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Disparity- and velocity-based signals for three-dimensional motion perception in human MT+

Nature Neuroscience volume 12, pages 1050–1055 (2009)Cite this article

Abstract

How does the primate visual system encode three-dimensional motion? The macaque middle temporal area (MT) and the human MT complex (MT+) have well-established sensitivity to two-dimensional frontoparallel motion and static disparity. However, evidence for sensitivity to three-dimensional motion has remained elusive. We found that human MT+ encodes two binocular cues to three-dimensional motion: changing disparities over time and interocular comparisons of retinal velocities. By varying important properties of moving dot displays, we distinguished these three-dimensional motion signals from their constituents, instantaneous binocular disparity and monocular retinal motion. An adaptation experiment confirmed direction selectivity for three-dimensional motion. Our results indicate that MT+ carries critical binocular signals for three-dimensional motion processing, revealing an important and previously overlooked role for this well-studied brain area.

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Figure 1: Stimuli and results for Experiment 1.
Figure 2: Stimuli and results for Experiment 2.
Figure 3: Stimuli and results for Experiment 3.
Figure 4: Stimuli and results for Experiment 4.

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References

  1. Born, R.T. & Bradley, D.C. Structure and function of visual area MT. Annu. Rev. Neurosci. 28, 157–189 (2005).

    Article  CAS  Google Scholar 

  2. Cumming, B.G. & DeAngelis, G.C. The physiology of stereopsis. Annu. Rev. Neurosci. 24, 203–238 (2001).

    Article  CAS  Google Scholar 

  3. DeAngelis, G.C. & Newsome, W.T. Organization of disparity-selective neurons in macaque area MT. J. Neurosci. 19, 1398–1415 (1999).

    Article  CAS  Google Scholar 

  4. Huk, A.C., Dougherty, R.F. & Heeger, D.J. Retinotopy and functional subdivision of human areas MT and MST. J. Neurosci. 22, 7195–7205 (2002).

    Article  CAS  Google Scholar 

  5. Maunsell, J.H. & Van Essen, D.C. Functional properties of neurons in middle temporal visual area of the macaque monkey. II. Binocular interactions and sensitivity to binocular disparity. J. Neurophysiol. 49, 1148–1167 (1983).

    Article  CAS  Google Scholar 

  6. 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 

  7. DeAngelis, G.C. & Newsome, W.T. Perceptual “read-out” of conjoined direction and disparity maps in extrastriate area MT. PLoS Biol. 2, e77 (2004).

    Article  Google Scholar 

  8. Nguyenkim, J.D. & DeAngelis, G.C. Disparity-based coding of three-dimensional surface orientation by macaque middle temporal neurons. J. Neurosci. 23, 7117–7128 (2003).

    Article  CAS  Google Scholar 

  9. Smith, A.T. & Wall, M.B. Sensitivity of human visual cortical areas to the stereoscopic depth of a moving stimulus. J. Vis. 8, 1–12 (2008).

    Article  Google Scholar 

  10. Julesz, B. Foundations of Cyclopean Perception (The University of Chicago Press, Chicago, 1971).

    Google Scholar 

  11. Cumming, B.G. & Parker, A.J. Binocular mechanisms for detecting motion-in-depth. Vision Res. 34, 483–495 (1994).

    Article  CAS  Google Scholar 

  12. Brooks, K.R. Interocular velocity difference contributes to stereomotion speed perception. J. Vis. 2, 218–231 (2002).

    Article  Google Scholar 

  13. Harris, J.M. & Rushton, S.K. Poor visibility of motion in depth is due to early motion averaging. Vision Res. 43, 385–392 (2003).

    Article  Google Scholar 

  14. Rokers, B., Cormack, L.K. & Huk, A.C. Strong percepts of motion through depth without strong percepts of position in depth. J. Vis. 8, 1–10 (2008).

    Article  Google Scholar 

  15. Fernandez, J.M. & Farell, B. Motion in depth from interocular velocity differences revealed by differential motion aftereffect. Vision Res. 46, 1307–1317 (2006).

    Article  Google Scholar 

  16. Beverley, K.I. & Regan, D. Evidence for the existence of neural mechanisms selectively sensitive to the direction of movement in space. J. Physiol. (Lond.) 235, 17–29 (1973).

    Article  CAS  Google Scholar 

  17. Shioiri, S., Saisho, H., & Yaguchi, H. Motion in depth based on inter-ocular velocity differences. Vision Res. 40, 2565–2572 (2000).

    Article  CAS  Google Scholar 

  18. Heeger, D.J., Boynton, G.M., Demb, J.B., Seidemann, E. & Newsome, W.T. Motion opponency in visual cortex. J. Neurosci. 19, 7162–7174 (1999).

    Article  CAS  Google Scholar 

  19. Qian, N., Andersen, R.A. & Adelson, E.H. Transparent motion perception as detection of unbalanced motion signals. I. Psychophysics. J. Neurosci. 14, 7357–7366 (1994).

    Article  CAS  Google Scholar 

  20. Likova, L.T. & Tyler, C.W. Stereomotion processing in the human occipital cortex. Neuroimage 38, 293–305 (2007).

    Article  Google Scholar 

  21. Norcia, A.M. & Tyler, C.W. Temporal frequency limits for stereoscopic apparent motion processes. Vision Res. 24, 395–401 (1984).

    Article  CAS  Google Scholar 

  22. Cumming, B.G. & Parker, A.J. Responses of primary visual cortical neurons to binocular disparity without depth perception. Nature 389, 280–283 (1997).

    Article  CAS  Google Scholar 

  23. Bridge, H. & Parker, A.J. Topographical representation of binocular depth in the human visual cortex using fMRI. J Vis 7, 1–14 (2007).

    Article  Google Scholar 

  24. Bradley, D.C., Qian, N. & Andersen, R.A. Integration of motion and stereopsis in middle temporal cortical area of macaques. Nature 373, 609–611 (1995).

    Article  CAS  Google Scholar 

  25. Dodd, J.V., Krug, K., Cumming, B.G. & Parker, A.J. Perceptually bistable three-dimensional figures evoke high choice probabilities in cortical area MT. J. Neurosci. 21, 4809–4821 (2001).

    Article  CAS  Google Scholar 

  26. Akase, E., Inokawa, H. & Toyama, K. Neuronal responsiveness to three-dimensional motion in cat posteromedial lateral suprasylvian cortex. Exp. Brain Res. 122, 214–226 (1998).

    Article  CAS  Google Scholar 

  27. Toyama, K., Komatsu, Y., Kasai, H., Fujii, K. & Umetani, K. Responsiveness of Clare-Bishop neurons to visual cues associated with motion of a visual stimulus in three-dimensional space. Vision Res. 25, 407–414 (1985).

    Article  CAS  Google Scholar 

  28. Cynader, M. & Regan, D. Neurons in cat visual cortex tuned to the direction of motion in depth: effect of positional disparity. Vision Res. 22, 967–982 (1982).

    Article  CAS  Google Scholar 

  29. Zeki, S.M. Cells responding to changing image size and disparity in the cortex of the rhesus monkey. J. Physiol. (Lond.) 242, 827–841 (1974).

    Article  CAS  Google Scholar 

  30. Poggio, G.F. & Talbot, W.H. Mechanisms of static and dynamic stereopsis in foveal cortex of the rhesus monkey. J. Physiol. (Lond.) 315, 469–492 (1981).

    Article  CAS  Google Scholar 

  31. Regan, D. & Cynader, M. Neurons in cat visual cortex tuned to the direction of motion in depth: effect of stimulus speed. Invest. Ophthalmol. Vis. Sci. 22, 535–550 (1982).

    CAS  PubMed  Google Scholar 

  32. Nadler, J.W., Angelaki, D.E. & DeAngelis, G.C. A neural representation of depth from motion parallax in macaque visual cortex. Nature 452, 642–645 (2008).

    Article  CAS  Google Scholar 

  33. Orban, G.A., Sunaert, S., Todd, J.T., Van Hecke, P. & Marchal, G. Human cortical regions involved in extracting depth from motion. Neuron 24, 929–940 (1999).

    Article  CAS  Google Scholar 

  34. Ponce, C.R., Lomber, S.G. & Born, R.T. Integrating motion and depth via parallel pathways. Nat. Neurosci. 11, 216–223 (2008).

    Article  CAS  Google Scholar 

  35. Barlow, H.B., Blakemore, C. & Pettigrew, J.D. The neural mechanism of binocular depth discrimination. J. Physiol. (Lond.) 193, 327–342 (1967).

    Article  CAS  Google Scholar 

  36. Hubel, D.H. & Wiesel, T.N. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. (Lond.) 195, 215–243 (1968).

    Article  CAS  Google Scholar 

  37. Tsao, D.Y. et al. Stereopsis activates V3A and caudal intraparietal areas in macaques and humans. Neuron 39, 555–568 (2003).

    Article  CAS  Google Scholar 

  38. Tailby, C., Majaj, N. & Movshon, T. Binocular integration of pattern motion signals by MT neurons and by human observers [Abstract]. J. Vis. 7, 95a (2007).

    Article  Google Scholar 

  39. Majaj, N.J., Tailby, C. & Movshon, J.A. (2007). Motion opponency in area MT of the macaque is mostly monocular [Abstract]. J. Vis. 7, 96a (2007).

    Article  Google Scholar 

  40. Rust, N.C., Mante, V., Simoncelli, E.P. & Movshon, J.A. How MT cells analyze the motion of visual patterns. Nat. Neurosci. 9, 1421–1431 (2006).

    Article  CAS  Google Scholar 

  41. Perrone, J.A. & Thiele, A. A model of speed tuning in MT neurons. Vision Res. 42, 1035–1051 (2002).

    Article  Google Scholar 

  42. Simoncelli, E.P. & Heeger, D.J. A model of neuronal responses in visual area MT. Vision Res. 38, 743–761 (1998).

    Article  CAS  Google Scholar 

  43. Wandell, B.A., Chial, S. & Backus, B.T. Visualization and measurement of the cortical surface. J. Cogn. Neurosci. 12, 739–752 (2000).

    Article  CAS  Google Scholar 

  44. Nestares, O. & Heeger, D.J. Robust multiresolution alignment of MRI brain volumes. Magn. Reson. Med. 43, 705–715 (2000).

    Article  CAS  Google Scholar 

  45. Glover, G.H. & Lai, S. Self-navigated spiral fMRI: interleaved versus single-shot. Magn. Reson. Med. 39, 361–368 (1998).

    Article  CAS  Google Scholar 

  46. Engel, S.A. et al. fMRI of human visual cortex. Nature 369, 525 (1994).

    Article  CAS  Google Scholar 

  47. Sereno, M.I. et al. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268, 889–893 (1995).

    Article  CAS  Google Scholar 

  48. Larsson, J., Landy, M.S. & Heeger, D.J. Orientation-selective adaptation to first- and second-order patterns in human visual cortex. J. Neurophysiol. 95, 862–881 (2006).

    Article  Google Scholar 

  49. Brainard, D.H. The Psychophysics Toolbox. Spat. Vis. 10, 433–436 (1997).

    Article  CAS  Google Scholar 

  50. Huk, A.C., Ress, D. & Heeger, D.J. Neuronal basis of the motion aftereffect reconsidered. Neuron 32, 161–172 (2001).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank D. Ress and T. Czuba for assistance with magnetic resonance imaging and comments on the manuscript and P. Neri for commenting on an earlier version of the manuscript. This work was supported by a National Science Foundation CAREER Award (BCS-0748413), a Mind Science Foundation Research Grant, and a pilot scanning grant from the University of Texas at Austin Imaging Research Center to A.C.H., and a Netherlands Organisation for Scientific Research grant to B.R. (2006/11353/ALW).

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Authors and Affiliations

  1. Neurobiology, Psychology, Center for Perceptual Systems, Institute for Neuroscience, and Imaging Research Center, The University of Texas at Austin, Austin, Texas, USA

    Bas Rokers, Lawrence K Cormack & Alexander C Huk

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  1. Bas Rokers
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  2. Lawrence K Cormack
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  3. Alexander C Huk
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Contributions

The authors jointly conceived the project, conducted the experiments and wrote the manuscript. B.R. programmed the visual displays and conducted the data analyses.

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Correspondence to Bas Rokers.

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Rokers, B., Cormack, L. & Huk, A. Disparity- and velocity-based signals for three-dimensional motion perception in human MT+. Nat Neurosci 12, 1050–1055 (2009). https://doi.org/10.1038/nn.2343

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