Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Segregation of object and background motion in the retina

Nature volume 423, pages 401–408 (2003)Cite this article

Abstract

An important task in vision is to detect objects moving within a stationary scene. During normal viewing this is complicated by the presence of eye movements that continually scan the image across the retina, even during fixation. To detect moving objects, the brain must distinguish local motion within the scene from the global retinal image drift due to fixational eye movements. We have found that this process begins in the retina: a subset of retinal ganglion cells responds to motion in the receptive field centre, but only if the wider surround moves with a different trajectory. This selectivity for differential motion is independent of direction, and can be explained by a model of retinal circuitry that invokes pooling over nonlinear interneurons. The suppression by global image motion is probably mediated by polyaxonal, wide-field amacrine cells with transient responses. We show how a population of ganglion cells selective for differential motion can rapidly flag moving objects, and even segregate multiple moving objects.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Simulating local object motion on the retina in the presence of fixational eye movements.
Figure 2: Certain retinal ganglion cells are selective for object motion.
Figure 3: Spatial interactions that produce the sensitivity to object motion.
Figure 4: Transient excitation and inhibition are synchronous during coherent motion, causing suppression of firing.
Figure 5: The response of OMS cells is largely independent of the spatial pattern.
Figure 6: A model of retinal processing that accounts for differential motion sensitivity.
Figure 7: Pop-out of moving objects in a population of OMS ganglion cells.
Figure 8: A motion illusion revealed by the Japanese artist Ouchi38.

Similar content being viewed by others

References

  1. Yarbus, A. L. Eye Movements and Vision (Plenum, New York, 1967)

    Book  Google Scholar 

  2. Kowler, E. Eye Movements and their Role in Visual and Cognitive Processes (Elsevier, New York, 1990)

    Google Scholar 

  3. Ross, J., Morrone, M. C., Goldberg, M. E. & Burr, D. C. Changes in visual perception at the time of saccades. Trends Neurosci. 24, 113–121 (2001)

    Article  CAS  Google Scholar 

  4. Coppola, D. & Purves, D. The extraordinarily rapid disappearance of entopic images. Proc. Natl Acad. Sci. USA 93, 8001–8004 (1996)

    Article  ADS  CAS  Google Scholar 

  5. Skavenski, A. A., Hansen, R. M., Steinman, R. M. & Winterson, B. J. Quality of retinal image stabilization during small natural and artificial body rotations in man. Vision Res. 19, 675–683 (1979)

    Article  CAS  Google Scholar 

  6. Manteuffel, G., Plasa, L., Sommer, T. J. & Wess, O. Involuntary eye movements in salamanders. Naturwissenschaften 64, 533–534 (1977)

    Article  ADS  CAS  Google Scholar 

  7. Van der Steen, J. & Collewijn, H. Ocular stability in the horizontal, frontal and sagittal planes in the rabbit. Exp. Brain Res. 56, 263–274 (1984)

    Article  CAS  Google Scholar 

  8. Gibson, J. J. The Perception of the Visual World (Houghton Mifflin, Boston, 1950)

    Google Scholar 

  9. Vernon, M. D. The Psychology of Perception (Penguin, Baltimore, Maryland, 1962)

    Google Scholar 

  10. Graham, C. H. in Vision and Visual Perception (ed. Graham, C. H.) 575–588 (Wiley, New York, 1965)

    Google Scholar 

  11. Hammond, P. & Smith, A. T. On the sensitivity of complex cells in feline striate cortex to relative motion. Exp. Brain Res. 47, 457–460 (1982)

    Article  CAS  Google Scholar 

  12. Born, R. T. & Tootell, R. B. Segregation of global and local motion processing in primate middle temporal visual area. Nature 357, 497–499 (1992)

    Article  ADS  CAS  Google Scholar 

  13. Bender, D. B. & Davidson, R. M. Global visual processing in the monkey superior colliculus. Brain Res. 381, 372–375 (1986)

    Article  CAS  Google Scholar 

  14. Sterling, P. & Wickelgren, B. G. Visual receptive fields in the superior colliculus of the cat. J. Neurophysiol. 32, 1–15 (1969)

    Article  CAS  Google Scholar 

  15. Frost, B. J. & Nakayama, K. Single visual neurons code opposing motion independent of direction. Science 220, 744–745 (1983)

    Article  ADS  CAS  Google Scholar 

  16. Steinman, R. M. & Collewijn, H. Binocular retinal image motion during active head rotation. Vision Res. 20, 415–429 (1980)

    Article  CAS  Google Scholar 

  17. Cook, P. B., Lukasiewicz, P. D. & McReynolds, J. S. Action potentials are required for the lateral transmission of glycinergic transient inhibition in the amphibian retina. J. Neurosci. 18, 2301–2308 (1998)

    Article  CAS  Google Scholar 

  18. Werblin, F. S. Lateral interactions at inner plexiform layer of vertebrate retina: antagonistic responses to change. Science 175, 1008–1010 (1972)

    Article  ADS  CAS  Google Scholar 

  19. Enroth-Cugell, C. & Jakiela, H. G. Suppression of cat retinal ganglion cell responses by moving patterns. J. Physiol. 302, 49–72 (1980)

    Article  CAS  Google Scholar 

  20. Passaglia, C. L., Enroth-Cugell, C. & Troy, J. B. Effects of remote stimulation on the mean firing rate of cat retinal ganglion cells. J. Neurosci. 21, 5794–5803 (2001)

    Article  CAS  Google Scholar 

  21. Werblin, F., Maguire, G., Lukasiewicz, P., Eliasof, S. & Wu, S. M. Neural interactions mediating the detection of motion in the retina of the tiger salamander. Visual Neurosci. 1, 317–329 (1988)

    Article  CAS  Google Scholar 

  22. Famiglietti, E. V. Polyaxonal amacrine cells of rabbit retina: size and distribution of PA1 cells. J. Comp. Neurol. 316, 406–421 (1992)

    Article  CAS  Google Scholar 

  23. Volgyi, B., Xin, D., Amarillo, Y. & Bloomfield, S. A. Morphology and physiology of the polyaxonal amacrine cells in the rabbit retina. J. Comp. Neurol. 440, 109–125 (2001)

    Article  CAS  Google Scholar 

  24. Dacey, D. M. Axon-bearing amacrine cells of the macaque monkey retina. J. Comp. Neurol. 284, 275–293 (1989)

    Article  CAS  Google Scholar 

  25. Stafford, D. K. & Dacey, D. M. Physiology of the A1 amacrine: a spiking, axon-bearing interneuron of the macaque monkey retina. Vis. Neurosci. 14, 507–522 (1997)

    Article  CAS  Google Scholar 

  26. Grossman, G. E., Leigh, R. J., Bruce, E. N., Huebner, W. P. & Lanska, D. J. Performance of the human vestibuloocular reflex during locomotion. J. Neurophysiol. 62, 264–272 (1989)

    Article  CAS  Google Scholar 

  27. Hochstein, S. & Shapley, R. M. Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. J. Physiol. 262, 265–284 (1976)

    Article  CAS  Google Scholar 

  28. Shapley, R. M. & Victor, J. D. Nonlinear spatial summation and the contrast gain control of cat retinal ganglion cells. J. Physiol. 290, 141–161 (1979)

    Article  CAS  Google Scholar 

  29. Victor, J. D. & Shapley, R. M. The nonlinear pathway of Y ganglion cells in the cat retina. J. Gen. Physiol. 74, 671–689 (1979)

    Article  CAS  Google Scholar 

  30. Demb, J. B., Zaghloul, K., Haarsma, L. & Sterling, P. Bipolar cells contribute to nonlinear spatial summation in the brisk-transient (Y) ganglion cell in mammalian retina. J. Neurosci. 21, 7447–7454 (2001)

    Article  CAS  Google Scholar 

  31. Wu, S. M., Gao, F. & Maple, B. R. Functional architecture of synapses in the inner retina: segregation of visual signals by stratification of bipolar cell axon terminals. J. Neurosci. 20, 4462–4470 (2000)

    Article  CAS  Google Scholar 

  32. Greschner, M., Bongard, M., Rujan, P. & Ammermuller, J. Retinal ganglion cell synchronization by fixational eye movements improves feature estimation. Nature Neurosci. 5, 341–347 (2002)

    Article  CAS  Google Scholar 

  33. Regan, D. Human Perception of Objects: Early Visual Processing of Spatial Form Defined by Luminance, Color, Texture, Motion, and Binocular Disparity (Sinauer, Sunderland, Massachusetts, 2000)

    Google Scholar 

  34. Singer, W. Neuronal synchrony: a versatile code for the definition of relations? Neuron 24, 49–65 (1999)

    Article  CAS  Google Scholar 

  35. Blakemore, C. & Vital-Durand, F. Organization and post-natal development of the monkey's lateral geniculate nucleus. J. Physiol. 380, 453–491 (1986)

    Article  CAS  Google Scholar 

  36. Kaplan, E. & Shapley, R. M. The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proc. Natl Acad. Sci. USA 83, 2755–2757 (1986)

    Article  ADS  CAS  Google Scholar 

  37. Shapley, R., Kaplan, E. & Soodak, R. Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque. Nature 292, 543–545 (1981)

    Article  ADS  CAS  Google Scholar 

  38. Ouchi, H. Japanese Optical and Geometrical Art (Dover, New York, 1977)

    Google Scholar 

  39. Meister, M., Pine, J. & Baylor, D. A. Multi-neuronal signals from the retina: acquisition and analysis. J. Neurosci. Methods 51, 95–106 (1994)

    Article  CAS  Google Scholar 

  40. Baccus, S. A. & Meister, M. Fast and slow contrast adaptation in retinal circuitry. Neuron 36, 909–919 (2002)

    Article  CAS  Google Scholar 

  41. Warland, D. K., Reinagel, P. & Meister, M. Decoding visual information from a population of retinal ganglion cells. J. Neurophysiol. 78, 2336–2350 (1997)

    Article  CAS  Google Scholar 

  42. DeVries, S. H. Correlated firing in rabbit retinal ganglion cells. J. Neurophysiol. 81, 908–920 (1999)

    Article  CAS  Google Scholar 

  43. Chichilnisky, E. J. A simple white noise analysis of neuronal light responses. Network 12, 199–213 (2001)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank members of the Meister laboratory for advice; P. Cavanagh, F. Engert, V. Murthy and K. Nakayama for comments on the manuscript; and H. van der Steen for providing the eye movement data in Fig. 1b. This work was supported by a grant from NEI (M.M.) and NRSA (S.A.B.).

Author information

Authors and Affiliations

  1. Division of Health Sciences and Technology, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, Massachusetts, 02138, USA

    Bence P. Ölveczky

  2. Program in Neuroscience, Harvard University, 220 Longwood Avenue, Boston, Massachusetts, 02115, USA

    Bence P. Ölveczky

  3. Department of Molecular and Cellular Biology, Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts, 02138, USA

    Stephen A. Baccus & Markus Meister

Authors
  1. Bence P. Ölveczky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen A. Baccus
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Markus Meister
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Markus Meister.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ölveczky, B., Baccus, S. & Meister, M. Segregation of object and background motion in the retina. Nature 423, 401–408 (2003). https://doi.org/10.1038/nature01652

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01652

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing