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Distribution and specificity of S-cone (“blue cone”) signals in subcortical visual pathways

Published online by Cambridge University Press:  20 February 2014

PAUL R. MARTIN*
Affiliation:
Department of Ophthalmology and Save Sight Institute, The University of Sydney, Sydney, New South Wales, Australia Australian Research Council Centre of Excellence in Vision Science, The University of Sydney, Sydney, New South Wales, Australia
BARRY B. LEE
Affiliation:
SUNY College of Optometry, New York, New York Max Planck Institute for Biophysical Chemistry, Göttingen, Germany

Abstract

We review here the distribution of S-cone signals and properties of S-cone recipient receptive fields in subcortical pathways. Nearly everything we know about S-cone signals in the subcortical visual system comes from the study of visual systems in cats and primates (monkeys); in this review, we concentrate on results from macaque and marmoset monkeys. We discuss segregation of S-cone recipient (blue-on and blue-off) receptive fields in the dorsal lateral geniculate nucleus and describe their receptive field properties. We treat in some detail the question of detecting weak S-cone signals as an introduction for newcomers to the field. Finally, we briefly consider the question on how S-cone signals are distributed among nongeniculate targets.

Type
Review Articles
Copyright
Copyright © Cambridge University Press 2014 

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References

Buzás, P., Kóbor, P., Petykó, Z., Telkes, I., Martin, P.R. & Lénárd, L. (2013). Receptive field properties of color opponent neurons in the cat lateral geniculate nucleus. The Journal of Neuroscience 33, 14511461.Google Scholar
Chatterjee, S. & Callaway, E.M. (2002). S cone contributions to the magnocellular visual pathway in macaque monkey. Neuron 35, 11351146.CrossRefGoogle Scholar
Chatterjee, S. & Callaway, E.M. (2003). Parallel colour-opponent pathways to primary visual cortex. Nature 426, 668671.Google Scholar
Cheong, S.K., Tailby, C., Martin, P.R., Levitt, J.B. & Solomon, S.G. (2011). Slow intrinsic rhythm in the koniocellular visual pathway. Proceedings of the National Academy of Sciences of the United States of America 108, 1465914663.CrossRefGoogle ScholarPubMed
Cheong, S.K., Tailby, C., Solomon, S.G. & Martin, P.R. (2013). Cortical-like receptive fields in the lateral geniculate nucleus of marmoset monkeys. The Journal of Neuroscience 33, 68646876.CrossRefGoogle ScholarPubMed
Chichilnisky, E.J. & Baylor, D.A. (1999). Receptive-field microstructure of blue-yellow ganglion cells in primate retina. Nature Neuroscience 2, 889893.CrossRefGoogle ScholarPubMed
Cleland, B.G., Levick, W.R., Morstyn, R. & Wagner, H.G. (1976). Lateral geniculate relay of slowly-conducting retinal afferents to cat visual cortex. The Journal of Physiology 255, 299320.Google Scholar
Conway, B.R., Chatterjee, S., Field, G.D., Horwitz, G.D., Johnson, E.N., Koida, K. & Mancuso, K. (2010). Advances in color science: From retina to behavior. The Journal of Neuroscience 30, 1495514963.Google Scholar
Creutzfeldt, O., Lee, B.B. & Valberg, A. (1986). Colour and brightness signals of parvocellular lateral geniculate neurons. Experimental Brain Research 63, 2134.Google Scholar
Croner, L.J. & Kaplan, E. (1995). Receptive fields of P and M ganglion cells across the primate retina. Vision Research 35, 724.Google Scholar
Crook, J.D., Davenport, C.M., Peterson, B.B., Packer, O.S., Detwiler, P.B. & Dacey, D.M. (2009). Parallel ON and OFF cone bipolar inputs establish spatially coextensive receptive field structure of blue-yellow ganglion cells in primate retina. The Journal of Neuroscience 29, 83728387.CrossRefGoogle ScholarPubMed
Crook, J.M., Lee, B.B., Tigwell, D.A. & Valberg, A. (1987). Thresholds to chromatic spots of cells in the macaque geniculate nucleus as compared to detection sensitivity in man. The Journal of Physiology 392, 193211.CrossRefGoogle ScholarPubMed
Dacey, D.M., Crook, J.D. & Packer, O.S. (2013). Distinct synaptic mechanisms create parallel S-ON and S-OFF color opponent pathways in the primate retina. Visual Neuroscience, 113.Google Scholar
Dacey, D.M., Liao, H.W., Peterson, B.B., Robinson, F.R., Smith, V.C., Pokorny, J., Yau, K.W. & Gamlin, P.D. (2005). Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433, 749754.CrossRefGoogle 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, 421427.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, 1527.CrossRefGoogle ScholarPubMed
DeMonasterio, F.M. (1979). Asymmetry of on- and off-pathways of blue sensitive-cones of the retina of macaques. Brain Research 166, 3948.CrossRefGoogle Scholar
DeMonasterio, F.M. & Gouras, P. (1975). Functional properties of ganglion cells of the rhesus monkey retina. The Journal of Physiology 251, 167195.Google Scholar
DeMonasterio, F.M., Gouras, P. & Tolhurst, D.J. (1975). Trichromatic colour opponency in ganglion cells of the rhesus monkey retina. The Journal of Physiology 251, 197216.Google Scholar
Derrington, A.M., Krauskopf, J. & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. The Journal of Physiology 357, 241265.Google Scholar
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. The Journal of Physiology 357, 219240.Google Scholar
DeValois, R.L. (1960). Colour vision mechanisms in monkey. The Journal of General Physiology 43, 115.CrossRefGoogle Scholar
DeValois, R.L., Abramov, I. & Jacobs, G.H. (1966). Analysis of response patterns of LGN cells. Journal of the Optical Society of America 56, 966977.CrossRefGoogle Scholar
DeValois, R.L., Cottaris, N.P., Elfar, S.D., Mahon, L.E. & Wilson, J.A. (2000). Some transformations of color information from lateral geniculate nucleus to striate cortex. Proceedings of the National Academy of Sciences of the United States of America 97, 49975002.Google Scholar
Diller, L., Packer, O.S., Verweij, J., McMahon, M.J., Williams, D.R. & Dacey, D.M (2004). L and M cone contributions to the midget and parasol ganglion cell receptive fields of macaque monkey retina. The Journal of Neuroscience 24, 10791088.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. The Journal of Physiology 258, 433452.Google Scholar
Enroth-Cugell, C. & Robson, J. (1966). The contrast sensitivity of retinal ganglion cells of the cat. The Journal of Physiology 187, 517552.Google Scholar
Field, G.D., Gauthier, J.L., Sher, A., Greschner, M., Machado, T.A., Jepson, L.H., Shlens, J., Gunning, D.E., Mathieson, K., Dabrowski, W., Paninski, L., Litke, A.M. & Chichilnisky, E.J. (2010). Functional connectivity in the retina at the resolution of photoreceptors. Nature 467, 673677.Google Scholar
Field, G.D., Sher, A., Gauthier, J.L., Greschner, M., Shlens, J., Litke, A.M. & Chichilnisky, E.J. (2007). Spatial properties and functional organization of small bistratified ganglion cells in primate retina. The Journal of Neuroscience 27, 1326113272.CrossRefGoogle ScholarPubMed
Forte, J.D., Hashemi-Nezhad, M., Dobbie, W.J., Dreher, B. & Martin, P.R. (2005). Spatial coding and response redundancy in parallel visual pathways of the marmoset Callithrix jacchus. Visual Neuroscience 22, 479491.Google Scholar
Gielen, C.C.A.M., van Gisbergen, J.A.M. & Vendrik, A.J.H. (1982). Reconstruction of cone-system contributions to responses of colour-opponent neurones in monkey lateral geniculate. Biological Cybernetics 44, 211221.CrossRefGoogle ScholarPubMed
Gouras, P. (1968). Identification of cone mechanisms in monkey ganglion cells. The Journal of Physiology 199, 533547.Google Scholar
Hammond, B.R. Jr., Wooten, B.R. & Snodderly, D.M. (1997). Individual variations in the spatial profile of human macular pigment. Journal of the Optical Society of America A, Optics, Image Science and Vision 14, 11871196.Google Scholar
Hashemi-Nezhad, M., Blessing, E.M., Dreher, B. & Martin, P.R. (2008). Segregation of short-wavelength sensitive (“blue”) cone signals among neurons in the lateral geniculate nucleus and striate cortex of marmosets. Vision Research 48, 26042614.Google Scholar
Hendry, S.H.C. & Reid, R.C. (2000). The koniocellular pathway in primate vision. Annual Review of Neuroscience 23, 127153.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1960). Receptive fields of optic nerve fibres in the spider monkey. The Journal of Physiology 154, 572580.Google Scholar
Hunt, D.M. & Peichl, L. (2013). S cones: Evolution, retinal distribution, development, and spectral sensitivity. Visual Neuroscience, 124.Google Scholar
Jacobs, G.H. (2008). Primate color vision: A comparative perspective. Visual Neuroscience 25, 619633.CrossRefGoogle ScholarPubMed
Kaas, J.H., Huerta, M.F., Weber, J.T. & Harting, J.K. (1978). Patterns of retinal terminations and laminar organization of the lateral geniculate nucleus of primates. The Journal of Comparative Neurology 182, 517554.Google Scholar
Kaplan, E. & Shapley, R.M. (1986). The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proceedings of the National Academy of Sciences of the United States of America 83, 27552757.Google Scholar
Kilavik, B.E., Silveira, L.C. & Kremers, J. (2003). Centre and surround responses of marmoset lateral geniculate neurones at different temporal frequencies. The Journal of Physiology 546, 903919.Google Scholar
Klug, K., Herr, S., Ngo, I.T., Sterling, P. & Schein, S. (2003). Macaque retina contains an S-cone OFF midget pathway. The Journal of Neuroscience 23, 98819887.Google Scholar
Kremers, J., Weiss, S. & Silveira, L.C. (2004). Spatiotemporal properties of the magno and parvocellular neurons of the lateral geniculate nucleus of the marmoset (Callithrix jacchus). Neurociências 1, 138149.Google Scholar
Lamb, T.D. (1995). Photoreceptor spectral sensitivities: Common shape in the long-wavelength region. Vision Research 35, 30833091.Google Scholar
Lee, B.B. (2008). Neural models and physiological reality. Visual Neuroscience 25, 231241.Google Scholar
Lee, B.B., Martin, P.R. & Grünert, U. (2010). Retinal connectivity and primate vision (review). Progress in Retinal and Eye Research 29, 622639.Google Scholar
Lee, B.B., Shapley, R.M., Hawken, M.J. & Sun, H. (2012). Spatial distributions of cone inputs to cells of the parvocellular pathway investigated with cone-isolating gratings. Journal of the Optical Society of America A, Optics, Image Science, and Vision 29, A223A232.CrossRefGoogle ScholarPubMed
Lee, B.B., Valberg, A., Tigwell, D.A. & Tryti, J. (1987). An account of responses of spectrally opponent neurons in macaque lateral geniculate nucleus to successive contrast. Proceedings of the Royal Society of London. Series B 230, 293314.Google Scholar
Lee, B.B., Virsu, V. & Elepfandt, A. (1983). Cell responses in dorsal layers of macaque lateral geniculate nucleus as a function of intensity and wavelength. Journal of Neurophysiology 50, 849863.Google Scholar
Lee, S.C.S. & Grünert, U. (2007). Connections of diffuse bipolar cells in primate retina are biased against S-cones. The Journal of Comparative Neurology 502, 126140.Google Scholar
Lee, S.C.S., Telkes, I. & Grünert, U (2005). S-cones do not contribute to the OFF-midget pathway in the retina of the marmoset, Callithrix jacchus. The European Journal of Neuroscience 22, 437447.CrossRefGoogle ScholarPubMed
Lennie, P. & Movshon, J.A. (2005). Coding of color and form in the geniculostriate visual pathway. Journal of the Optical Society of America A, Optics and Image Science and Vision 22, 20132033.Google Scholar
Malpeli, J.G. & Schiller, P.H. (1978). Lack of blue OFF-center cells in the visual system of the monkey. Brain Research 141, 385389.Google Scholar
Marc, R.E. & Sperling, H.G. (1977). Chromatic organization of primate cones. Science 196, 454456.CrossRefGoogle ScholarPubMed
Martin, P.R., Blessing, E.M., Buzás, P., Szmajda, B.A. & Forte, J.D. (2011). Transmission of colour and acuity signals by parvocellular cells in marmoset monkeys. The Journal of Physiology 589, 27952812.CrossRefGoogle ScholarPubMed
Martin, P.R. & Grünert, U. (1999). Analysis of the short wavelength sensitive (“blue”) cone mosaic in the primate retina: A comparison of new world and old world monkeys. The Journal of Comparative Neurology 406, 114.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
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. The European Journal of Neuroscience 9, 15361541.Google Scholar
McMahon, M.J., Lankheet, M.J.M., Lennie, P. & Williams, D.R. (2000). Fine structure of parvocellular receptive fields in the primate fovea revealed by laser interferometry. The Journal of Neuroscience 20, 20432053.Google Scholar
Michael, C.R. (1973). Opponent-color and opponent-contrast cells in lateral geniculate nucleus of the ground squirrel. Journal of Neurophysiology 36, 536550.Google Scholar
Miyagishima, K.J., Grünert, U. & Li, W. (2013). Processing of S-cone signals in the inner plexiform layer of the mammalian retina. Visual Neuroscience, 111.Google ScholarPubMed
Mollon, J.D. (1989). “Tho’ she kneel’d in the place where they grew…” The uses and origins of primate colour vision. The Journal of Experimental Biology 146, 2138.Google Scholar
Nathans, J. (1999). The evolution and physiology of human color vision: Insights from molecular genetic studies of visual pigments. Neuron 24, 299312.CrossRefGoogle ScholarPubMed
Pearlman, A.L. & Daw, N.W. (1970). Opponent color cells in the cat lateral geniculate nucleus. Science 167, 8486.CrossRefGoogle ScholarPubMed
Reid, R.C. & Shapley, R.M. (2002). Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus. The Journal of Neuroscience 22, 61586175.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. 8393. London: Plenum Press.CrossRefGoogle Scholar
Rodieck, R.W. & Stone, J. (1965). Analysis of receptive fields of cat retinal ganglion cells. Journal of Neurophysiology 28, 833849.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Watanabe, M. (1993). Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus, and parvicellular laminae of the lateral geniculate nucleus. The Journal of Comparative Neurology 338, 289303.Google Scholar
Roorda, A. & Williams, D.R. (1999). The arrangement of the three cone classes in the living human eye. Nature 397, 520522.CrossRefGoogle ScholarPubMed
Roy, S., Martin, P.R., Dreher, B., Saalmann, Y.B., Hu, D. & Vidyasagar, T.R. (2009). Segregation of short-wavelength sensitive (S) cone signals in the macaque dorsal lateral geniculate nucleus. The European Journal of Neuroscience 30, 15171526.Google Scholar
Sand, A., Schmidt, T.M. & Kofuji, P. (2012). Diverse types of ganglion cell photoreceptors in the mammalian retina. Progress in Retinal and Eye Research 31, 287302.Google Scholar
Schiller, P.H. & Malpeli, J.G. (1978). Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. Journal of Neurophysiology 41, 788797.Google Scholar
Shyue, S.K., Hewett-Emmett, D., Sperling, H.G., Hunt, D.M., Bowmaker, J.K., Mollon, J.D. & Li, W.H. (1995). Adaptive evolution of color vision genes in higher primates. Science 269, 12651267.Google Scholar
Sincich, L.C., Zhang, Y., Tiruveedhula, P., Horton, J.C. & Roorda, A. (2009). Resolving single cone inputs to visual receptive fields. Nature Neuroscience 12, 967969.Google Scholar
Smith, V.C. & Pokorny, J. (1975). Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm. Vision Research 15, 161171.Google Scholar
Snodderly, D.M., Auran, J.D. & Delori, F.C. (1984 a). The macular pigment. II. Spatial distribution in primate retinas. Investigative Ophthalmology & Visual Science 25, 674685.Google ScholarPubMed
Snodderly, D.M., Brown, P.K., Delori, F.C. & Auran, J.D. (1984 b). The macular pigment. I. Absorbance spectra, localization, and discrimination from other yellow pigments in primate retinas. Investigative Ophthalmology & Visual Science 25, 660673.Google Scholar
Solomon, S.G., Lee, B.B., White, A.J., Rüttiger, L. & Martin, P.R. (2005). Chromatic organization of ganglion cell receptive fields in the peripheral retina. The Journal of Neuroscience 25, 45274539.Google Scholar
Solomon, S.G., Tailby, C., Cheong, S.K. & Camp, A.J. (2010). Linear and non-linear contributions to the visual sensitivity of neurons in primate lateral geniculate nucleus. Journal of Neurophysiology 104, 18841898.Google Scholar
Stockman, A., MacLeod, D.I. & Johnson, N.E. (1993). Spectral sensitivities of the human cones. Journal of the Optical Society of America A, Optics and Image Science and Vision 10, 24912521.CrossRefGoogle ScholarPubMed
Sun, H., Smithson, H.E., Zaidi, Q. & Lee, B.B. (2006 a). Do magnocellular and parvocellular ganglion cells avoid short-wavelength cone input? Visual Neuroscience 23, 441446.Google Scholar
Sun, H., Smithson, H.E., Zaidi, Q. & Lee, B.B. (2006 b). Specificity of cone inputs to macaque retinal ganglion cells. Journal of Neurophysiology 95, 837849.Google Scholar
Szmajda, B.A., Buzás, P., FitzGibbon, T. & Martin, P.R. (2006). Geniculocortical relay of blue-off signals in the primate visual system. Proceedings of the National Academy of Sciences of the United States of America 103, 1951219517.CrossRefGoogle ScholarPubMed
Szmajda, B.A., Martin, P.R. & Grünert, U. (2008). Retinal ganglion cell inputs to the koniocellular pathway. The Journal of Comparative Neurology 510, 251268.Google Scholar
Tailby, C., Dobbie, W.J., Hashemi-Nezhad, M., Forte, J.D. & Martin, P.R. (2010). Receptive field asymmetries produce color-dependent direction selectivity in primate lateral geniculate nucleus. Journal of Vision 10, 118.Google Scholar
Tailby, C., Solomon, S.G. & Lennie, P. (2008 a). Functional asymmetries in visual pathways carrying S-cone signals in macaque. The Journal of Neuroscience 28, 40784087.CrossRefGoogle ScholarPubMed
Tailby, C., Szmajda, B.A., Buzás, P., Lee, B.B. & Martin, P.R. (2008 b). Transmission of blue (S) cone signals through the primate lateral geniculate nucleus. Journal of Physiology 586, 59475967.Google Scholar
Tovée, M.J., Bowmaker, J.K. & Mollon, J.D. (1992). The relationship between cone pigments and behavioural sensitivity in a New World monkey (Callithrix jacchus jacchus). Vision Research 32, 867878.Google Scholar
Valberg, A., Lee, B.B. & Tigwell, D.A. (1986). Neurones with strong inhibitory s-cone inputs in the macaque lateral geniculate nucleus. Vision Research 26, 10611064.Google Scholar
Walls, G.L. (1953). The Lateral Geniculate Nucleus and Visual Histophysiology. University of California Press, Berkeley.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. The Journal of Physiology 533, 519535.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, 11151156.Google Scholar
Wikler, K.C. & Rakic, P. (1990). Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates. The Journal of Neuroscience 10, 33903401.Google Scholar
Wilson, P.D., Rowe, M.H. & Stone, J. (1976). Properties of relay cells in cat’s lateral geniculate nucleus: A comparison of W-cells with X- and Y-cells. Journal of Neurophysiology 39, 11931209.Google Scholar
Wyszecki, G. & Stiles, W.S. (1982). Color Science: Concepts and Methods, Quantitative Data and Formulae. New York: Wiley.Google Scholar
Xiao, Y. (2013). Processing of the S-cone signals in the early visual cortex of primates. Visual Neuroscience, 17.Google Scholar
Yeh, T., Lee, B.B. & Kremers, J. (1995 a). Temporal response of ganglion cells of the macaque retina to cone-specific modulation. Journal of the Optical Society of America A Optics, Image Science, and Vision 12, 456464.CrossRefGoogle ScholarPubMed
Yeh, T., Lee, B.B., Kremers, J., Cowing, J.A., Hunt, D.M., Martin, P.R. & Troy, J.B. (1995 b). Visual responses in the lateral geniculate nucleus of dichromatic and trichromatic marmosets (Callithrix jacchus). The Journal of Neuroscience 15, 78927904.Google Scholar