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Visual experience promotes the isotropic representation of orientation preference

Published online by Cambridge University Press:  03 May 2004

DAVID M. COPPOLA  and
LEONARD E. WHITE
DAVID M. COPPOLA
Affiliation:
Department of Biology, Centenary College, Shreveport
LEONARD E. WHITE
Affiliation:
Department of Community and Family Medicine, Doctor of Physical Therapy Division, Duke University Medical Center, Durham Department of Neurobiology, Duke University Medical Center, Durham Center for the Study of Aging and Human Development, Duke University Medical Center, Durham
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Abstract

Within the visual cortex of several mammalian species, more circuitry is devoted to the representation of vertical and horizontal orientations than oblique orientations. The sensitivity of this representation of orientation preference to visual experience during cortical maturation and the overabundance of cardinal contours in the environment suggest that vision promotes the development of this cortical anisotropy. We tested this idea by measuring the distribution of cortical orientation preference and the degree of orientation selectivity in developing normal and dark-reared ferrets using intrinsic signal optical imaging. The area of the angle map of orientation preference representing cardinal and oblique orientations was determined; in addition, orientation selectivity indices were computed separately for cardinal and oblique difference images. In normal juvenile animals, we confirm a small, but statistically significant overrepresentation of near horizontal orientations in the cortical angle map. However, the degree of anisotropy did not increase in the weeks that followed eye opening when orientation selectivity matured; rather, it decreased. In dark-reared ferrets, an even greater cortical anisotropy emerged, but angle maps in these animals developed an apparently anomalous overrepresentation of near vertical orientations. Thus, the overrepresentation of cardinal orientations in the visual cortex does not require experience with an anisotropic visual environment; indeed, cortical anisotropy can develop in the complete absence of vision. These observations suggest that the role of visual experience in cortical maturation is to promote the isotropic representation of orientation preference.

Keywords

Cardinal biasOrientation selectivityMapsOblique effectOptical imaging
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 1 , January 2004 , pp. 39 - 51
Copyright
2004 Cambridge University Press

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References

REFERENCES

Ackerman, C.J., Smyth, D., & Thompson, I.D. (2002). Visual experience before eye-opening and the development of the retinogeniculate pathway. Neuron 36, 869–879.CrossRefGoogle Scholar
Albus, K. (1975). A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat. II. The spatial organization of the orientation domain. Experimental Brain Research 24, 181–202.Google Scholar
Annis, R.C. & Frost, B. (1973). Human visual ecology and orientation anisotropies in acuity. Science 182, 729–731.CrossRefGoogle Scholar
Appelle, S. (1972). Perception and discrimination as a function of stimulus orientation: The “oblique effect” in man and animals. Psychological Bulletin 78, 266–278.CrossRefGoogle Scholar
Atkinson, J., Braddick, O., & French, J. (1980). Infant astigmatism; Its disappearance with age. Vision Research 20, 891–893.CrossRefGoogle Scholar
Basole, A., White, L.E., & Fitzpatrick, D. (2003). Mapping multiple stimulus features in the population response of visual cortical neurons. Nature 423, 986–990.CrossRefGoogle Scholar
Bauer, R. & Jordan, W. (1993). Different anisotropies for texture and grating stimuli in the visual map of cat striate cortex. Vision Research 33, 1447–1450.CrossRefGoogle Scholar
Blakemore, C. & Van Sluyters, R.C. (1975). Innate and environmental factors in the development of the kitten's visual cortex. Journal of Physiology (London) 248, 663–716.CrossRefGoogle Scholar
Blasdel, G.G. & Salama, G. (1986). Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321, 579–585.CrossRefGoogle Scholar
Bonhoeffer, T. & Grinvald, A. (1991). Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature 353, 429–431.CrossRefGoogle Scholar
Bonhoeffer, T. & Grinvald, A. (1996). Optical imaging based on intrinsic signals: The methodology. In Brain Mapping: The Methods, ed. Toga, A.W. & Mazziotta, J.C., pp. 55–97. San Diego, California: Academic Press.
Bosking, W.H., Crowley, J.C., & Fitzpatrick, D. (2002). Spatial coding of position and orientation in primary visual cortex. Nature Neuroscience 5, 874–882.CrossRefGoogle Scholar
Buisseret, P. & Imbert, M. (1976). Visual cortical cells: Their developmental properties in normal and dark-reared kittens. Journal of Physiology (London) 255, 511–525.CrossRefGoogle Scholar
Buisseret, P., Gary-Lobo, E., & Imbert M. (1982). Plasticity in the kitten's visual cortex: Effects of the suppression of visual experience upon the orientational properties of visual cortical cells. Brain Research 256, 417–426.CrossRefGoogle Scholar
Callaway, E.M. (1998). Visual scenes and cortical neurons: What you see is what you get. Proceedings of the National Academy of Sciences of the U.S.A. 95, 3344–3345.CrossRefGoogle Scholar
Callaway, E.M. & Katz, L.C. (1991). Effects of binocular deprivation on the development of clustered horizontal connections in cat striate cortex. Proceedings of the National Academy of Sciences of the U.S.A. 88, 745–749.CrossRefGoogle Scholar
Chapman, B. & Bonhoeffer, T. (1998). Overrepresentation of horizontal and vertical orientation preferences in developing ferret area 17. Proceedings of the National Academy of Sciences of the U.S.A. 95, 2609–2614.CrossRefGoogle Scholar
Chapman, B. & Stryker, M.P. (1993). Development of orientation selectivity in ferret visual cortex and effects of deprivation. Journal of Neuroscience 13, 5251–5262.Google Scholar
Chapman, B., Stryker, M.P., & Bonhoeffer, T. (1996). Development of orientation preference maps in ferret primary visual cortex. Journal of Neuroscience 16, 6443–6453.Google Scholar
Coppola, D.M., Purves, H.R., McCoy, A.N., & Purves, D. (1998a). The distribution of oriented contours in the real world. Proceedings of the National Academy of Sciences of the U.S.A. 95, 4002–4006.Google Scholar
Coppola, D.M., White, L.E., & Fitzpatrick D. (1998b). Differential effects of binocular lid suture on maps of orientation preference, ocular dominance and visual space in developing ferret visual cortex. Society for Neuroscience Abstracts 24, 1874.Google Scholar
Coppola, D.M., White, L.E., Fitzpatrick, D., & Purves, D. (1998c). Unequal distribution of cortical space devoted to the analysis of oriented contours. Proceedings of the National Academy of Sciences of the U.S.A. 95, 2621–2523.Google Scholar
Crair, M.C., Gillespie, D.C., & Stryker, M.P. (1998). The role of visual experience in the development of columns in cat visual cortex. Science 279, 566–5270.CrossRefGoogle Scholar
Crair, M.C., Horton, J.C., Antonini, A., & Stryker, M.P. (2001). Emergence of ocular dominance columns in cat visual cortex by two weeks of age. Journal of Comparative Neurology 430, 235–249.3.0.CO;2-P>CrossRefGoogle Scholar
Cynader, M.S. & Mitchell, D.E. (1980). Prolonged sensitivity to monocular deprivation in dark-reared cats. Journal of Neurophysiology 43, 1026–1040.CrossRefGoogle Scholar
De Valois, R.L. & De Valois, K.K. (1988). Spatial Vision. New York: Oxford University Press.
De Valois, R.L., Yund, E.W., & Helper, N. (1982). The orientation and direction selectivity of cells in Macaque visual cortex. Vision Research 22, 531–544.CrossRefGoogle Scholar
Dragoi, V., Turcu, C.M., & Sur, M. (2001). Stability of cortical responses and the statistics of natural scenes. Neuron 32, 1–20.Google Scholar
Durack, J.C. & Katz, L.C. (1996). Development of horizontal connections in layer 2/3 of ferret visual cortex. Cerebral Cortex 6, 178–183.CrossRefGoogle Scholar
FitzGibbon, T., Wingate, R.J., & Thompson, I.D. (1996). Soma and axon diameter distributions and central projections of ferret retinal ganglion cells. Visual Neuroscience 13, 773–786.CrossRefGoogle Scholar
Frégnac, Y. & Imbert, M. (1978). Early development of visual cortical cells in normal and dark-reared kittens: The relationship between orientation selectivity and ocular dominance. Journal of Physiology (London) 278, 27–44.CrossRefGoogle Scholar
Frégnac, Y. & Imbert, M. (1984). Development of neuronal selectivity in primary visual cortex of cat. Physiology Reviews 64, 325–434.CrossRefGoogle Scholar
Furmanski, C.S. & Engel, S. (2000). An oblique effect in human primary visual cortex. Nature Neuroscience 3, 535–536.CrossRefGoogle Scholar
Garraghty, P.E., Frost, D.O., & Sur, M. (1987). The morphology of retinogeniculate X- and Y-cell axonal arbors in dark-reared cats. Experimental Brain Research 66, 115–127.Google Scholar
Guyton, D.L., Greene, P.R., & Schotz, R.T. (1989). Dark-rearing interference with emmetropization in Rhesus Monkey. Investigative Ophthalmology and Visual Science 30, 761–764.Google Scholar
Hendrickson, A. & Boothe, R. (1976). Morphology of the retina and dorsal lateral geniculate nucleus in dark-reared monkeys (Macaca nemestrina). Vision Research 16, 517–521.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology (London) 160, 106–154.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1963a). Shape and arrangement of columns in the cat's striate cortex. Journal of Physiology (London) 165, 559–568.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1963b). Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. Journal of Neurophysiology 26, 994–1002.Google Scholar
Hübener, M. & Bonhoeffer, T. (2002). Optical imaging of functional architecture in cat primary visual cortex. In The Cat Primary Visual Cortex, ed. Payne, B.R & Peters, A., pp. 131–166. San Diego, California: Academic Press.CrossRef
Hübener, M., Shoham, D., Grinvald, A., & Bonhoeffer, T. (1997). Spatial relationships among three columnar systems in cat area 17. Journal of Neuroscience 17, 9270–9284.CrossRefGoogle Scholar
Issa, N.P., Trepel, C., & Stryker, M.P. (2000). Spatial frequency maps in cat visual cortex. Journal of Neuroscience 20, 8504–8514.CrossRefGoogle Scholar
Kaschube, M., Coppola, D.M., Löwel, S., Wolf, F., & White, L.E. (2002). Quantifying the variability of orientation maps in ferret visual cortex. Society for Neuroscience Abstracts 28, #159. 17.Google Scholar
Katz, L.C. & Crowley, J.C. (2002). Development of cortical circuits: Lessons from ocular dominance columns. Nature Reviews Neuroscience 3, 34–42.CrossRefGoogle Scholar
Kee, C., Hung, L., Qiao, Y., Habib, A., & Smith, E.L. (2002). Prevalence of astigmatism in infant monkeys. Vision Research 42, 1349–1359.CrossRefGoogle Scholar
Keil, M.S. & Cristóbal, G. (2000). Separating the chaff from the wheat: Possible origins of the oblique effect. Journal of the Optical Society of America A 17, 697–710.CrossRefGoogle Scholar
Kennedy, H. & Orban, G.A. (1979). Preferences for horizontal or vertical orientation in cat visual cortical neurons. Journal of Physiology (London) 296, 61P–62P.Google Scholar
Krug, K., Akerman, C.J., & Thompson, I.D. (2001). Responses of neurons in neonatal cortex and thalamus to patterned visual stimulation through the naturally closed lids. Journal of Neurophysiology 85, 1436–1443.CrossRefGoogle Scholar
Leventhal, A.G. & Hirsch, H.V.B. (1977). Effects of early experience upon orientation sensitivity and binocularity of neurons in visual cortex of cats. Proceedings of the National Academy of Sciences of the U.S.A. 74, 1272–1276.CrossRefGoogle Scholar
Leventhal, A.G. & Hirsch, H.V.B. (1980). Receptive-field properties of different classes of neurons in visual cortex of normal and dark-reared cats. Journal of Neurophysiology 43, 1111–1132.CrossRefGoogle Scholar
Li, B.W., Peterson, M.R., & Freeman, R.D. (2003). The oblique effect: A neural basis in the striate cortex. Journal of Neurophysiology 90, 204–217.CrossRefGoogle Scholar
Löwel, S., Freeman, B., & Singer, W. (1987). Topographical organization of the orientation column in system in large flat-mounts of the cat visual cortex: A 2-deoxyglucose study. Journal of Comparative Neurology 255, 401–415.CrossRefGoogle Scholar
Luhmann, H.J., Martinez-Millen, L., & Singer, W. (1986). Development of horizontal intrinsic connections in striate cortex. Experimental Brain Research 63, 443–448.CrossRefGoogle Scholar
Mansfield, R.J. & Ronner, S.F. (1978). Orientation anisotropy in monkey visual cortex. Brain Research 149, 229–234.CrossRefGoogle Scholar
Mante, V. & Carandini, M. (2003). Visual cortex: Seeing motion. Current Biology 13, R906–R908.CrossRefGoogle Scholar
McMahon, M.J. & MacLeod, D.I.A. (2003). The origin of the oblique effect examined with pattern adaptation and masking. Journal of Vision 3, 230–239.Google Scholar
Mitchell, D.E., Freeman, R.D., Millodot, M., & Haegerstrom, G. (1973). Meridional amblyopia: Evidence for modification of the human visual system by early visual experience. Vision Research 13, 535–558.CrossRefGoogle Scholar
Monier, C., Chavane, F., Baudot, P., Graham, L.J., & Frégnac, Y. (2003). Orientation and direction selectivity of synaptic inputs in visual cortical neurons: A diversity of combinations produces spike tuning. Neuron 37, 663–680.CrossRefGoogle Scholar
Mower, G.D. (1991). The effect of dark-rearing on the time course of the critical period in cat visual cortex. Developmental Brain Research 58, 151–158.CrossRefGoogle Scholar
Müller, J.R., Metha, A.B., Krauskopf, J., & Lennie, P. (2001). Rapid adaptation in visual cortex to the structure of images. Science 285, 1405–1408.Google Scholar
Müller, T., Stetter, M., Hübener, M., Sengpiel, F., Bonhoeffer, T., Gödecke, I., Chapman, B., Löwel, S., & Obermayer, K. (2000). An analysis of orientation and ocular dominance patterns in the visual cortex of cats and ferrets. Neural Computation 12, 2573–2595.CrossRefGoogle Scholar
Nelson, D.A. & Katz, L.C. (1995). Emergence of functional circuits in ferret visual cortex visualized by optical imaging. Neuron 15, 23–34.CrossRefGoogle Scholar
Orban, G.A., Vandenbussche, E., & Vogels, R. (1984). Human orientation discrimination tested with long stimuli. Vision Research 24, 121–128.CrossRefGoogle Scholar
Payne, B.R. & Berman, N.E.J. (1983). Functional organization of neurons in cat striate cortex: Variations in preferred orientation and orientation selectivity with receptive-field type, ocular dominance, and location in visual-field map. Journal of Neurophysiology 49, 1051–1072.CrossRefGoogle Scholar
Pettigrew, J.D., Nikara, T., & Bishop, P.O. (1968). Responses to moving slits by single units. Experimental Brain Research 6, 373–390.Google Scholar
Purves, D. & Lotto, R.B. (2003). Why We See What We Do. Sunderlund, Massachusetts: Sinauer Associates, Inc..
Rao, S.C., Toth, L.J., & Sur, M. (1997). Optical imaged maps of orientation preference in primary visual cortex of cats and ferrets. Journal of Comparative Neurology 387, 358–370.Google Scholar
Ruthazer, E.S. & Stryker, M.P. (1996). The role of activity in the development of long-range horizontal connections in area 17 of the ferret. Journal of Neuroscience 16, 7253–7269.Google Scholar
Ruthazer, E.S., Baker, G.E., & Stryker, M.P. (1999). Development and organization of ocular dominance bands in primary visual cortex of the sable ferret. Journal of Comparative Neurology 407, 151–165.3.0.CO;2-1>CrossRefGoogle Scholar
Sengpiel, F., Stawinski, P., & Bonhoeffer, T. (1999). Influence of experience on orientation maps in cat visual cortex. Nature Neuroscience 2, 727–732.CrossRefGoogle Scholar
Sherman, S.M. & Spear, P.D. (1982). Organization of visual pathways in normal and visually deprived cats. Physiological Reviews 62, 738–855.CrossRefGoogle Scholar
Sherman, S.M. & Stone, J. (1973). Physiological normality of the retinal in visually deprived cats. Brain Research 60, 224–230.CrossRefGoogle Scholar
Skottun, B.C., Zhang, J., & Grosof, D.H. (1994). On the direction selectivity of cells in the visual cortex to drifting dot patterns. Visual Neuroscience 11, 885–897CrossRefGoogle Scholar
Swindale, N.V., Matsubara, J.A., & Cynader, M.S. (1987). Surface organization of orientation and direction selectivity in cat area 18. Journal of Neuroscience 7, 1414–1427.CrossRefGoogle Scholar
Swindale, N.V., Shoham, D., Grinvald, A., Bonhoeffer, T., & Hübener, M. (2000). Visual cortex maps are optimized for uniform coverage. Nature Neuroscience 3, 822–826.CrossRefGoogle Scholar
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 Scholar
Vitek, D.J., Schall, J.D., & Leventhal, A.G. (1985). Morphology, central projections, and dendritic field orientation of retinal ganglion cells in the ferret. Journal of Comparative Neurology 241, 1–11.Google Scholar
Wallman, J. (1993). Retinal control of eye growth and refraction. Progress in Retinal Research 12, 134–153.Google Scholar
Wang, G., Ding, S., & Yunokuchi, K. (2003). Difference in the representation of cardinal and oblique contours in cat visual cortex. Neuroscience Letters 338, 77–81.CrossRefGoogle Scholar
White, L.E., Bosking, W.H., & Fitzpatrick, D. (2001a). Consistent mapping of orientation preference across irregular functional domains in ferret visual cortex. Visual Neuroscience 18, 65–76.Google Scholar
White, L.E., Bosking, W.H., Williams, S.M., & Fitzpatrick, D. (1999). Maps of central visual space in ferret V1 and V2 lack matching inputs from the two eyes. Journal of Neuroscience 19, 7089–7099.Google Scholar
White, L.E., Coppola, D.M., & Fitzpatrick, D. (2001b). The contribution of sensory experience to the development of orientation maps in ferret visual cortex. Nature 411, 1049–1052.Google Scholar
Wiesel, T.N. & Hubel, D.H. (1974). Ordered arrangement of orientation columns in monkeys lacking visual experience. Journal of Comparative Neurology 158, 307–318.CrossRefGoogle Scholar
Wiesel, T.N. & Raviola, E. (1977). Myopia and eye enlargement after neonatal lid fusion in monkeys. Nature 266, 66–68.CrossRefGoogle Scholar
Wingate, R.J.T., FitzGibbon, T., & Thompson, I.D. (1992). Lucifer yellow, retrograde tracers, and fractal analysis characterise adult ferret retinal ganglion cells. Journal of Comparative Neurology 323, 449–474.CrossRefGoogle Scholar
Yinon, U., Koslowe, K.C., & Rassin, M.I. (1984). The optical effects of eyelid closure on the eyes of kittens reared in light and dark. Current Eye Research 3, 431–439.CrossRefGoogle Scholar