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Neuronal responses in extrastriate cortex to objects in optic flow fields

Published online by Cambridge University Press:  02 June 2009

Helen Sherk ,
Kathleen Mulligan  and
Jong-Nam Kim
Helen Sherk
Affiliation:
Department of Biological Structure, University of Washington, Seattle
Kathleen Mulligan
Affiliation:
Department of Biological Structure, University of Washington, Seattle
Jong-Nam Kim
Affiliation:
Department of Biological Structure, University of Washington, Seattle
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Abstract

During locomotion, observers respond to objects in the environment that may represent obstacles to avoid or landmarks for navigation. Although much is known about how visual cortical neurons respond to stimulus objects moving against a blank background, nothing is known about their responses when objects are embedded in optic flow fields (the patterns of motion seen during locomotion). We recorded from cells in the lateral suprasylvian visual area (LS) of the cat, an area probably analogous to area MT. In our first experiments, optic flow simulations mimicked the view of a cat trotting across a plain covered with small balls; a black bar lying on the balls served as a target object. In subsequent experiments, optic flow simulations were composed of natural elements, with target objects representing bushes, rocks, and variants of these. Cells did not respond to the target bar in the presence of optic flow backgrounds, although they did respond to it in the absence of a background. However, 273/423 cells responded to at least one of the taller, naturalistic objects embedded in optic flow simulations. These responses might represent a form of image segmentation, in that cells detected objects against a complex background. Surprisingly, the responsiveness of cells to objects in optic flow fields was not correlated with preferred direction as measured with a moving bar or whole-field texture. Because the direction of object motion was determined solely by receptive-field location, it often differed considerably from a cell's preferred direction. About a quarter of the cells responded well to objects in optic flow movies but more weakly or not at all to bars moving in the same direction as the object, suggesting that the optic flow background modified or suppressed direction selectivity.

Keywords

Lateral suprasylvian cortexOptic flowImage segmentationExtrastriate cortex
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 5 , September 1997 , pp. 879 - 895
Copyright
Copyright © Cambridge University Press 1997

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References

Albright, T. (1992). Form-cue invariant motion processing in primate visual cortex. Science 255, 1141–1143.CrossRefGoogle ScholarPubMed
Allman, J., Miezin, F. & McGuinness, E. (1985). Direction- and velocity-specific responses from beyond the classical receptive field in the middle temporal visual area (MT). Perception 14, 105–126.CrossRefGoogle ScholarPubMed
Allman, J., Miezin, F. & McGuinness, E. (1990). Effects of background motion on the responses of neurons in the first and second cortical visual areas. In Signal and Sense. Local and Global Order in Perceptual Maps, ed. Edelman, G.E., Gall, W.E. & Cowan, W.M., New York: Wiley-Liss.Google Scholar
Blakemore, C. & Zumbroich, T.J. (1987). Stimulus selectivity and functional organization in the lateral suprasylvian visual cortex of the cat. Journal of Physiology 389, 569–603.CrossRefGoogle ScholarPubMed
Camarda, R. & Rizzolatti, G. (1976). Visual receptive fields in the lateral suprasylvian area (Clare-Bishop area) of the cat. Brain Research 101, 427–443.CrossRefGoogle ScholarPubMed
Collett, T.S. & Harkness, L.I.K. (1982). Depth vision in animals. In Analysis of Visual Behavior, ed. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W., pp. 131–141. Cambridge, Massachusetts: MIT Press.Google Scholar
Dreher, B., Wang, C, Turlejski, K.J., Djavadian, R.L. & Burke, W. (1996). Areas PMLS and 21a of cat visual cortex: Two functionally distinct areas. Cerebral Cortex 6, 585–599.CrossRefGoogle ScholarPubMed
Duffy, C.J. & Wurtz, R.H. (1991). Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. Journal of Neurophysiology 65, 1329–1345.CrossRefGoogle Scholar
Field, D.J. (1987). Relations between the statistics of natural images and the response properties of cortical cells. Journal of the Optical Society of America A 4, 2379–2394.CrossRefGoogle ScholarPubMed
Gibson, J.J. (1950). The Perception of the Visual World. Boston, Massachusetts: Houghton-Mifflin.Google Scholar
Gizzi, M.S., Katz, E. & Movshon, J.A. (1990 a). Spatial and temporal analysis by neurons in the representation of the central visual field in the cat's lateral suprasylvian visual cortex. Visual Neuroscience 5, 463–468.Google ScholarPubMed
Gizzi, M.S., Katz, E., Schumer, R.A. & Movshon, J.A. (1990 b). Selectivity for orientation and direction of motion of single neurons in cat striate and extrastriate visual cortex. Journal of Neurophysiology 63, 1529–1543.CrossRefGoogle ScholarPubMed
Grant, S. & Shipp, S. (1991). Visuotopic organization of the lateral suprasylvian area and of an adjacent area of ectosylvian gyrus of the cat cortex. A physiological and connectional study. Visual Neuroscience 6, 315–338.CrossRefGoogle ScholarPubMed
Gulyas, B., Spileers, W. & Orbin, G.A. (1990). Modulation by a moving texture of cat area 18 neuron responses to moving bars. Journal of Neurophysiology 63, 404–423.CrossRefGoogle ScholarPubMed
Hamada, T. (1987). Neural response to the motion of textures in the lateral suprasylvian area of cats. Behavioral Brain Research 25, 175–185.CrossRefGoogle Scholar
Hammond, P. & MacKay, D.M. (1977). Differential responsiveness of simple and complex cells in cat striate cortex to visual texture. Experimental Brain Research 30, 275–296.Google ScholarPubMed
Hammond, P. & Smith, A.T. (1984). Sensitivity of complex cells in cat striate cortex to relative motion. Brain Research 301, 287–298.CrossRefGoogle ScholarPubMed
Hammond, P., Ahmed, B. & Smith, A.T. (1986). Relative motion sensitivity in cat striate cortex as a function of stimulus direction. Brain Research 386, 93–104.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1969). Visual area of the lateral suprasylvian gyrus (Clare-Bishop area) of the cat. Journal of Physiology (London) 202, 251–260.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1970). Stereoscopic vision in the monkey. Nature 225, 41–42.CrossRefGoogle ScholarPubMed
Kim, J-N., Mulligan, K. & Sherk, H. (1997). Simulated optic flow and extrastriate cortex. I. Optic flow versus texture. Journal of Neurophysiology 77, 554–561.CrossRefGoogle ScholarPubMed
Koenderink, J.J. (1986). Optic flow. Vision Research 26, 161–179.CrossRefGoogle ScholarPubMed
Kruger, K., Kiefer, W., Groh, A., Dinse, H.R. & von Seelen, W. (1993). The role of the lateral suprasylvian visual cortex of the cat in object-background interactions: Permanent deficits following lesions. Experimental Brain Research 97, 40–60.CrossRefGoogle ScholarPubMed
Lagae, L., Gulyas, B., Raiguel, S. & Orban, G.A. (1989). Laminar analysis of motion information processing in macaque V5. Brain Research 496, 361–367.CrossRefGoogle ScholarPubMed
Lagae, L., Maes, H., Raiguel, S., Xiao, D.K. & Orban, G.A. (1994). Responses of macaque STS neurons to optic flow components: A comparison of areas MT and MST. Journal of Neurophysiology 71, 1597–1626.CrossRefGoogle ScholarPubMed
Lamme, V.A.F., van Dijk, B.W. & Spekreijse, H. (1993). Contour from motion processing occurs in primary visual cortex. Nature 363, 541–543.CrossRefGoogle ScholarPubMed
Lappe, M., Bremmer, F., Pekel, M., Thiele, A. & Hoffmann, P. (1996). Optic flow processing in monkey STS: A theoretical and experimental approach. Journal of Neuroscience 16, 6265–6285.CrossRefGoogle ScholarPubMed
Lappe, M. & Rauschecker, J.P. (1994). Heading detection from optic flow. Nature 369, 712–713.CrossRefGoogle ScholarPubMed
Lee, D.N. (1976). A theory of visual control of braking based on information about time-to-collision. Perception 5, 437–459.CrossRefGoogle ScholarPubMed
Li, C.-Y. & Li, W. (1994). Extensive integration field beyond the classical receptive field of cat's striate cortical neurons—classification and tuning properties. Vision Research 34, 2337–2355.Google ScholarPubMed
Lomber, S.G., Cornwell, P., Sun, J.S., MacNeil, M.A. & Payne, B.R. (1994). Reversible inactivation of visual processing operations in middle suprasylvian cortex of the behaving cat. Proceedings of the National Academy of Sciences of the U.S.A. 91, 2999–3003.CrossRefGoogle ScholarPubMed
Lomber, S.G., Payne, B.R., Cornwell, P. & Long, K.D. (1996). Perceptual and cognitive visual functions of parietal and temporal cortices in the cat. Cerebral Cortex 6, 673–695.CrossRefGoogle ScholarPubMed
Marr, D. (1982). Vision. San Francisco, California: W.H. Freeman and Co.Google Scholar
Morrone, M.C., Di Sefano, M. & Burr, D.C. (1986). Spatial and temporal properties of neurons of the lateral suprasylvian cortex of the cat. Journal of Neurophysiology 56, 969–986.CrossRefGoogle ScholarPubMed
Mulligan, K., Kim, J.-N. & Sherk, H. (1997). Simulated optic flow and extrastriate cortex. II. Responses to bars versus large-field stimuli. Journal of Neurophysiology 77, 562–570.CrossRefGoogle ScholarPubMed
Nakayama, K. (1985). Biological image motion processing: A review. Vision Research 25, 625–660.CrossRefGoogle ScholarPubMed
Olavarria, J.F., DeYoe, E.A., Knierim, J.J., Fox, J.M. & Van Essen, D.C. (1992). Neural responses to visual texture patterns in middle temporal area of the macaque monkey. Journal of Neurophysiology 68, 164–181.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, 2595–2599.CrossRefGoogle ScholarPubMed
Palmer, L.A., Rosenquist, A.C. & Tusa, R.J. (1978). The retinotopic organization of lateral suprasylvian visual areas in the cat. Journal of Comparative Neurology 177, 237–256.CrossRefGoogle ScholarPubMed
Perrone, J.A. & Stone, L.S. (1994). A model of self-motion estimation within primate extrastriate visual cortex. Virion Research 34, 2917–2938.Google Scholar
Pettigrew, J.D., Cooper, M.L. & Blasdel, G.G. (1979). Improved use of, tapetal reflection for eye-position monitoring. Investigative Ophthalmology and Visual Science 18, 490–495.Google ScholarPubMed
Rauschecker, J.P., von Grunau, M.W. & Poulin, C. (1987). Centrifugal organization of direction preferences in the cat's lateral suprasylvian visual cortex and its relation to flow field processing. Journal of Neuroscience 7, 943–958.CrossRefGoogle ScholarPubMed
Royden, C.S. (1994). Analysis of misperceived observer motion during simulated eye rotations. Vision Research 34, 3215–3222.CrossRefGoogle ScholarPubMed
Rudolph, K.K. & Pasternak, T. (1996). Lesions in cat lateral suprasylvian cortex affect the perception of complex motion. Cerebral Cortex 6, 814–822.CrossRefGoogle ScholarPubMed
Saito, H., Yukie, M., Tanaka, M., 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, 145–157.CrossRefGoogle ScholarPubMed
Shelepin, Y.E. (1983). Spatial frequency characteristics of receptive fields of neurons in the lateral suprasylvian area of the cat cortex. Neurophysiology 14, 443–447.CrossRefGoogle Scholar
Sherk, H. & Mulligan, K.A. (1993). A reassessment of the lower visual field map in striate-recipient lateral suprasylvian cortex. Visual Neuroscience 10, 131–158.CrossRefGoogle ScholarPubMed
Sillito, A.M., Grieve, K.L., Jones, H.E., Cudeiro, J. & Davis, J. (1995). Visual cortical mechanisms detecting focal orientation discontinuities. Nature 378, 492–496.CrossRefGoogle ScholarPubMed
Spear, P.D. (1991). Functions of extrastriate visual cortex. In The Neural Basis of Visual Function, ed. Leventhal, A., pp. 339–370. Basingstoke, England: McMillan Press.Google Scholar
Spear, P.D. & Baumann, T.P. (1975). Receptive-field characteristics of single neurons in lateral suprasylvian visual area of the cat. Journal of Neurophysiology 38, 1403–1420.CrossRefGoogle ScholarPubMed
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, 134–144.CrossRefGoogle ScholarPubMed
Tolhurst, D.J., Tadmor, Y. & Chao, T. (1992). Amplitude spectra of natural images. Ophthalmalogical and Physiological Optics 12, 229–232.CrossRefGoogle ScholarPubMed
Toyama, K., Komatsu, Y. & Kozasa, T. (1986). The responsiveness of Clare-Bishop neurons to motion cues for motion stereopsis. Neuroscience Research 4, 83–109.CrossRefGoogle ScholarPubMed
Toyama, K. & Kozasa, T. (1982). Responses of Clare-Bishop neurones to three dimensional movement of a light stimulus. Vison Research 22, 571–574.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Desimone, R. (1986). Cortical connections of visual area MT in the macaque. Journal of Comparative Neurology 248, 190–222.CrossRefGoogle ScholarPubMed
Vaezy, S. & Clark, J.I. (1995). Characterization of the cellular micro-structure of ocular lens using 2D power law analysis. Annals of Biomedical Engineering 23, 482–490.CrossRefGoogle Scholar
Vishton, P.M. & Cutting, J.E. (1995). Wayfinding, displacements, and mental maps: Velocity fields are not typically used to determine one's aimpoint. Journal of Experimental Psychology 21, 978–995.Google Scholar
von Grunau, M. & Frost, B.J. (1983). Double-opponent process mechanism underlying RF-structure of directionally specific cells of cat lateral suprasylvian visual area. Experimental Brain Research 49, 84–92.CrossRefGoogle ScholarPubMed
Wang, Y. & Frost, B.J. (1992). Time to collision is signalled by neurons in the nucleus rotundus of pigeons. Nature 356, 236–238.CrossRefGoogle ScholarPubMed
Watt, R. (1994). A computational examination of image segmentation and the initial stages of human vision. Perception 23, 383–398.CrossRefGoogle ScholarPubMed
Wright, M.M. (1969). Visual receptive fields of cells in a cortical area remote from the striate cortex in the cat. Nature 223, 973–975.CrossRefGoogle Scholar
Yin, T.C.T. & Greenwood, M. (1992). Visual response properties of neurons in the middle and lateral suprasylvian cortices of the behaving cat. Experimental Brain Research 88, 1–14.CrossRefGoogle ScholarPubMed