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Spatial coding and response redundancy in parallel visual pathways of the marmoset Callithrix jacchus

Published online by Cambridge University Press:  06 October 2005

JASON D. FORTE ,
MAZIAR HASHEMI-NEZHAD ,
WILLIAM J. DOBBIE ,
BOGDAN DREHER  and
PAUL R. MARTIN
JASON D. FORTE
Affiliation:
National Vision Research Institute of Australia, Cnr Keppel & Cardigan Streets, Carlton, Australia Department of Optometry and Vision Sciences, The University of Melbourne, Parkville, Australia
MAZIAR HASHEMI-NEZHAD
Affiliation:
Department of Anatomy & Histology and Institute for Biomedical Research, School of Medical Sciences, The University of Sydney, Australia
WILLIAM J. DOBBIE
Affiliation:
National Vision Research Institute of Australia, Cnr Keppel & Cardigan Streets, Carlton, Australia Department of Optometry and Vision Sciences, The University of Melbourne, Parkville, Australia
BOGDAN DREHER
Affiliation:
Department of Anatomy & Histology and Institute for Biomedical Research, School of Medical Sciences, The University of Sydney, Australia
PAUL R. MARTIN
Affiliation:
National Vision Research Institute of Australia, Cnr Keppel & Cardigan Streets, Carlton, Australia Department of Optometry and Vision Sciences, The University of Melbourne, Parkville, Australia
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Abstract

Many neurons in the primary visual cortex (area V1) show pronounced selectivity for the orientation and spatial frequency of visual stimuli, whereas most neurons in subcortical afferent streams show little selectivity for these stimulus attributes. It has been suggested that this transformation is a functional sign of increased coding efficiency, whereby the redundancy (or overlap in response properties) is reduced at consecutive levels of visual processing. Here we compared experimentally the response redundancy in area V1 with that in the three main dorsal thalamic afferent streams, the parvocellular (PC), koniocellular (KC), and magnocellular (MC) divisions of the dorsal lateral geniculate nucleus (LGN) in marmosets. The spatial frequency and orientation tuning of single cells in the LGN and area V1 were measured, using luminance contrast sine-wave gratings. A joint spatial frequency-orientation response selectivity profile was calculated for each cell. Response redundancy for each population was estimated by cross-multiplication of the joint selectivity profiles for pairs of cells. We show that when estimated in this way, redundancy in LGN neurons is approximately double that of neurons in cortical area V1. However, there are differences between LGN subdivisions, such that the KC pathway has a spatial representation that lies between the redundant code of the PC and MC pathways and the more efficient sparse spatial code of area V1.

Keywords

Spatial visionParvocellularMagnocellularKoniocellularVisual cortexLateral geniculate nucleus
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 4 , July 2005 , pp. 479 - 491
Copyright
2005 Cambridge University Press

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References

REFERENCES

Barlow, H.B. (1997). The knowledge used in vision and where it comes from. Philosophical Transactions of the Royal Society B (London) 352, 1141–1147.Google Scholar
Barlow, H.B. (1981). Critical limiting factors in the design of the eye and visual cortex. Proceedings of the Royal Society B (London) 212, 1–34.Google Scholar
Berman, N.E., Wilkes, M.E., & Payne, B.R. (1987). Organization of orientation and direction selectivity in areas 17 and 18 of cat cerebral cortex. Journal of Neurophysiology 58, 676–699.Google Scholar
Blessing, E.M., Solomon, S.G., Hashemi-Nezhad, M., Morris, B.J., & Martin, P.R. (2004). Chromatic and spatial properties of parvocellular cells in the lateral geniculate nucleus of the marmoset (Callithrix jacchus). Journal of Physiology 557, 229–245.Google Scholar
Bredfeldt, C.E. & Ringach, D.L. (2002). Dynamics of spatial frequency tuning in macaque V1. Journal of Neuroscience 22, 1976–1984.Google Scholar
Bullier, J. & Henry, G.H. (1980). Ordinal position and afferent input of neurons in monkey striate cortex. Journal of Comparative Neurology 193, 913–935.Google Scholar
Bullier, J. & Kennedy, H. (1983). Projection of the lateral geniculate nucleus onto cortical area V2 in the macaque monkey. Experimental Brain Research 53, 168–72.Google Scholar
Campbell, F.W., Cleland, B.G., Cooper, G.F., & Enroth-Cugell, C. (1968a). The angular selectivity of visual cortical cells to moving gratings. Journal of Physiology 198, 227–250.Google Scholar
Campbell, F.W., Cooper, G.F., & Enroth-Cugell, C. (1968b). The spatial selectivity of visual cells of the cat. Journal of Physiology 203, 223–235.Google Scholar
Chen, G., Dan, Y., & Li, C.-Y. (2005). Stimulation of non-classical receptive field enhances orientation selectivity in the cat. Journal of Physiology 564, 233–243.Google Scholar
Dacey, D.M. (1993). Morphology of a small-field bistratified ganglion cell type in the macaque and human retina. Visual Neuroscience 10, 1081–1098.Google Scholar
Dacey, D.M. & Lee, B.B. (1994). The ‘blue-on’ opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367, 731–735.Google Scholar
Dacey, D.M. & Packer, O.S. (2003). Colour coding in the primate retina: Diverse cell types and cone-specific circuitry. Current Opinion in Neurobiology 13, 421–427.Google Scholar
Dacey, D.M., Peterson, B.B., Robinson, F.R., & Gamlin, P.D. (2003). Fireworks in the primate retina: In vitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 37, 15–27.Google Scholar
Dan, Y., Atick, J.J., & Reid, R.C. (1996). Efficient coding of natural scenes in the lateral geniculate nucleus: Experimental test of a computational theory. Journal of Neuroscience 16, 3351–3362.Google Scholar
Dawis, S., Shapley, R., Kaplan, E., & Tranchina, D. (1984). The receptive field organization of X-cells in the cat: Spatiotemporal coupling and asymmetry. Vision Research 24, 549–564.Google Scholar
De Valois, R.L., Yund, E.W., & Hepler, N. (1982a). The orientation and direction selectivity of cells in macaque visual cortex. Vision Research 22, 531–544.Google Scholar
De Valois, R.L., Albrecht, D.G., & Thorell, L.G. (1982b). Spatial frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545–559.Google Scholar
De Valois, R.L., Cottaris, N.P., Mahon, L.E., Elfar, S.D., & Wilson, J.A. (2000). Spatial and temporal receptive fields of geniculate and cortical cells and directional selectivity. Vision Research 40, 3685–3702.Google Scholar
Derrington, A.M., Krauskopf, J., & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. Journal of Physiology 357, 241–265.Google Scholar
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology 357, 219–240.Google Scholar
Dobbie, W.J., Solomon, S.G., Blessing, E.M., Hashemi-Nezhad, M., Forte, J., Dreher, B., & Martin, P.R. (2003). Spatiotemporal model for direction selectivity in blue-on cells in the primate lateral geniculate nucleus. Proceedings of the Australian Neuroscience Society 14, Program number 299.Google Scholar
Dow, B.M. (1974). Functional classes of cells and their laminar distribution in macaque visual cortex. Journal of Neurophysiology 37, 927–946.Google Scholar
Dreher, B., Fukada, Y., & Rodieck, R.W. (1976). Identification, classification and anatomical segregation of cells with X-like and Y-like properties in the lateral geniculate nucleus of Old-World primates. Journal of Physiology 258, 433–452.Google Scholar
Hawken, M.J. & Parker, A.J. (1984). Contrast sensitivity and orientation selectivity in lamina IV of the striate cortex of Old-World monkeys. Experimental Brain Research 54, 367–372.Google Scholar
Hendry, S.H.C. & Reid, R.C. (2000). The koniocellular pathway in primate vision. Annual Review of Neuroscience 23, 127–153.Google Scholar
Henry, G.H., Bishop, P.O., & Dreher, B. (1974a). Orientation, axis and direction as stimulus parameters for striate cells. Vision Research 14, 767–777.Google Scholar
Henry, G.H., Dreher, B., & Bishop, P.O. (1974b). Orientation specificity of cells in cat striate cortex. Journal of Neurophysiology 37, 1394–1409.Google Scholar
Henry, G.H., Michalski, A., Wimborne, B.M., & McCart, R.J. (1994). The nature and origin of orientation specificity in neurons of the visual pathway. Progress in Neurobiology 43, 381–437.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1959). Receptive fields of single neurones in the cat's striate cortex. Journal of Physiology 148, 574–591.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106–154.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology 195, 215–243.Google Scholar
Irvin, G.E., Norton, T.T., Sesma, M.A., & Casagrande, V.A. (1986). W-like response properties of interlaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus). Brain Research 362, 254–270.Google Scholar
Irvin, G.E., Casagrande, V.A., & Norton, T.T. (1993). Center/surround relationships of magnocellular, parvocellular, and koniocellular relay cells in primate lateral geniculate nucleus. Visual Neuroscience 10, 363–373.Google Scholar
Kaplan, E., Lee, B.B., & Shapley, R.M. (1989). New views of primate retinal function. In Progress in Retinal Research, ed. Osborne, N. & Chader, J., pp. 273–336. New York: Pergamon.
Kaplan, E. & Shapley, R.M. (1982). X and Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology 330, 125–143.Google Scholar
Kilavik, B.E., Silveira, L.C., & Kremers, J. (2003). Centre and surround responses of marmoset lateral geniculate neurones at different temporal frequencies. Journal of Physiology 546, 903–919.Google Scholar
Leventhal, A.G., Rodieck, R.W., & Dreher, B. (1981). Retinal ganglion cell classes in the Old World monkey: Morphology and central projections. Science 213, 1139–1142.Google Scholar
Levick, W.R. & Thibos, L.N. (1982). Analysis of orientation bias in cat retina. Journal of Physiology 329, 243–261.Google Scholar
Levitt, J.B., Tyler, C.J., & Lund, J.S. (1998). Receptive field properties of neurons in marmoset striate cortex. Society for Neuroscience Abstracts 24, 645 (254.2).Google Scholar
Maffei, L. & Fiorentini, A. (1973). The visual cortex as a spatial frequency analyser. Vision Research 13, 1255–1267.Google Scholar
Marcelja, S. (1979). Initial processing of visual information within the retina and the LGN. Biological Cybernetics 32, 217–226.Google Scholar
Martin, P.R. (2004). Colour through the thalamus. Clinical and Experimental Optometry 87, 249–257.Google Scholar
Martin, P.R., White, A.J.R., Goodchild, A.K., Wilder, H.D., & Sefton, A.E. (1997). Evidence that blue-on cells are part of the third geniculocortical pathway in primates. European Journal of Neuroscience 9, 1536–1541.Google Scholar
Mazer, J.A., Vinje, W.E., McDermott, J., Schiller, P.H., & Gallant, J.L. (2002). Spatial frequency and orientation tuning dynamics in area V1. Proceedings of the National Academy of Sciences of the U.S.A. 99, 1645–1650.Google Scholar
Mechler, F. & Ringach, D.L. (2002). On the classification of simple and complex cells. Vision Research 42, 1017–1033.Google Scholar
Norton, T.T. & Casagrande, V.A. (1982). Laminar organization of receptive-field properties in lateral geniculate nucleus of bush baby (Galago crassicaudatus). Journal of Neurophysiology 47, 715–741.Google Scholar
Olshausen, B.A. & Field, D.J. (1997). Sparse coding with an overcomplete basis set: A strategy employed by V1? Vision Research 37, 3311–3325.Google Scholar
Perry, V.H., Oehler, R., & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 1101–1123.Google Scholar
Reich, D.S., Mechler, F., & Victor, J.D. (2001). Independent and redundant information in nearby cortical neurons. Science 294, 2566–2568.Google Scholar
Rodieck, R.W. (1965). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Research 5, 583–601.Google Scholar
Rodieck, R.W. (1991). Which cells code for color? In From Pigments to Perception: Advances in Understanding Visual Processes, ed. Valberg, A. & Lee, B.B., pp. 83–93. London: Plenum Press.
Rodieck, R.W. (1998). The First Steps in Seeing. Sunderland, Massachusetts: Sinauer.
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and trans-species comparisons. Brain, Behavior and Evolution 23, 121–164.Google Scholar
Rodman, H.R., Gross, C.G., & Albright, T.D. (1989). Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal. Journal of Neuroscience 9, 2033–2050.Google Scholar
Rosa, M.G.P., Tweedale, R., & Elston, G.N. (2000). Visual responses of neurons in the middle temporal area of new world monkeys after lesions of striate cortex. Journal of Neuroscience 20, 5552–5563.Google Scholar
Rose, D. (1977). Responses of single units in cat visual cortex to moving bars of light as a function of bar length. Journal of Physiology 271, 1–23.Google Scholar
Sawatari, A. & Callaway, E.M. (1996). Convergence of magno- and parvocellular pathways in layer 4B of macaque primary visual cortex. Nature 380, 442–446.Google Scholar
Schein, S., Sterling, P., Ngo, I.T., Huang, T.M., & Herr, S. (2004). Evidence that each S cone in macaque fovea drives one narrow-field and several wide-field blue-yellow ganglion cells. Journal of Neuroscience 24, 8366–8378.Google Scholar
Schiller, P.H., Finlay, B.L., & Volman, S.F. (1976a). Quantitative studies of single-cell properties in monkey striate cortex. II. Orientation specificity and ocular dominance. Journal of Neurophysiology 39, 1320–1333.Google Scholar
Schiller, P.H., Finlay, B.L., & Volman, S.F. (1976b). Quantitative studies of single-cell properties in monkey striate cortex. III. Spatial frequency. Journal of Neurophysiology 39, 1334–1351.Google Scholar
Schwartz, O. & Simoncelli, E.P. (2001). Natural signals statistics and sensory gain control. Nature Neuroscience 4, 819–825.Google Scholar
Shou, T. & Leventhal, A.G. (1989). Organized arrangement of orientation-sensitive relay cells in the cat's dorsal lateral geniculate nucleus. Journal of Neuroscience 9, 4287–4302.Google Scholar
Silveira, L.C.L. & De Mello, H.D. (1998). Parallel pathways of primate vision—Sampling of information in the Fourier space by M and P cells. In Development and Organization of the Retina, ed. Chalupa, L.M. & Finlay, B.L., pp. 173–199. New York: Plenum Press.
Simoncelli, E.P. (2003). Vision and the statistics of the visual environment. Current Opinion in Neurobiology 13, 144–149.Google Scholar
Sincich, L.C., Park, K.F., Wohlgemuth, M.J., & Horton, J.C. (2004). Bypassing V1: A direct geniculate input to area MT. Nature Neuroscience 7, 1123–1128.Google Scholar
Skottun, B.C., De Valois, R.L., Grosof, D.H., Movshon, J.A., Albrecht, D.G., & Bonds, A.B. (1991). Classifying simple and complex cells on the basis of response modulation. Vision Research 31, 1079–1086.Google Scholar
Smith, E.L., Chino, Y.M., Ridder, W.H., Kitagawa, K., & Langston, A. (1990). Orientation bias of neurons in the lateral geniculate nucleus of macaque monkeys. Visual Neuroscience 5, 525–545.Google Scholar
Solomon, S.G., White, A.J.R., & Martin, P.R. (1999). Temporal contrast sensitivity in the lateral geniculate nucleus of a New World monkey, the marmoset Callithrix jacchus. Journal of Physiology 517, 907–917.Google Scholar
Solomon, S.G., White, A.J.R., & Martin, P.R. (2002). Extra-classical receptive field properties of parvocellular, magnocellular and koniocellular cells in the primate lateral geniculate nucleus. Journal of Neuroscience 22, 338–349.Google Scholar
Thibos, L.N. & Levick, W.R. (1985). Orientation bias of brisk-transient y-cells of the cat retina for drifting and altering gratings. Experimental Brain Research 58, 1–10.Google Scholar
Thompson, K.G., Zhou, Y., & Leventhal, A.G. (1994). Direction-sensitive X and Y cells within the A laminae of the cat's LGNd. Visual Neuroscience 11, 927–938.Google Scholar
Troilo, D., Howland, H.C., & Judge, S.J. (1993). Visual optics and retinal cone topography in the common marmoset (Callithrix jacchus). Vision Research 33, 1301–1310.Google Scholar
Vidyasagar, T.R. & Heide, W. (1984). Geniculate orientation biases seen with moving sine wave gratings: Implications for a model of simple cell afferent connectivity. Experimental Brain Research 57, 176–200.Google Scholar
Vidyasagar, T.R., Kulikowski, J.J., Lipnicki, D.M., & Dreher, B. (2002). Convergence of parvocellular and magnocellular information channels in the primary visual cortex of the macaque. European Journal of Neuroscience 16, 945–956.Google Scholar
Vinje, W.E. & Gallant, J.L. (2002). Natural stimulation of the nonclassical receptive field increases information transmission efficiency in V1. Journal of Neuroscience 22, 2904–2915.Google Scholar
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells of the primate retina. Journal of Comparative Neurology 289, 434–454.Google Scholar
Webster, M.A. & De Valois, R.L. (1985). Relationship between spatial-frequency and orientation tuning of striate-cortex cells. Journal of the Optical Society of America A 2, 1124–1132.Google Scholar
White, A.J.R., Goodchild, A.K., Wilder, H.D., Sefton, A.E., & Martin, P.R. (1998). Segregation of receptive field properties in the lateral geniculate nucleus of a New-World monkey, the marmoset Callithrix jacchus. Journal of Neurophysiology 80, 2063–2076.Google Scholar
White, A.J.R., Solomon, S.G., & Martin, P.R. (2001). Spatial properties of koniocellular cells in the lateral geniculate nucleus of the marmoset Callithrix jacchus. Journal of Physiology 533, 519–535.Google Scholar
Wiesel, T.N. & Hubel, D.H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. Journal of Neurophysiology 29, 1115–1156.Google Scholar
Xu, X., Ichida, J., Shostok, Y., Bonds, A.B., & Casagrande, V.A. (2002). Are primate lateral geniculate nucleus (LGN) cells really sensitive to orientation or direction? Visual Neuroscience 19, 97–108.Google Scholar
Yabuta, N.H., Sawatari, A., & Callaway, E.M. (2001). Two functional channels from primary visual cortex to dorsal visual cortical areas. Science 292, 297–300.Google Scholar
Yoshioka, T., Levitt, J.B., & Lund, J.S. (1994). Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: Anatomy of interlaminar projections. Visual Neuroscience 11, 467–489.Google Scholar
Yukie, M. & Iwai, E. (1981). Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys. Journal of Comparative Neurology 201, 81–97.Google Scholar