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.

  • Letter
  • Published:

Temporal dynamics of a neural solution to the aperture problem in visual area MT of macaque brain

Nature volume 409, pages 1040–1042 (2001)Cite this article

Abstract

A critical step in the interpretation of the visual world is the integration of the various local motion signals generated by moving objects. This process is complicated by the fact that local velocity measurements can differ depending on contour orientation and spatial position. Specifically, any local motion detector can measure only the component of motion perpendicular to a contour that extends beyond its field of view1,2. This “aperture problem”3 is particularly relevant to direction-selective neurons early in the visual pathways, where small receptive fields permit only a limited view of a moving object. Here we show that neurons in the middle temporal visual area (known as MT or V5) of the macaque brain reveal a dynamic solution to the aperture problem. MT neurons initially respond primarily to the component of motion perpendicular to a contour's orientation, but over a period of approximately 60 ms the responses gradually shift to encode the true stimulus direction, regardless of orientation. We also report a behavioural correlate of these neural responses: the initial velocity of pursuit eye movements deviates in a direction perpendicular to local contour orientation, suggesting that the earliest neural responses influence the oculomotor response.

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: The aperture problem.
Figure 2: Evolution of direction tuning.
Figure 3: Visual tracking of an orientated bar.

Similar content being viewed by others

References

  1. Wallach, H. Uber visuell wahrgenommene Bewegungsrichtung. Psychol. Forsch. 20, 325–380 (1935).

    Article  Google Scholar 

  2. Wuerger, S., Shapley, R. & Rubin, N. “On the visually perceived direction of motion,” by Hans Wallach: 60 years later. Perception 11, 1317–1367 (1996).

    Article  Google Scholar 

  3. Marr, D. & Ullman, S. Directional selectivity and its use in early visual processing. Proc. R. Soc. Lond. B. 211, 151–180 (1981).

    Article  ADS  CAS  Google Scholar 

  4. Movshon, J. A. & Newsome, W. T. Visual response properties of striate cortical neurons projecting to area MT in macaque monkeys. J. Neurosci. 16, 7733–7741 (1996).

    Article  CAS  Google Scholar 

  5. Movshon, J. A., Adelson, E. H., Gizzi, M. S. & Newsome, W. T. The analysis of moving visual patterns. Exp. Brain Res. Suppl. 11, 117–151 (1986).

    Article  Google Scholar 

  6. Rodman, H. R. & Albright, T. D. Single-unit analysis of pattern-motion selective properties in the middle temporal visual area (MT). Exp. Brain Res. 75, 53–64 (1989).

    Article  CAS  Google Scholar 

  7. Stoner, G. R. & Albright, T. D. Neural correlates of perceptual motion coherence. Nature 358, 412–414 (1992).

    Article  ADS  CAS  Google Scholar 

  8. Albright, T. D. & Desimone, R. Local precision of visuotopic organization in the middle temporal area (MT) of the macaque. Exp. Brain Res. 65, 582–592 (1987).

    Article  CAS  Google Scholar 

  9. Maunsell, J. H. & Van Essen, D. C. Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J. Neurophysiol. 49, 1127–1147 (1983).

    Article  CAS  Google Scholar 

  10. Albright, T. D. Direction and orientation selectivity of neurons in visual area MT of the macaque. J. Neurophysiol. 52, 1106–1130 (1984).

    Article  CAS  Google Scholar 

  11. Pack, C. C. & Born, R. T. Latency of direction tuning in cortical area MT of alert macaque. Soc. Neurosci. Abstr. 25, 673 (1999).

    Google Scholar 

  12. Newsome, W. T., Wurtz, R. H., Dürsteler, M. R. & Mikami, A. Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey. J. Neurosci. 5, 825–840 (1985).

    Article  CAS  Google Scholar 

  13. Groh, J. M., Born, R. T. & Newsome, W. T. How is a sensory map read out? Effects of microstimulation in visual area MT on saccades and smooth pursuit eye movements. J. Neurosci. 17, 4312–4330 (1997).

    Article  CAS  Google Scholar 

  14. Lisberger, S. G. & Movshon, J. A. Visual motion analysis for pursuit eye movements in area MT of macaque monkeys. J. Neurosci. 19, 2224–2246 (1999).

    Article  CAS  Google Scholar 

  15. Krauzlis, R. J. & Lisberger, S. G. Temporal properties of visual motion signals for the initiation of smooth pursuit eye movements in monkeys. J. Neurophysiol. 72, 150–162 (1994).

    Article  CAS  Google Scholar 

  16. Robinson, D. A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans. Biomed. Eng. 10, 137–145 (1963).

    CAS  Google Scholar 

  17. Lorençeau, J., Shiffrar, M., Wells, N. & Castet, E. Different motion sensitive units are involved in recovering the direction of moving lines. Vision Res. 33, 1207–1217 (1993).

    Article  Google Scholar 

  18. Yo, C. & Wilson, H. R. Perceived direction of moving two-dimensional patterns depends on duration, contrast and eccentricity. Vision Res. 32, 135–147 (1992).

    Article  CAS  Google Scholar 

  19. Masson, G. S., Rybarczyk, Y., Castet, E. & Mestre, D. R. Temporal dynamics of motion integration for the initiation of tracking eye movements at ultra-short latencies. Vis. Neurosci. 17, 753–767 (2000).

    Article  CAS  Google Scholar 

  20. Beutter B. R. & Stone, L. S. Human motion perception and smooth eye movements show similar directional biases for elongated apertures. Vision Res. 38, 1273–1286 (1998).

    Article  Google Scholar 

  21. Hildreth, E. C. The Measurement of Visual Motion (MIT Press, Cambridge, Massachusetts, 1984).

    MATH  Google Scholar 

  22. Watanabe, T. & Cole, R. Propagation of local motion correspondence. Vision Res. 35, 2853–2861 (1995).

    Article  CAS  Google Scholar 

  23. Lidèn, L. H. & Pack, C. C. The role of terminators and occlusion cues in motion integration and segmentation: A neural network model. Vision Res. 39, 3301–3320 (1999).

    Article  Google Scholar 

  24. Chey, J., Grossberg, S. & Mingolla, E. Neural dynamics of motion grouping: From aperture ambiguity to object speed and direction. J. Opt. Soc. Am. 14, 2570–2594 (1997).

    Article  ADS  Google Scholar 

  25. Wilson, H. R., Ferrera V. P. & Yo, C. A psychophysically motivated model for two-dimensional motion perception. Vis. Neurosci. 1, 79–97 (1992).

    Article  Google Scholar 

  26. Duncan, R. O., Albright, T. D. & Stoner, G. R. Occlusion and the interpretation of visual motion: perceptual and neuronal effects of context. J. Neurosci. 20, 5885–5897 (2000).

    Article  CAS  Google Scholar 

  27. Born, R. T., Groh, J. M., Zhao, R. & Lukasewycz, S. J. Segregation of object and background motion in visual area MT: effects of microstimulation on eye movements. Neuron 26, 725–734 (2000).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank P. Abrams for technical assistance, and J. Assad and T. Watanabe for comments on a previous version of the manuscript. This work was supported by a McDonnell-Pew Cognitive Neuroscience grant to C.C.P., and grants from NIH/NEI and The Giovanni Armenise-Harvard Foundation for Scientific Research to R.T.B.

Author information

Authors and Affiliations

  1. Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, 02115, Massachusetts, USA

    Christopher C. Pack & Richard T. Born

Authors
  1. Christopher C. Pack
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard T. Born
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christopher C. Pack.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pack, C., Born, R. Temporal dynamics of a neural solution to the aperture problem in visual area MT of macaque brain. Nature 409, 1040–1042 (2001). https://doi.org/10.1038/35059085

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35059085

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