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Perception and neuronal coding of subjective contours in the owl

Abstract

Robust form perception and underlying neuronal mechanisms require generalized representation of object boundaries, independent of how they are defined. One visual ability essential for form perception is reconstruction of contours absent from the retinal image. Here we show that barn owls perceive subjective contours defined by grating gaps and phase-shifted abutting gratings. Moreover, single-neuron recordings from visual forebrain (visual Wulst) of awake, behaving birds revealed a high proportion of neurons signaling such subjective contours, independent of local stimulus attributes. These data suggest that the visual Wulst is important in contour-based form perception and exhibits a functional complexity analogous to mammalian extrastriate cortex.

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Figure 1: Stimuli used in behavioral tests and corresponding psychophysical performance of two owls.
Figure 2: Responses of visual forebrain neurons to stimuli defined by contrast borders or subjective contours.
Figure 3
Figure 4: Responses to subjective contours in abutting gratings of different line density and spacing.
Figure 5: Mean responses of a total of 13 neurons were unaffected by variable density or spacing of the grating lines.

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References

  1. Kanizsa, G. Organization in Vision. Essays on Gestalt Perception (Praeger, New York, 1979).

    Google Scholar 

  2. Schumann, F. Beitraege zur analyse der gesichtswahrnehmungen. erste abhandlung. einige beobachtungen ueber die zusammenfassung von gesichtseindruecken zu einheiten. Z. Psychol. Physiol. Sinnesorgane 23, 1 –32 (1990).

    Google Scholar 

  3. Petry, S. & Meyer, G. E. The Perception of Illusory Contours (Springer, New York, 1987).

    Book  Google Scholar 

  4. Ramachandran, V. S. in The Perception of Illusory Contours (eds. Petry, S. & Meyer, G. E.) 93–108 (Springer, New York, 1987).

    Book  Google Scholar 

  5. Paradiso, M. A., Shimojo, S. & Nakayama, K. Subjective contours, tilt aftereffects, and visual cortical organization. Vision Res. 29, 1205– 1213 (1989).

    Article  CAS  Google Scholar 

  6. von der Heydt, R. in The Cognitive Neurosciences (ed. Gazzaniga, M. S.) 365–382 (MIT Press, Cambridge, Massachusetts, 1995).

  7. Gregory, R. L. Cognitive contours. Nature 238, 51– 52 (1972).

    Article  CAS  Google Scholar 

  8. Rock, I. & Anson, R. Illusory contours as the solution to a problem. Perception 8, 665– 681 (1979).

    Article  CAS  Google Scholar 

  9. Van Essen, D. C. & DeYoe, E. A. in The Cognitive Neurosciences (ed. Gazzaniga, M. S.) 383–400 (MIT Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

  10. Hubel, D. H. & Wiesel, T. N. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. (Lond.) 195, 215–243 (1968).

    Article  CAS  Google Scholar 

  11. Karten, H. J., Hodos, W., Nauta, W. J. & Revzin, A. M. Neural connections of the 'visual Wulst' of the avian telencephalon. Experimental studies in the pigeon (Columba livia) and owl (Speotyto cunicularia). J. Comp. Neurol. 150, 253–278 (1973).

    Article  CAS  Google Scholar 

  12. Pettigrew, J. D. Binocular visual processing in the owl's telencephalon. Proc. R. Soc. Lond. B Biol. Sci. 204, 435–454 (1979).

    Article  CAS  Google Scholar 

  13. Casini, G., Fontanesi, G. & Bagnoli, P. in Vision, Brain, and Behavior in Birds(eds. Zeigler, H. P. & Bischof, H.-J.) 159–169 (MIT Press, Cambridge, Massachusetts, 1993).

    Google Scholar 

  14. Pettigrew, J. D. in Visual Neuroscience (eds. Pettigrew, J. D., Sanderson, K. J. & Levick, W. R.) 208–222 (Cambridge Univ. Press, Cambridge, 1986).

    Google Scholar 

  15. Shimizu, T., Cox, K. & Karten, H. J. Intratelencephalic projections of the visual Wulst in pigeons (Columba livia). J. Comp. Neurol. 359 , 551–572 (1995).

    Article  CAS  Google Scholar 

  16. Pettigrew, J. D. & Konishi, M. Neurons selective for orientation and binocular disparity in the visual Wulst of the barn owl (Tyto alba). Science 193, 675– 678 (1976).

    Article  CAS  Google Scholar 

  17. Spillmann, L. & Werner, J. S. Long-range interactions in visual perception. Trends Neurosci. 19, 428– 434 (1996).

    Article  CAS  Google Scholar 

  18. Gilbert, C. D., Das, A., Ito, M., Kapadia, M. & Westheimer, G. Spatial integration and cortical dynamics. Proc. Natl. Acad. Sci. USA 93, 615– 622 (1996).

    Article  CAS  Google Scholar 

  19. Shimizu, T. & Karten, H. J. in Vision, Brain, and Behavior in Birds(eds. Zeigler, H. P. & Bischof, H.-J.) 103– 114 (MIT Press, Cambridge, Massachusetts, 1993).

    Google Scholar 

  20. Nieder, A. & Klump, G. M. Adjustable frequency selectivity of auditory forebrain neurons recorded in a freely moving songbird via radiotelemetry. Hear. Res. 127, 41–54 (1999).

    Article  CAS  Google Scholar 

  21. Grosof, D. H., Shapley, R. M. & Hawken, M. J. Macaque V1 neurons can signal 'illusory' contours. Nature 365, 550–552 (1993).

    Article  CAS  Google Scholar 

  22. Peterhans, E. Functional organization of area V2 in the awake monkey. Cereb. Cortex 12, 335–357 ( 1997).

    Article  Google Scholar 

  23. Bravo, M., Blake, R. & Morrison, S. Cats see subjective contours. Vision Res. 28, 861–865 ( 1988).

    Article  CAS  Google Scholar 

  24. De Weerd, P., Vandenbussche, E., De Bruyn, B. & Orban, G. A. Illusory contour orientation discrimination in the cat. Behav. Brain Res. 39, 1–17 ( 1990).

    Article  CAS  Google Scholar 

  25. van Hateren, J. H., Srinivasan, M. V. & Wait, P. B. Pattern recognition in bees: orientation discrimination . J. Comp. Physiol. A 167, 649– 654 (1990).

    Article  Google Scholar 

  26. van der Willigen, R. F., Frost, B. J. & Wagner, H. Stereoscopic depth perception in the owl. Neuroreport 9, 1233–1237 (1998).

    Article  CAS  Google Scholar 

  27. Sheth, B. R., Sharma, J., Rao, S. C. & Sur, M. Orientation maps of subjective contours in visual cortex. Science 274, 2110–2115 (1996).

    Article  CAS  Google Scholar 

  28. von der Heydt, R., Peterhans, E. & Baumgartner, G. Illusory contours and cortical neuron responses. Science 224, 1260–1262 ( 1984).

    Article  CAS  Google Scholar 

  29. von der Heydt, R. & Peterhans, E. Mechanisms of contour perception in monkey visual cortex. I. Lines of pattern discontinuity. J. Neurosci. 9, 1731–1748 (1989).

    Article  CAS  Google Scholar 

  30. Lamme, V. A., Zipser, K. & Spekreijse, H. Figure-ground activity in primary visual cortex is suppressed by anesthesia. Proc. Natl. Acad. Sci. USA 95, 3263–3268 (1998).

    Article  CAS  Google Scholar 

  31. Grossberg, S. & Mingolla, E. in The Perception of Illusory Contours (eds. Petry, S. & Meyer, G. E.) 116–125 (Springer, New York, 1987).

    Book  Google Scholar 

  32. De Weerd, P., Desimone, R. & Ungerleider, L. G. Cue-dependent deficits in grating orientation discrimination after V4 lesions in macaques. Vis. Neurosci. 13, 529–538 (1996).

    Article  CAS  Google Scholar 

  33. Steinbach, M. & Money, K. E. Eye movements of the owl. Vision Res. 13, 889–891 (1973).

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to R. v.d.Willigen for introduction to graphics programming. B. Gaese provided a clocked-sequence program for data collection. We thankB. Gaese and H. Luksch for suggestions on an earlier version of the manuscript and M. Schäfer for help with data analysis. Supported by a grant from the DFG to H.W. (WA 606/6).

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Correspondence to Andreas Nieder.

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Nieder, A., Wagner, H. Perception and neuronal coding of subjective contours in the owl. Nat Neurosci 2, 660–663 (1999). https://doi.org/10.1038/10217

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