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Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons

Abstract

Three types of looming-selective neurons have been found in the nucleus rotundus of pigeons, each computing a different optical variable related to image expansion of objects approaching on a direct collision course with the bird. None of these neurons respond to simulated approach toward stationary objects. A detailed analysis of these neurons' firing pattern to approaching objects of different sizes and velocities shows that one group of neurons signals relative rate of expansion τ (tau), a second group signals absolute rate of expansion ρ (rho), and a third group signals yet another optical variable η (eta). The ρ parameter is required for the computation of both τ and η, whose respective ecological functions probably provide precise 'time-to-collision' information and 'early warning' detection for large approaching objects.

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Figure 1: A schematic diagram of a spherical object of diameter d directly approaching an animal's eye (a).
Figure 2: Based on the differences in the time course of the neuronal responses relative to the moment of collision, the looming sensitive neurons in nucleus rotundus have been classified into three distinct classes.
Figure 3: Quantitative examination of the timing of the responses of same three neurons shown in Fig. 2.
Figure 4: Quantitative examination of the timing of the response for the population of nucleus rotundus looming-sensitive neurons when presented with approaching objects that varied in size or velocity.

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References

  1. Gibson, J. J. The Senses Considered as Perceptual Systems (Houghton Mifflin, Boston, 1966).

    Google Scholar 

  2. Gibson, J. J. The Ecological Approach to Visual Perception (Houghton Mifflin, Boston, 1979).

    Google Scholar 

  3. Nakayama, K. & Loomis, J. M. Optical velocity patterns, velocity-sensitive neurons and space perception: a hypothesis. Perception 3, 63–80 (1974).

    Article  CAS  Google Scholar 

  4. Frost, B. J., Wylie, D. R. & Wang, Y.-C. in Perception and Motor Control in Birds (eds Davies, M. N. O. & Green, P. R.) 248–269 (Springer-Verlag, Berlin, 1994).

    Book  Google Scholar 

  5. Longuet-Higgins, H. C. & Prazdny, K. The interpretation of moving retinal image. Proc. R. Soc. Lond. B 206, 358– 397 (1980).

    Google Scholar 

  6. Wylie, D. R., Kripalani, T. & Frost, B. J. Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation. I. Functional organization of neurons discriminating between translational and rotational visual flow. J. Neurophysiol. 70, 2632–2646 (1993).

    Article  CAS  Google Scholar 

  7. Roy, J.-P. & Wurtz, R. H. The role of disparity-sensitive cortical neurons in signalling the direction of self-motion. Nature 348, 160–162 ( 1990).

    Article  CAS  Google Scholar 

  8. Tanaka, K. & Saito, H. Analysis of motion of the visual field by direction, expansion/contraction, and rotation cells clustered in the dorsal part of the medial superior temporal area of the Macaque Monkey. J. Neurophysiol. 62, 626–641 (1989).

    Article  CAS  Google Scholar 

  9. Schiff, W. Perception of impending collision: A study of visually directed avoidant behaviour. Psychol. Monogr. 79, 1–26 (1965).

    Article  Google Scholar 

  10. Dill, L. M. The escape response of the zebra danio (Brachydanio rerio). I. The stimulus for escape. Anim. Behav. 22, 771–722 (1974).

    Google Scholar 

  11. Ingle, D. J. & Shook, B. L. in Brain Mechanisms of Spatial Vision (eds Ingle, D. J., Jeannerod, M. & Lee, D. N.) 229– 258 (Martinus Nijhoft, Dordrecht, 1985).

    Google Scholar 

  12. Hayes, W. N. & Saiff, E. I. Visual alarm reactions in turtles . Anim. Behav. 15, 102– 108 (1967).

    Article  CAS  Google Scholar 

  13. Tronick, E. Approach response of domestic chicks to an optical display. J. Comp. Physiol. Psychol. 64, 529–531 ( 1967).

    Article  CAS  Google Scholar 

  14. Schiff, W., Caviness, J. A. & Gibson, J. J. Persistent fear responses in rhesus monkeys to the optical stimulus of 'looming'. Science 136, 982– 983 (1962).

    Article  CAS  Google Scholar 

  15. Bower, T. G. R., Broughton, J. M. & Moore, M. K. Infant responses to approaching objects: an indicator of response to distal variables. Percept. Psychophys. 9, 193–196 (1970).

    Article  Google Scholar 

  16. Ball, W. & Tronick, E. Infant responses to impending collision . Science 171, 818–820 (1971).

    Article  CAS  Google Scholar 

  17. Lee, D. N. A theory of visual control of braking based on information about time-to-collision. Perception 5, 437–459 ( 1976).

    Article  CAS  Google Scholar 

  18. Lee, D. N. The optic flow field: The foundation of vision. Philos. Trans. R. Soc. Lond. B Biol. Sci. 290, 169–179 (1980).

    Article  CAS  Google Scholar 

  19. Lee, D. N., & Reddish, P. E. Plummeting gannets: a paradigm of ecological optics. Nature 293, 293– 294 (1980).

    Article  Google Scholar 

  20. Lee, D. N., & Reddish, P. E. Visual regulation of gait in long jumping. J. Exp. Psychol. Hum. Percept. Perform. 8, 448–459 (1982).

    Article  Google Scholar 

  21. Sun, H.-J., Carey, D. P. & Goodale, M. A. A mammalian model of optic-flow utilization in the control of locomotion. Exp. Brain Res. 91, 171– 175 (1992).

    Article  CAS  Google Scholar 

  22. Wagner, H. Flow-field variables trigger landing in flies. Nature 297, 147 –148 (1982).

    Article  Google Scholar 

  23. Lee, D. N. & Young, D. S. in Brain Mechanisms and Spatial Vision (eds Ingle, D. J., Jeannerod, M. & Lee, D. N.) 1– 30 (Martinus Nijhoff, Dordrecht, 1985).

    Book  Google Scholar 

  24. Regan, D. & Hamstra, S. J. Dissociation of discrimination thresholds for time to contact and for rate of angular expansion. Vision Res. 33, 447–462 (1993).

    Article  CAS  Google Scholar 

  25. Tresilian, J. R. Four questions of time to contact: A critical examination of research on interceptive timing . Perception 22, 653–680 (1993).

    Article  CAS  Google Scholar 

  26. Wann, J. P. Anticipating arrival: Is the tau margin a specious theory? J. Exp. Psychol. Hum. Percept. Perform. 22, 1031–1048 (1996).

    Article  CAS  Google Scholar 

  27. Rind, F. C. & Simmons, P. J. Orthopteran DCMD neuron: A reevaluation of responses to moving objects. I. Selective responses to approaching objects . J. Neurophysiol. 68, 1654– 1666 (1992).

    Article  CAS  Google Scholar 

  28. Simmons, P. J. & Rind, F. C. Orthopteran DCMD neuron: A reevaluation of responses to moving objects. II. Critical cues for detecting approaching objects. J. Neurophysiol. 68, 1667– 1682 (1992).

    Article  CAS  Google Scholar 

  29. Hatsopoulos, N., Gabbiani, F. & Laurent, G. Elementary computation of object approach by a wide-field visual neuron. Science 270, 1000– 1003 (1995).

    Article  CAS  Google Scholar 

  30. Wang, Y. & Frost, B. J. Time to collision is signalled by neurons in the nucleus rotundus of pigeons. Nature 356, 236–238 (1992).

    Article  CAS  Google Scholar 

  31. Wang, Y. C., Jiang, S. & Frost, B. J. Visual processing in pigeon nucleus rotundus: luminance, colour, motion and looming subdivisions. Visual Neurosci. 10, 21–31 (1993).

    Article  CAS  Google Scholar 

  32. Frost, B. J. & Sun, H.-J. in From Living Eyes to Seeing Machines (eds Srinivasan, M. V. & Venkatesh, S.) 80– 103 (Oxford Univ. Press, Oxford, 1997).

    Google Scholar 

  33. DeLucia, P. R. Pictorial and motion-based information for depth perception. J. Exp. Psychol. Hum. Percept. Perform. 17, 738–748 (1991).

    Article  CAS  Google Scholar 

  34. Robertson, R. M. & Johnson, A. G. Retinal image size triggers obstacle avoidance in flying locusts. Naturwissenschaften 80 , 176–178 (1993).

    Article  Google Scholar 

Download references

Acknowledgements

The authors wish to thank T. Kripalani and S. David for excellent technical assistance and D. Fleet and N. Troje for helpful discussions and comments on the manuscripts. HJS was supported by a Postgraduate Scholarship from the Natural Science and Engineering Research Council (NSERC) of Canada. This work was supported by an NSERC grant OGP0000353 and an Alexander von Humboldt Research Award to BJF.

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Sun, H., Frost, B. Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons. Nat Neurosci 1, 296–303 (1998). https://doi.org/10.1038/1110

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