAS  Google Scholar 

  30. Mazer, J.A., Vinje, W.E., McDermott, J., Schiller, P.H. & Gallant, J.L. Spatial frequency and orientation tuning dynamics in area V1. Proc. Natl. Acad. Sci. USA 99, 1645–1650 (2002).

    Article  CAS  Google Scholar 

  31. Dragoi, V., Rivadulla, C. & Sur, M. Foci of orientation plasticity in visual cortex. Nature 411, 80–86 (2001).

    Article  CAS  Google Scholar 

  32. Chapman, B., Zahs, K.R. & Stryker, M.P. Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex. J. Neurosci. 11, 1347–1358 (1991).

    Article  CAS  Google Scholar 

  33. Ferster, D. Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. J. Neurosci. 6, 1284–1301 (1986).

    Article  CAS  Google Scholar 

  34. Reid, R.C. & Alonso, J.M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281–284 (1995).

    Article  CAS  Google Scholar 

  35. Douglas, R.J., Koch, C., Mahowald, M., Martin, K.A.C. & Suarez, H.H. Recurrent excitation in neocortical circuits. Science 269, 981–985 (1995).

    Article  CAS  Google Scholar 

  36. 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 

  37. Dragoi, V. & Sur, M. Dynamic properties of recurrent inhibition in primary visual cortex: contrast and orientation dependence of contextual effects. J. Neurophysiol. 83, 1019–1030 (2000).

    Article  CAS  Google Scholar 

  38. Troyer, T.W., Krukowski, A.E., Priebe, N.J. & Miller, K.D. Contrast-invariant orientation tuning in cat visual cortex: thalamocortical input tuning and correlation-based intracortical connectivity. J. Neurosci. 18, 5908–5927 (1998).

    Article  CAS  Google Scholar 

  39. McLaughlin, D., Shapley, R., Shelley, M. & Wielaard, D.J. A neuronal network model of macaque primary visual cortex (V1): orientation selectivity and dynamics in the input layer 4Calpha. Proc. Natl. Acad. Sci. USA 97, 8087–8092 (2000).

    Article  CAS  Google Scholar 

  40. Green, D.M. & Swets, J.A. Signal Detection Theory and Psychophysics (Wiley, New York, 1966).

    Google Scholar 

  41. Sanchez-Vives, M.V., Nowak, L.G. & McCormick, D.A. Membrane mechanisms underlying contrast adaptation in cat area 17 in vivo. J. Neurosci. 20, 4267–4285 (2000).

    Article  CAS  Google Scholar 

  42. Abbott, L.F., Varela, J.A., Sen, K. & Nelson, S.B. Synaptic depression and cortical gain control. Science 275, 220–224 (1997).

    Article  CAS  Google Scholar 

  43. Chance, F.S., Nelson, S.B. & Abbott L.F. Synaptic depression and the temporal response characteristics of V1 cells. J. Neurosci. 18, 4785–4799 (1998).

    Article  CAS  Google Scholar 

  44. Galarreta, M. & Hestrin, S. Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat. Neurosci. 1, 587–594 (1998).

    Article  CAS  Google Scholar 

  45. Varela, J.A., Song, S., Turrigiano, G.G. & Nelson, S.B. Differential depression at excitatory and inhibitory synapses in visual cortex. J. Neurosci. 19, 4293–4304 (1999).

    Article  CAS  Google Scholar 

  46. Rainer, G., Rao, S.C. & Miller, E.K. Prospective coding for objects in primate prefrontal cortex. J. Neurosci. 19, 5493–5505 (1999).

    Article  CAS  Google Scholar 

  47. Wörgötter, F. & Eysel, U.T. Correlations between directional and orientational tuning of cells in cat striate cortex. Exp. Brain Res. 83, 665–669 (1991).

    PubMed  Google Scholar 

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Acknowledgements

Supported by McDonnell-Pew and Merck fellowships to V. D., by an MIT-Riken Neuroscience Center grant to E. K. M. and by an NIH grant to M. S.

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Correspondence to Valentin Dragoi.

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Dragoi, V., Sharma, J., Miller, E. et al. Dynamics of neuronal sensitivity in visual cortex and local feature discrimination. Nat Neurosci 5, 883–891 (2002). https://doi.org/10.1038/nn900

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