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:

Electrical microstimulation of cortical area MST biases heading perception in monkeys

Nature Neuroscience volume 1, pages 59–63 (1998)Cite this article

Abstract

As we move through the environment, the pattern of visual motion on the retina provides rich information about our movement through the scene. Human subjects can use this information, often termed "optic flow", to accurately estimate their direction of self movement (heading) from relatively sparse displays. Physiological observations on the motion-sensitive areas of monkey visual cortex suggest that the medial superior temporal area (MST) is well suited for the analysis of optic flow information. To test whether MST is involved in extracting heading from optic flow, we perturbed its activity in monkeys trained on a heading discrimination task. Electrical microstimulation of MST frequently biased the monkeys' decisions about their heading, and these induced biases were often quite large. This result suggests that MST has a direct role in the perception of heading from optic flow.

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: Stimulus geometry and timing.
Figure 2: Example data from a single MST microstimulation experiment.
Figure 3: Histograms showing the shifts of the psychometric functions for all of the 67 experiments in the sample, signed according to the preference of the neurons at the stimulation site.
Figure 4: Interaction between pursuit and microstimulation effect.

Similar content being viewed by others

References

  1. Gibson, J. J. Perception of the visual world (Houghton-Mifflin, Boston, 1950 )

    Google Scholar 

  2. Koenderink, J. J. & van Doorn, A.J. Facts on optic flow. Biol. Cybern. 56, 247–254 (1987)

    Article  CAS  Google Scholar 

  3. Van den Berg, A. V. Judgements of heading. Vision Res. 36, 2337– 2350 (1996)

    Article  CAS  Google Scholar 

  4. Saito, H., Yukie . et al. Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey. J. Neurosci. 6, 145–157 (1986)

    Article  CAS  Google Scholar 

  5. Tanaka, K. et al. Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey. J. Neurosci. 6, 134– 144 (1986)

    Article  CAS  Google Scholar 

  6. Tanaka, K., Fukada, Y. & Saito, H. Underlying mechanisms of the response specificity of expansion/contraction and rotation cells in the dorsal part of the medial superior temporal area of the macaque monkey. J. Neurophysiol. 62, 642–656 (1989)

    Article  CAS  Google Scholar 

  7. 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 

  8. Duffy, C. J. & Wurtz, R.H. Sensitivity of MST neurons to optic flow stimuli. I.A continuum of response selectivity of large-field stimuli . J. Neurophysiol. 65, 1329– 1345 (1991)

    Article  CAS  Google Scholar 

  9. Graziano, M. S., Andersen, R.A. & Snowden, R.J. Tuning of MST neurons to spiral motions. J. Neurosci. 14, 54–67 (1994)

    Article  CAS  Google Scholar 

  10. Lagae, L., Raiguel, S. & Orban, G.A. Speed and direction selectivity of macaque middle temporal neurons. J. Neurophys. 69, 19–39 (1993)

    Article  CAS  Google Scholar 

  11. Lagae, L., Maes, H., Raiguel, S., Xiao, D.K. & Orban, G.A. Responses of macaque STS neurons to optic flow components: a comparison of MT and MST. J. Neurophysiol. 71, 1597–1626 (1994)

    Article  CAS  Google Scholar 

  12. Duffy, C. J. & Wurtz, R.H. Response of monkey MST neurons to optic flow stimuli with shifted centers of motion. J. Neurosci. 15, 5192–5208 (1995)

    Article  CAS  Google Scholar 

  13. Duffy, C. J. & Wurtz, R.H. Planar directional contributions to optic flow responses in MST neurons. J. Neurophys. 77, 782–796 (1997)

    Article  CAS  Google Scholar 

  14. Bradley, D. C., Maxwell, M., Andersen, R.A., Banks, M.S. & Shenoy, K.V. Mechanisms of heading perception in primate visual cortex. Science 273, 1544 –1547 (1996)

    Article  CAS  Google Scholar 

  15. Doty, R. W. Electrical stimulation of the brain in behavioral context. Ann. Rev. Psychol. 20, 289–320 (1969)

    Article  CAS  Google Scholar 

  16. Schmidt, E. M. et al. Feasibility of a visual prosthesis for the blind based on intracortical microstimulation of the visual cortex. Brain 119, 507– 522 (1996)

    Article  Google Scholar 

  17. Salzman, C. D., Murasugi, C.M., Britten, K.H. & Newsome, W.T. Microstimulation in visual area MT: Effects on direction discrimination performance . J. Neurosci. 12, 2331– 2355 (1992)

    Article  CAS  Google Scholar 

  18. Celebrini, S. & Newsome, W.T. Microstimulation of extrastriate area MST influences performance on a direction discrimination task. J. Neurophys. 73, 437–448 (1995)

    Article  CAS  Google Scholar 

  19. Britten, K. H. Clustering of response selectivity in the medial superior temporal area of extrastriate cortex of the macaque monkey. Visual Neuroscience in press (1998)

  20. Banks, M. S., Erlich, S. M., Backus, B. T. & Crowell, J. A. Estimating heading during real and simulated eye movements. Vision Res. 36, 431–443 (1996)

    Article  CAS  Google Scholar 

  21. Warren, W. H. & Hannon, D. J. Eye movements and optical flow . J. Opt. Soc. Am. A 7, 160– 169 (1990)

    Article  Google Scholar 

  22. Royden, C. S., Crowell, J. A. & Banks, M. S. Estimating heading during eye movements. Vision Res. 34, 3197–3214 (1994)

    Article  CAS  Google Scholar 

  23. Newsome, W. T., Wurtz, R. H. & Komatsu, H. Relation of cortical areas MT and MST to pursuit eye movements. II.Differentiation of retinal from extraretinal inputs. J. Neurophysiol. 60, 604–620 (1988)

    Article  CAS  Google Scholar 

  24. Bremmer, S., Ilg, U. J., Thiele, A., Distler, C. & Hoffman, K. P. Eye position effects in monkey cortex. I.Visual and pursuit-related activity in extrastriate areas MT and MST. J. Neurophys. 77, 944–961 (1997)

    Article  CAS  Google Scholar 

  25. Squatrito, S. & Maioli, M. G. Encoding of smooth pursuit direction and eye position by neurons of area MSTd of macaque monkey. J. Neurosci. 17, 3847–3860 (1997)

    Article  CAS  Google Scholar 

  26. Geesaman, B. J., Born, R. T., Andersen, R. A. & Tootell, R. B. H. Maps of complex motion selectivity in the superior temporal sulcus of the alert macaque monkey: a double-label 2-deoxyglucose study. Cerebral Cortex 7, 749–757 (1997)

    Article  CAS  Google Scholar 

  27. Murasugi, C. M., Salzman, C. D. & Newsome, W. T. Microstimulation in visual area MT: effects of varying pulse amplitude and frequency. J. Neurosci. 13, 1719–1729 (1993)

    Article  CAS  Google Scholar 

  28. Quick, R. F. A vector magnitude model of contrast detection. Kybernetik 16, 65–67 (1974)

    Article  Google Scholar 

  29. Rieger, J. H. & Lawton, D. T. Processing differential image motion . J. Opt. Soc. Am. A 2, 354– 359 (1985)

    Article  CAS  Google Scholar 

  30. Heeger, D. J. & Jepson, A. D. Subspace methods for recovering rigid motion I: algorithm and implementation. Int. J. Comp. Vis. 7, 95–117 (1992)

    Article  Google Scholar 

  31. Perrone, J. A. & Stone, L. S. A model of self-motion estimation within primate extrastriate visual cortex. Vision Res. 34, 2917–2938 (1994)

    Article  CAS  Google Scholar 

  32. Royden, C. S., Banks, M. S. & Crowell, J.A. The perception of heading during eye movements. Nature 360, 583–585 (1992)

    Article  CAS  Google Scholar 

  33. Komatsu, H. & Wurtz, R. H. Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. J. Neurophysiol. 62, 31–47 (1989)

    Article  CAS  Google Scholar 

  34. Judge, S. J., Richmond, B. J. & Chu, F. C. Implantation of magnetic search coils for measurement of eye position: An improved method. Vision Res. 20, 535– 538 (1980)

    Article  CAS  Google Scholar 

  35. Celebrini, S. & Newsome, W. T. Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey. J. Neurosci. 14, 4109–4124 (1994)

    Article  CAS  Google Scholar 

  36. Hoel, P., Port, S. & Stone, C. Introduction to statistical theory. (Houghton Mifflin, Boston, 1971)

    Google Scholar 

Download references

Acknowledgements

The authors wish to thank Elizabeth Disbrow, Ryen Tarbet, and Jesse Moore for skilled technical assistance. We also thank M.S. Banks for consultation on the design of stimuli, and Arthur Jones for expert computer programming. Finally, we acknowledge Sylvia Elfar, Hilary Heuer, Steve Lisberger, Brian Mulloney, and Kristy Nace for reading earlier versions of the manuscript. This work was supported by National Eye Institute grant EY10562 to KHB, and RvW was supported in part by the Netherlands Organization for Scientific Research (NWO).

Author information

Authors and Affiliations

  1. UC Davis Center for Neuroscience, 1544 Newton Court, Davis, 95616, California, USA

    Kenneth H. Britten & Richard J. A. van Wezel

  2. Section of Neurobiology, Physiology and Behavior, 1544 Newton Court, Davis, 95616, California, USA

    Kenneth H. Britten

  3. Department of Comparative Physiology, Utrecht University, Utrecht, The Netherlands

    Richard J. A. van Wezel

Authors
  1. Kenneth H. Britten
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard J. A. van Wezel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kenneth H. Britten.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Britten, K., van Wezel, R. Electrical microstimulation of cortical area MST biases heading perception in monkeys. Nat Neurosci 1, 59–63 (1998). https://doi.org/10.1038/259

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/259

This article is cited by

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