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Centrifugal directional bias in the middle temporal visual area (MT) of the macaque

Published online by Cambridge University Press:  02 June 2009

Thomas D. Albright
Thomas D. Albright
Affiliation:
Department of Psychology, Princeton University, Princeton
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Abstract

We have examined the distribution of preferred directions of motion for neurons in the middle temporal visual area (MT) of the macaque. We found a marked anisotropy favoring directions that are oriented away from the center of gaze. This anisotropy is present only among neurons with peripherally located receptive fields. This peripheral centrifugal directionality bias corresponds well to the biased distribution of motions characteristic of optic flow fields, which are generated by displacement of the visual world during forward locomotion. The bias may facilitate the processing of this common form of visual stimulation and could underlie previously observed perceptual anisotropies favoring centrifugal motion. We suggest that the bias could arise from exposure of modifiable cortical circuitry to a naturally occurring form of selective visual experience.

Keywords

Extrastriate cortexVisual area MTMotionOptic flowDirectional bias
Type
Research Articles
Information
Visual Neuroscience , Volume 2 , Issue 2 , February 1989 , pp. 177 - 188
Copyright
Copyright © Cambridge University Press 1989

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References

Albright, T. D. (1984). Direction and orientation selectivity of neurons in visual area MT of the macaque. Journal of Neurophysiology 52, 1106–1130.CrossRefGoogle ScholarPubMed
Albright, T. D. & Desimone, R. (1987). Local precision of visuotopic organization in the middle temporal area (MT) of the macaque. Experimental Brain Research 65, 582–592.CrossRefGoogle ScholarPubMed
Albright, T. D., Desimone, R. & Gross, C. G. (1984). Columnar organization of directionally selective cells in visual area MT of the macaque. Journal of Neurophysiology 51, 16–31.CrossRefGoogle ScholarPubMed
Allman, J. M. & Kass, J. H. (1971). A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey (Aotus trivirgatus). Brain Research 31, 85–105.CrossRefGoogle ScholarPubMed
Allman, J. M., Miezin, F. & McGuinness, E. (1985). Stimulus specific responses from beyond the classical receptive field: Neurophysiological mechanisms for local-global comparisons in visual neurons.. Annual Review of Neuroscience 8, 407–430.CrossRefGoogle ScholarPubMed
Annis, R. C. & Frost, B. (1973). Human visual ecology and orientation anisotropies in acuity. Science 182, 729–731.CrossRefGoogle ScholarPubMed
Baker, J. F., Petersen, S. E., Newsome, W. T. & Allman, J. M. (1981). Visual response properties of neurons in four extrastriate visual areas of the owl monkey {Aotus trivirgatus): a quantitative comparison of the medial (M), dorsomedial (DM), dorsolateral (DL), and middle temporal (MT) areas. Journal of Neurophysiology 45, 387–406.CrossRefGoogle ScholarPubMed
Ball, K. & Sekuler, R. (1980). Human vision favors centrifugal motion. Perception 9, 317–325.CrossRefGoogle ScholarPubMed
Barlow, H. B. (1975). Visual experience and cortical development. Nature (London) 258, 199–204.CrossRefGoogle ScholarPubMed
Barlow, H. B., Blackmore, C. & Pettigrew, J. D. (1967). The neural mechanism of bionocular depth discrimination. Journal of Physiology (London) 198 a, 327–342.CrossRefGoogle Scholar
Batschelet, E. (1965). Statistical Methods for the Analysis of Problems in Animal Orientation and Certain Biological Rhythms.. American Institute of Biological Sciences: Washington, DC.Google Scholar
Blackmore, C. & Cooper, G. F. (1970). Development of the brain depends on the visual environment. Nature 228, 477–478.CrossRefGoogle Scholar
Blasdel, G. G., Mitchell, D. E., Muir, D. W. & Pettigrew, J. D. (1977). A physiological and behavioral study in cats of the effect of early visual experience with contours of a single orientation.. Journal of Physiology (London) 265, 615–636.CrossRefGoogle ScholarPubMed
Boussaoud, D., Ungerleider, L. G. & Desimone, R. (1987). Cortical pathways for motion analysis: connections of visual areas MST and FST in macaques. Society for Neuroscience Abstracts 13, 1625.Google Scholar
Bruce, C., Desimone, R. & Gross, C. G. (1981). Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. Journal of Neurophysiology 46, 369–384.CrossRefGoogle Scholar
Clocksin, W. F. (1980). Perception of surface slant and edge labels from optical flow: a computational approach.. Perception 9, 253–269.CrossRefGoogle ScholarPubMed
Cyander, M., Berman, N. & Hein, A. (1975). Cats raised in a onedirectional world: effects on receptive fields in visual cortex andsuperior colliculus. Experimental Brain Research 22, 267–280.Google Scholar
Daw, M. W. & Wyatt, H. J. (1976). Kittens reared in a unidirectional environment: evidence for a critical period.. Journal of Physiology (London) 257, 155–170.CrossRefGoogle Scholar
Dubner, R. & Zeki, S. M. (1971). Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus in the monkey. Brain Research 35, 528–532.CrossRefGoogle Scholar
Freeman, R. D., Mitchell, D. E. & Millodot, M. (1972). A neural effect of partial visual deprivation in humans. Science 75, 1384–1386.CrossRefGoogle Scholar
Freeman, R. D. & Freeman, J. D. (1973). Alteration of visual cortex from environmental asymmetries. Nature 246, 359–360.CrossRefGoogle ScholarPubMed
Fuchs, A. F. (1967). Silver staining of myelin by means of physical development. Orvostucomany 20, 433–489.Google Scholar
Gattass, R. & Gross, C. G. (1981). Visual topography of the striate projection zone in the posterior superior temporal sulcus (MT) of the macaque. Journal of Neurophysiology 46, 621–637.CrossRefGoogle ScholarPubMed
Georgeson, M. A. & Harris, M. G. (1978). Apparent foveofugal drift of counterphase gratings. Perception 7, 527–536.CrossRefGoogle ScholarPubMed
Gibson, J. J. (1950). The Perception of the Visual World. Boston: Houghton Mifflin.Google Scholar
Helmholtz, H. von (1924). Physiological Optics, Vol. 3. English Translation by Southall, J. P. C. for the Optical Society of America from the 3rd German edition of (1909) Handbuch der Physiologischen Optik. Hamburg: Voss.Google Scholar
Hirsch, H. V. B. & Spinelli, D. N. (1970). Visual experience modified distribution of horizontally and vertically oriented receptive fields in cats. Science 168, 868–871.CrossRefGoogle ScholarPubMed
Hirsch, H. V. B. & Spinelli, D. N. (1971). Modification of the distribution of receptive-field orientation in cats by selective visual exposure during development. Experimental Brain Research 13, 509–527.Google Scholar
Hodos, W. & Campbell, C. B. G. (1969). Scala Naturae: Why there is no theory in comparative psychology. Psychological Reviews 76, 337–350.CrossRefGoogle Scholar
Koenderink, J. J. (1986). Optic flow. Vision Research 26, 161–180.CrossRefGoogle ScholarPubMed
Latour, P. L. (1962). Visual threshold during eye movements. Vision Research 2, 261–262.CrossRefGoogle Scholar
Lee, D. N. (1980). The optical flow field: the foundation of vision. Philosophical Transactions of the Royal Society B (London) 290, 169–179.Google ScholarPubMed
Leventhal, A. G. & Schall, J. D. (1983). Structural basis of orientation sensitivity of cat retinal ganglion cells. Journal of Comparative Neurology 220, 465–475.CrossRefGoogle ScholarPubMed
Levick, W. R. & Thibos, L. N. (1982). Analysis of orientation bias in cat retina. Journal of Physiology (London) 329, 243–261.CrossRefGoogle ScholarPubMed
Mardia, K. V. (1972). Statistics of Directional Data. New York: Academic Press.Google Scholar
Maunsell, J. H. R. & Van Essen, D. C. (1983 a). Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation.. Journal of Neurophysiology 49, 1127–1147.CrossRefGoogle ScholarPubMed
Maunsell, J. H. R. & Van Essen, D. C. (1983 b). The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 2563–2586.CrossRefGoogle ScholarPubMed
Maunsell, J. H. R. & Van Essen, D. C. (1987). Topographic organization of the middle temporal visual area in the macaque monkey: representational biases and the relationship to callosal connections and myeloarchitectonic boundaries. Journal of Comparative Neurology 266, 535–555.CrossRefGoogle ScholarPubMed
Miezin, F., McGuinness, E. & Allman, J. M. (1982). Antagonistic direction specific mechanisms in area MT in the owl monkey. Society for Neuroscience Abstracts 8, 681.Google Scholar
Mikami, A., Newsome, W. T. & Wurtz, R. H. (1986). Motion selectivity in macaque visual cortex: II. Spatio-temporal range of directional interactions in MT and VI. Journal of Neurophysiology 55, 1328–1339.CrossRefGoogle Scholar
Mitchell, D. E. (1980). The influence of early visual experience on visual perception. InVisual Coding and Adaptability, ed. Harris, C. S.. pp. 1–50. Hillsdale, New Jersey: Lawrence Erlbaum Associates.Google Scholar
Motter, B. C. & Mountcastle, V. B. (1981). The functional properties of the light-sensitive neurons of the posterior parietal cortex studied in waking monkeys: foveal sparing and opponent vector organization. Journal of Neuroscience 1, 3–26.CrossRefGoogle ScholarPubMed
Ranschecker, J. P., von Grünau, 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 Scholar
Regan, D. & Beverly, K. L. (1984). Psychophysics of visual flow patterns and motion in depth. In Sensory Experience, Adaptation, and Perception: Festschrift for Ivo Kohler. ed. Spillman, L. & Wooten, B. R., pp. 215–240, Hillsdale, New Jersey: Lawrence Erlbaum Associates.Google Scholar
Richards, W. & Steinbach, M. J. (1972). Impaired motion detection preceding smooth eye movements. Vision Research 12, 353–356.CrossRefGoogle ScholarPubMed
Rodman, H. R. & Albright, T. D. (1987). Coding of visual stimulus velocity in area MT of the macaque. Vision Research 27, 2035–2048.CrossRefGoogle ScholarPubMed
Schall, J. D., Vitek, D. J. & Leventhal, A. G. (1986). Retinal constraints on orientation specificity in cat visual cortex.. Journal of Neuroscience 6, 823–836.CrossRefGoogle ScholarPubMed
Scott, T. R., Lanvender, A. D., McWhirt, R. A. & Powell, D. A. (1966). Directional asymmetry of motion aftereffect. Journal of Experimental Psychology 71, 806–815.CrossRefGoogle ScholarPubMed
Siegel, R. M., Andersen, R. A., Essick, G. K. & Asanuma, C. (1985). The functional and anatomical subdivision of the inferior parietal lobule. Society for Neuroscience Abstracts 11, 1012.Google Scholar
Stryker, M. P., Sherk, H., Leventhal, A. G. & Hirssch, H. V. B. (1978). Physiological consequences for the cat's visual cortex effectively restricting early visual experience with oriented contours. Journal of Neurophysiology 41, 896–909.CrossRefGoogle ScholarPubMed
Switkes, E., Mayer, M. J. & Sloan, J. A. (1978). Spatial-frequency analysis of the visual environment: anisotropy and the carpentered environment hypothesis. Vision Research 18, 1393–1399.CrossRefGoogle ScholarPubMed
Tanaka, K., Hikosaka, H., Satto, H., Yukie, Y., 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
Tretter, F., Cyander, M. & Singer, W. (1975). Modification of direction selectivity in neurons in the visual cortex of kittens.. Brain Research 84, 143–149.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
Ungerleider, L. G. & Mishkin, M. (1979). The striate projection zone in the superior temporal sulcus of Macaca mulatto: localization and topographic organization. Journal of Comparative Neurology 188, 347–366.CrossRefGoogle Scholar
Van Essen, D. C. (1985). Functional organization of primate visual cortex. In Cerebral Cortex, Vol. 3, ed. Peters, A. A. & Jones, E. G.. pp. 259–329. New York: Plenum Press.Google Scholar
Van Essen, D. C., Maunsell, J. H. R. & Bixby, J. L. (1981). The middle temporal visual area in the macaque: myeloarchitecture, connections, functional properties, and topographic connections. Journal of Comparative Neurology 199, 293–326.CrossRefGoogle Scholar
Van Essen, D. C., Newsome, W. T. & Maunsell, J. H. R. (1984). The visual-field representation in striate cortex of the macaque monkey: asymmetries, anisotropies, and individual variability. Vision Research 24, 429–448.CrossRefGoogle ScholarPubMed
Vidyasagar, T. R. & Urbas, J. V. (1982). LGN neurones with and without inputs from visual cortical areas 17 and 18. Experimental Brain Research 46, 157–169.CrossRefGoogle Scholar
Vital-Durand, F. & Jeannerod, M. (1974). Maturation of the optokinetic response: genetic and environmental factors.. Brain Research 71, 249–257.CrossRefGoogle ScholarPubMed
Wiesel, T. (1982). Postnatal development of the visual cortex and the influence of environment. Nature 299, 583–591.CrossRefGoogle ScholarPubMed
Zeki, S. M. (1974). Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. Journal of Physiology (London) 236, 549–573.CrossRefGoogle ScholarPubMed
Zeki, S. M. (1978). Functional organization in the visual cortex of rhesus monkey. Nature (London) 274, 423–428.CrossRefGoogle Scholar