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Neural responses to velocity gradients in macaque cortical area MT

Published online by Cambridge University Press:  02 June 2009

Stefan Treue
Affiliation:
Cognitive Neuroscience Laboratory, Department of Neurology, University of Tübingen, Auf der Morgenstelle 15, 72076 Tübingen, Germany
Richard A. Andersen
Affiliation:
Division of Biology, California Institute of Technology, Pasadena

Abstract

Visual motion, i.e. the pattern of changes on the retinae caused by the motion of objects or the observer through the environment, contains important cues for the accurate perception of the three-dimensional layout of the visual scene. In this study, we investigate if neurons in the visual system, specifically in area MT of the macaque monkey, are able to differentiate between various velocity gradients. Our stimuli were random dot patterns designed to eliminate stimulus variables other than the orientation of a velocity gradient. We develop a stimulus space (“deformation space”) that allows us to easily parameterize our stimuli. We demonstrate that a substantial proportion of MT cells show tuned responses to our various velocity gradients, often exceeding the response evoked by an optimized flat velocity profile. This suggests that MT cells are able to represent complex aspects of the visual environment and that their properties make them well suited as building blocks for the complex receptive-field properties encountered in higher areas, such as area MST to which many cells in area MT project.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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References

Allman, J., Miezin, F. & McGuiness, E. (1985). Direction- and velocity-specific responses from beyond the classical receptive field in the middle temporal visual area (MT). Perception 14, 105126.CrossRefGoogle ScholarPubMed
Andersen, G. J. (1989). Perception of three-dimensional structure from optical flow without locally smooth velocity. Journal of Experimental Psychology: Human Perception and Performance 15, 363371.Google ScholarPubMed
Andersen, R. A., & Siegel, R. M. (1990). Motion processing in the primate cortex. In Signal and Sense: Local and Global Order in Perceptual Maps, ed. Edelman, G. M., Gall, W. E. & Cowan, W. M. pp. 163184, New York: John Wiley.Google Scholar
Bradley, D. C., Qian, N. & Andersen, R. A. (1995). Integration of motion and stereopsis in midlle temporal cortical area of macaques. Nature 373, 609.CrossRefGoogle Scholar
Braunstein, M. L. & Andersen, G. J. (1984). Shape and depth perception from parallel projections of three-dimensional motion. Journal of Experimental Psychology: Human Perception and Performance 10, 749759.Google ScholarPubMed
Crowell, J. A. & Banks, M. S. (1993). Perceiving heading with different retinal regions and types of optic flow. Perception & Psychophysics 53, 325337.CrossRefGoogle ScholarPubMed
Dobbins, A., Zucker, S. W. & Cynader, M. S. (1990). A mean field model of optic flow estimation by MT neurons. Society for Neuroscience Abstracts 16, 6.Google Scholar
Duffy, C. J. & Wurtz, R. H. (1991 a). Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. Journal of Neuroscience 11, 13291345.Google Scholar
Duffy, C. J. & Wurtz, R. H. (1991 b). Sensitivity of MST neurons to optic flow stimuli. II. Mechanisms of response selectivity revealed by small-field stimuli. Journal of Neuroscience 11, 13461359.Google Scholar
Gallant, J. L., Braun, J. & Van Essen, D. C. (1993). Selectivity for polar, hyperbolic, and Cartesian gratings in macaque visual cortex. Science 259, 100103.CrossRefGoogle ScholarPubMed
Gibson, J. J. (1950). The Perception of the Visual World. Boston, Massachusetts: Houghton Mifflin.Google Scholar
Golomb, B., Andersen, R. A., Nakayama, K., MacLeod, D. I. A. & Wong, A. (1985). Visual thresholds for shearing motion in monkey and man. Vision Research 25, 813820.CrossRefGoogle ScholarPubMed
Graziano, M. S. A., Andersen, R. A. & Snowden, R. J. (1994). Tuning of MST neurons to spiral motions. Journal of Neuroscience 14, 5467.CrossRefGoogle ScholarPubMed
Harris, M., Freeman, T. & Hughes, J. (1992). Retinal speed gradients and the perception of surface slant. Vision Research 32, 587590.CrossRefGoogle ScholarPubMed
Husain, M., Treue, S. & Andersen, R. A. (1989). Surface interpolation in 3-D structure-from-motion perception. Neural Compulation 1, 324333.CrossRefGoogle Scholar
Koenderink, J. J. (1986). Optic flow. Vision Research 26, 161180.CrossRefGoogle ScholarPubMed
Koenderink, J. J. & Van Doorn, A. J. (1981). Exterospecific component of the motion parallax field. Journal of the Optical Society of America 71, 953957.CrossRefGoogle ScholarPubMed
Lagae, L., Maes, H., Raiguel, S., Ziao, D. K. & Orban, G. A. (1994). Responses of macaque STS neurons to optic flow components: A comparison of area MTand MST. Journal of Neurophysiology 71, 15971626.CrossRefGoogle Scholar
Landy, M. S., Dosher, B.A., Sperling, G. & Perkins, M. E. (1991). The kinetic depth effect and optic flow II. First- and second-order motion. Vision Research 31, 859876.CrossRefGoogle ScholarPubMed
Longuet-Higgins, H. C. & Prazdny, K. (1980). The interpretation of a moving retinal image. Proceedings of the Royal Society B (London) 208, 385397.Google ScholarPubMed
MacKay, D. M. (1961). Visual effects of non-redundant stimulation. Nature 192, 739740.CrossRefGoogle Scholar
Nakayama, K. (1981). Differential motion hyperacuity under conditions of common image motion. Vision Research 21, 14751482.CrossRefGoogle ScholarPubMed
Nakayama, K., Silverman, G., MacLeod, D. I. A. & Mulligan, J. (1985). Sensitivity to shearing and compressive motion in random dots. Perception 14, 97241.CrossRefGoogle ScholarPubMed
Orban, G. A., Lagae, L., Verri, A., Raiguel, S., Xiao, D., Maes, H. & Torre, V. (1992). First order analysis of optical flow in monkey brain. Proceedings of the National Academy of Sciences of the U.S.A. 89, 25952599.CrossRefGoogle ScholarPubMed
Regan, D. (1985). Visual flow and direction of locomotion. Science 227, 10641065.CrossRefGoogle ScholarPubMed
Regan, D. (1986). Visual processing of four kinds of relative motion. Vision Research 26, 127145.CrossRefGoogle ScholarPubMed
Regan, D. & Beverley, K. I. (1981). How do we avoid confounding the direction we are looking and the direction we are moving? Science 215, 194196.CrossRefGoogle Scholar
Regan, D. & Beverly, K. I. (1985). Visual responses to vorlicity and the neural analysis of optic flow. Journal of the Optical Society of America 2, 280283.CrossRefGoogle ScholarPubMed
Regan, D., Erkelens, C. J. & Collewijn, H. (1986). Necessary conditions for the perception of motion in depth. Investigative Ophthalmology and Visual Science 27, 584596.Google ScholarPubMed
Rieger, J. H. & Lawton, D. T. (1985). Processing differential image motion. Journal of the Optical Society of America A 2, 354360.CrossRefGoogle ScholarPubMed
Robinson, D. A. (1963). A method of measuring eye movement using a sceral search coil in a magnetic field. IEEE Transactions of Biomedical Engineering 10, 137145.Google Scholar
Rogers, B. J. & Graham, M. (1979). Motion parallax as an independent cue for depth perception. Perception 8, 125134.CrossRefGoogle ScholarPubMed
Rogers, B. & Graham, M. (1982). Similarities between motion parallax and stereopsis in human depth perception. Vision Research 22, 261270.CrossRefGoogle ScholarPubMed
Royden, C. S., Crowell, J. A. & Banks, M. S. (1994). Estimating heading during eye movements. Vision Research 34, 31973214.CrossRefGoogle ScholarPubMed
Saito, H., Yukie, M., Tanaka, K., Hikosaka, K., Fukada, Y. & Iwai, E. (1986). Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey. Journal of Neuroscience 6, 145157.CrossRefGoogle ScholarPubMed
Siegel, R. M. & Andersen, R. A. (1986). Motion perceptual deficits following ibotenic acid lesions of the middle temporal area in the behaving rhesus monkey. Society for Neuroscience Abstracts 12, 1183.Google Scholar
Siegel, R. M. & Andersen, R. A. (1988). Perception of three-dimensional structure from motion in monkey and man. Nature 331, 259261.CrossRefGoogle ScholarPubMed
Snowden, R. J., Treue, S., Erickson, R. E. & Andersen, R. A. (1991). The response of area MT and V1 neurons to transparent motion. Journal of Neuroscience 11, 27682785.CrossRefGoogle ScholarPubMed
Tanaka, K., Fukada, Y. & Saito, H. (1989). Underlying mechanisms of the response specificity of expansion/contraction, and rotation cells clustered in the dorsal part of the medial superior temporal area of the macaque monkey. Journal of Neurophysiology 62, 642656.CrossRefGoogle Scholar
Tanaka, K., Hikosaka, K., Saito, H., Yukie, M., Fukada, Y. & Iwai, E. (1986). Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey. Journal of Neuroscience. 6, 134144.CrossRefGoogle ScholarPubMed
Tanaka, K. & Saito, H. (1989). 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. Journal of Neurophysiology 62, 626641.CrossRefGoogle ScholarPubMed
Treue, S., Husain, M. & Andersen, R. (1991). Human perception of structure from motion. Vision Research 31, 5975.CrossRefGoogle ScholarPubMed
Warren, W. H. & Hannon, D. J. (1988). Direction of self-motion is perceived from optical flow. Nature 336, 162163.CrossRefGoogle Scholar
Warren, W. H., Morris, M. W. & Kalish, M. (1988). Perception of translational heading from optical flow. Journal of Experimental Psychology: Human Perception and Performance 14, 646660.Google ScholarPubMed
Xiao, D. K., Marcar, V. L., Raiouel, S. E. & Orban, G. A. (1994). Does the surround really surround the classical receptive field of macaque MT cells? Society for Neuroscience Abstracts 20, 773.Google Scholar