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:

Neural synchrony correlates with surface segregation rules

Nature volume 405, pages 685–689 (2000)Cite this article

An Erratum to this article was published on 19 October 2000

Abstract

To analyse an image, the visual system must decompose the scene into its relevant parts. Identifying distinct surfaces is a basic operation in such analysis, and is believed to precede object recognition1,2. Two superimposed gratings moving in different directions (plaid stimuli) may be perceived either as two surfaces, one being transparent and sliding on top of the other (component motion) or as a single pattern whose direction of motion is intermediate to the component vectors (pattern motion)3,4,5,6. The degree of transparency, and hence the perception, can be manipulated by changing only the luminance of the grating intersections7,8,9,10,11,12. Here we show that neurons in two visual cortical areas—A18 and PMLS—synchronize their discharges when responding to contours of the same surface but not when responding to contours belonging to different surfaces. The amplitudes of responses correspond to previously described rate predictions3,13,14,15,16 for component and pattern motion, but, in contrast to synchrony, failed to reflect the transition from component to pattern motion induced by manipulating the degree of transparency. Thus, dynamic changes in synchronization could encode, in a context-dependent way, relations among simultaneous responses to spatially superimposed contours and thereby bias their association with distinct surfaces.

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: Dependence of synchrony on transparency conditions and receptive field (RF) configuration.
Figure 2: Comparison between single gratings and plaids.
Figure 3: Changes in synchrony induced by manipulating the duty cycle of plaid components.
Figure 4: Effect of transparency manipulation on response amplitudes and synchrony.

Similar content being viewed by others

References

  1. Stoner, G. R. & Albright, T. D. The interpretation of visual motion: evidence for surface segmentation mechanisms. Vision Res. 36, 1291–1310 ( 1996).

    Article  CAS  Google Scholar 

  2. Shimojo, S., Silverman, G. H. & Nakayama, K. An occlusion-related mechanism of depth perception based on motion and interocular sequence. Nature 333, 265–268 (1988)

    Article  ADS  CAS  Google Scholar 

  3. Movshon, J. A, Adelson, E. H., Gizzi, M. & Newsome, W. T. in Study Group on Pattern Recognition Mechanisms (eds Chagas, C. Gatass, R. & Gross, C. G.) (Pontifica Academia Scientiarum, Vatican City, 1985).

    Google Scholar 

  4. Adelson, E. H. & Movshon, J. A. Phenomenal coherence of moving visual patterns. Nature 300, 523– 525 (1982).

    Article  ADS  CAS  Google Scholar 

  5. Stoner, G. R., Albright, T. D. & Ramachandran, V. S. Transparency and coherence in human motion perception. Nature 344, 153–155 (1990)

    Article  ADS  CAS  Google Scholar 

  6. Smith, A. T. & Harris, L. R. Use of plaid patterns to distinguish the corticofugal and direct retinal inputs to the brainstem optokinetic nystagmus generator. Exp. Brain Res. 86, 324– 332 (1991).

    CAS  PubMed  Google Scholar 

  7. Metelli, F. The perception of transparency. Sci. Am. 230, 90–98 (1974).

    Article  CAS  Google Scholar 

  8. Beck, J. & Ivry, R. On the role of figural organization in perceptual transparency. Percept. Psychophys. 44 , 585–594 (1988).

    Article  CAS  Google Scholar 

  9. Albright, T. D. & Stoner, G. R. Visual motion perception. Proc. Natl Acad. Sci. USA 92, 2433–2440 (1995).

    Article  ADS  CAS  Google Scholar 

  10. Stoner, G. R. & Albright T. D. Luminance contrast affects motion coherency in plaid patterns by acting as depth from occlusion cue. Vision Res. 38, 387–401 (1998).

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  12. Castelo-Branco, M. et al. MT/MST activation depends on the interpretation of stimuli: a functional fMRI study of the perception of plaids. Soc. Neurosci. Abstr. 23, 460 (1997).

    Google Scholar 

  13. 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 

  14. Gizzi, M. S., Katz, E., Schumer, R. A. & Movshon, J. A. Selectivity for orientation and direction of motion of single neurons in cat striate and extrastriate visual cortex. J. Neurophysiol. 63, 1529–1543 (1990).

    Article  CAS  Google Scholar 

  15. Scannell, J. W. et al. Visual motion processing in the anterior ectosylvian sulcus of the cat. J. Neurophysiol. 76, 895 –907 (1996).

    Article  CAS  Google Scholar 

  16. Merabet, L., Desautels, A., Minville, K. & Casanova, C. Motion integration in a thalamic visual nucleus. Nature 396, 265–268 (1998).

    Article  ADS  CAS  Google Scholar 

  17. Gray, C. M., Konig, P., Engel, A. K. & Singer, W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338, 334–337 (1989).

    Article  ADS  CAS  Google Scholar 

  18. Engel, A. K., Konig, P., Kreiter, A. K. & Singer, W. Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex. Science 252, 1177– 1179 (1991).

    Article  ADS  CAS  Google Scholar 

  19. Freiwald, W. A., Kreiter, A. K. & Singer, W. Stimulus dependent intercolumnar synchronization of single unit responses in cat area 17. NeuroReport 6 , 2348–2352 (1995).

    Article  CAS  Google Scholar 

  20. Kreiter, A. K. & Singer, W. Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey. J. Neurosci. 16, 2381– 2396 (1996).

    Article  CAS  Google Scholar 

  21. Brecht, M., Singer, W. & Engel, A. K. Correlation analysis of corticotectal interactions in the cat visual system. J. Neurophysiol. 79, 2394–2407 (1998).

    Article  CAS  Google Scholar 

  22. Brecht, M., Singer, W. & Engel, A. K. Collicular saccade vectors defined by synchronization. Soc. Neurosci. Abstr. 23, 843 (1997).

    Google Scholar 

  23. Castelo-Branco, M., Neuenschwander, S. & Singer, W. Synchronization of visual responses between the cortex, lateral geniculate nucleus, and retina in the anesthetized cat. J. Neurosci. 18, 6395–6410 (1998).

    Article  CAS  Google Scholar 

  24. Palmer, L. A., Rosenquist, A. C. & Tusa, R. J. The retinotopic organization of lateral suprasylvian visual areas in the cat. J. Comp. Neurol. 177, 237–256 (1978).

    Article  CAS  Google Scholar 

  25. Perkel, D. H., Gerstein, G. L. & Moore, G. P. Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophys. J. 7, 419–440 (1967).

    Article  CAS  Google Scholar 

  26. König, P. A method for the quantification of synchrony and oscillatory properties of neuronal activity. J. Neurosci. Methods 54, 31–37 (1994).

    Article  Google Scholar 

  27. Edwards, A. L. Multiple Regression Analysis and the Analysis of Variance and Covariance (W. H. Freeman, New York, 1985).

    MATH  Google Scholar 

  28. Batschelet, E. Circular Statistics in Biology (Academic, London, 1993 ).

    MATH  Google Scholar 

  29. Swindale, N. V. Orientation tuning curves: empirical description and estimation of parameters. Biol. Cybern. 78, 45–56 (1998).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank H. Klon-Lipok, P. Janson and S. Grimm for their technical assistance in electrode manufacture and histology. This research was sponsored by the Max-Planck-Gesellschaft. M.C.-B. was partially supported by the Gulbenkian Foundation and Programa Praxis, Portugal.

Author information

Authors and Affiliations

  1. Max-Planck-Institut für Hirnforschung, Deutschordenstraße 46, Frankfurt am Main, 60528, Germany

    Miguel Castelo-Branco, Rainer Goebel, Sergio Neuenschwander & Wolf Singer

Authors
  1. Miguel Castelo-Branco
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rainer Goebel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sergio Neuenschwander
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wolf Singer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wolf Singer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Castelo-Branco, M., Goebel, R., Neuenschwander, S. et al. Neural synchrony correlates with surface segregation rules. Nature 405, 685–689 (2000). https://doi.org/10.1038/35015079

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35015079

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