Abstract

Receptive fields of midget ganglion cells and parvocellular lateral geniculate nucleus (LGN) neurons show color-opponent responses because they receive antagonistic input from the middle- and long-wavelength sensitive cones. It has been controversial as to whether this opponency can derive from random connectivity; if receptive field centers of cells near the fovea are cone-specific due to midget morphology, this would confer some degree of color opponency even with random cone input to the surround. A simple test of this mixed surround hypothesis is to compare spatial frequency tuning curves for luminance gratings and gratings isolating cone input to the receptive field center. If tuning curves for luminance gratings were bandpass, then with the mixed surround hypothesis tuning curves for gratings isolating the receptive field center cone class should also be bandpass, but to a lesser extent than for luminance. Tuning curves for luminance, chromatic, and cone-isolating gratings were measured in macaque retinal ganglion cells and LGN cells. We defined and measured a bandpass index to compare luminance and center cone-isolating tuning curves. Midget retinal ganglion cells and parvocellular LGN cells had bandpass indices between 0.1 and 1 with luminance gratings, but the index was usually near 1 (meaning low-pass tuning) when the receptive field center cone class alone was modulated. This is strong evidence for a considerable degree of cone-specific input to the surround. A fraction of midget and parvocellular cells showed evidence of incomplete specificity. Fitting the data with receptive field models revealed considerable intercell variability, with indications in some cells of a more complex receptive structure than a simple difference of Gaussians model.

© 2012 Optical Society of America

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    [CrossRef]
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    [CrossRef]
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    [CrossRef]
  33. D. J. Calkins and P. Sterling, “Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina,” Nature 381, 613–615 (1996).
    [CrossRef]
  34. H. R. Joo, B. B. Peterson, T. J. Haun, and D. M. Dacey, “Characterization of a novel large-field cone bipolar cell type in the primate retina: evidence for selective cone connections,” Vis. Neurosci. 28, 29–37 (2011).
    [CrossRef]
  35. H. Wässle, U. Grünert, P. R. Martin, and B. B. Boycott, “Color coding in the primate retina: predictions and constrants from anatomy,” in Structural and Functional Organization of the Neocortex. A Symposium in the Memory of Otto D. Creutzfeldt, B. Albowitz, K. Albus, U. Kuhnt, H. Ch. Nothdurft, and P. Wahle, eds. (Springer, 1994), pp. 94–104.
  36. O. Packer, A. E. Hendrickson, and C. A. Curcio, “Photoreceptor topography of the retina in the adult pigtail macaque (macaca nemestrina),” J. Comp. Neurol. 288, 165–183 (1989).
    [CrossRef]
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    [CrossRef]

2011

J. D. Crook, M. B. Manookin, O. S. Packer, and D. M. Dacey, “Horizontal cell feedback without cone type-selective inhibition mediates “red-green” color opponency in midget ganglion cells of the primate retina,” J. Neurosci. 31, 1762–1772 (2011).
[CrossRef]

P. R. Martin, E. M. Blessing, P. Buzas, B. A. Szmajda, and J. D. Forte, “Transmission of colour and acuity signals by parvocellular cells in marmoset monkeys,” J. Physiol. 589, 2795–2812 (2011).
[CrossRef]

H. R. Joo, B. B. Peterson, T. J. Haun, and D. M. Dacey, “Characterization of a novel large-field cone bipolar cell type in the primate retina: evidence for selective cone connections,” Vis. Neurosci. 28, 29–37 (2011).
[CrossRef]

2010

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

B. B. Lee, P. R. Martin, and U. Grünert, “Retinal connectivity and primate vision,” Prog. Retin. Res. 29, 622–639 (2010).
[CrossRef]

2008

B. B. Lee, “Neural models and physiological reality,” Vis. Neurosci. 25, 231–241 (2008).
[CrossRef]

2006

P. Buzas, E. M. Blessing, B. A. Szmadja, and P. R. Martin, “Specificity of M and L cone inputs to receptive fields in the parvocellular pathway: random wiring with functional bias,” J. Neurosci. 26, 11148–11161 (2006).
[CrossRef]

2005

S. G. Solomon, B. B. Lee, A. J. White, L. Ruttiger, and P. R. Martin, “Chromatic organization of ganglion cell receptive fields in the peripheral retina,” J. Neurosci. 25, 4527–4539 (2005).
[CrossRef]

2002

R. C. Reid and R. M. Shapley, “Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus,” J. Neurosci. 22, 6158–6175 (2002).

2001

P. R. Martin, B. B. Lee, A. J. White, S. G. Solomon, and L. Rüttiger, “Chromatic sensitivity of ganglion cells in peripheral primate retina,” Nature 410, 933–936 (2001).
[CrossRef]

2000

1998

B. B. Lee, J. Kremers, and T. Yeh, “Receptive fields of primate ganglion cells studied with a novel technique,” Vis. Neurosci. 15, 161–175 (1998).
[CrossRef]

1997

E. A. Benardete and E. Kaplan, “The receptive field of the primate P retinal ganglion cell I: linear dynamics,” Vis. Neurosci. 14, 169–186 (1997).
[CrossRef]

1996

A. G. Shapiro, J. Pokorny, and V. C. Smith, “Cone-rod receptor spaces with illustrations that use CRT phosphor and light-emitting-diode spectra,” J. Opt. Soc. Am. A 13, 2319–2328 (1996).
[CrossRef]

D. J. Calkins and P. Sterling, “Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina,” Nature 381, 613–615 (1996).
[CrossRef]

K. T. Mullen and F. A. Kingdom, “Losses in peripheral colour sensitivity predicted from “hit or miss” post-receptoral cone connections,” Vis. Res. 36, 1995–2000 (1996).
[CrossRef]

1995

L. J. Croner and E. Kaplan, “Receptive fields of P and M ganglion cells across the primate retina,” Vis. Res. 35, 7–24 (1995).
[CrossRef]

1992

R. C. Reid and R. M. Shapley, “Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus,” Nature 356, 716–718 (1992).
[CrossRef]

1989

B. B. Lee, P. R. Martin, and A. Valberg, “Sensitivity of macaque retinal ganglion cells to chromatic and luminance flicker,” J. Physiol. 414, 223–243 (1989).

O. Packer, A. E. Hendrickson, and C. A. Curcio, “Photoreceptor topography of the retina in the adult pigtail macaque (macaca nemestrina),” J. Comp. Neurol. 288, 165–183 (1989).
[CrossRef]

1984

A. M. Derrington and P. Lennie, “Spatial and temporal contrast sensitivities of neurons in lateral geniculate nucleus of macaque,” J. Physiol. 357, 219–240 (1984).

E. Kaplan and R. Shapley, “The origin of the S (slow) potential in the mammalian lateral geniculate nucleus,” Exp. Brain Res. 55, 111–116 (1984).
[CrossRef]

1983

B. B. Lee, V. Virsu, and O. D. Creutzfeldt, “Linear signal transmission from prepotentials to cells in the macaque lateral geniculate nucleus,” Exp. Brain Res. 52, 50–56 (1983).
[CrossRef]

W. Paulus and A. Kröger-Paulus, “A new concept of retinal colour coding,” Vis. Res. 23, 529–540 (1983).
[CrossRef]

C. Enroth-Cugell, J. G. Robson, D. E. Schweitzer-Tong, and A. B. Watson, “Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation,” J. Physiol. 341, 279–307 (1983).

T. P. Hicks, B. B. Lee, and T. R. Vidyasagar, “The responses of cells in macaque lateral geniculate nucleus to sinusoidal gratings,” J. Physiol. 337, 183–200 (1983).

1981

B. B. Lee, V. Virsu, and A. Elepfandt, “Phase of responses to moving gratings in cells of the cat retina and lateral geniculate nucleus,” J. Neurophysiol. 45, 807–817 (1981).

1975

V. C. Smith and J. Pokorny, “Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm,” Vis. Res. 15, 161–171 (1975).
[CrossRef]

1972

E. G. Merrill and A. Ainsworth, “Glass-coated platinum-plated tungsten microelectrodes,” Med. Biol. Eng. 10, 662–672 (1972).
[CrossRef]

1969

B. B. Boycott and J. E. Dowling, “Organization of the primate retina: light microscopy,” Phil. Trans. R. Soc. Lond. B 255, 109–184 (1969).
[CrossRef]

1966

T. Wiesel and D. H. Hubel, “Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey,” J. Neurophysiol. 29, 1115–1156 (1966).

C. Enroth-Cugell and J. G. Robson, “The contrast sensitivity of retinal ganglion cells of the cat,” J. Physiol. 187, 517–552 (1966).

1965

R. L. DeValois, “Analysis and coding of color vision in the primate visual system,” Cold Spring Harb. Symp. Quant. Biol. 30, 567–579 (1965).
[CrossRef]

Ainsworth, A.

E. G. Merrill and A. Ainsworth, “Glass-coated platinum-plated tungsten microelectrodes,” Med. Biol. Eng. 10, 662–672 (1972).
[CrossRef]

Albright, T. D.

Benardete, E. A.

E. A. Benardete and E. Kaplan, “The receptive field of the primate P retinal ganglion cell I: linear dynamics,” Vis. Neurosci. 14, 169–186 (1997).
[CrossRef]

Blessing, E. M.

P. R. Martin, E. M. Blessing, P. Buzas, B. A. Szmajda, and J. D. Forte, “Transmission of colour and acuity signals by parvocellular cells in marmoset monkeys,” J. Physiol. 589, 2795–2812 (2011).
[CrossRef]

P. Buzas, E. M. Blessing, B. A. Szmadja, and P. R. Martin, “Specificity of M and L cone inputs to receptive fields in the parvocellular pathway: random wiring with functional bias,” J. Neurosci. 26, 11148–11161 (2006).
[CrossRef]

Boycott, B. B.

B. B. Boycott and J. E. Dowling, “Organization of the primate retina: light microscopy,” Phil. Trans. R. Soc. Lond. B 255, 109–184 (1969).
[CrossRef]

H. Wässle, U. Grünert, P. R. Martin, and B. B. Boycott, “Color coding in the primate retina: predictions and constrants from anatomy,” in Structural and Functional Organization of the Neocortex. A Symposium in the Memory of Otto D. Creutzfeldt, B. Albowitz, K. Albus, U. Kuhnt, H. Ch. Nothdurft, and P. Wahle, eds. (Springer, 1994), pp. 94–104.

Buzas, P.

P. R. Martin, E. M. Blessing, P. Buzas, B. A. Szmajda, and J. D. Forte, “Transmission of colour and acuity signals by parvocellular cells in marmoset monkeys,” J. Physiol. 589, 2795–2812 (2011).
[CrossRef]

P. Buzas, E. M. Blessing, B. A. Szmadja, and P. R. Martin, “Specificity of M and L cone inputs to receptive fields in the parvocellular pathway: random wiring with functional bias,” J. Neurosci. 26, 11148–11161 (2006).
[CrossRef]

Calkins, D. J.

D. J. Calkins and P. Sterling, “Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina,” Nature 381, 613–615 (1996).
[CrossRef]

Chichilnisky, E. J.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

Creutzfeldt, O. D.

B. B. Lee, V. Virsu, and O. D. Creutzfeldt, “Linear signal transmission from prepotentials to cells in the macaque lateral geniculate nucleus,” Exp. Brain Res. 52, 50–56 (1983).
[CrossRef]

Croner, L. J.

L. J. Croner and E. Kaplan, “Receptive fields of P and M ganglion cells across the primate retina,” Vis. Res. 35, 7–24 (1995).
[CrossRef]

Crook, J. D.

J. D. Crook, M. B. Manookin, O. S. Packer, and D. M. Dacey, “Horizontal cell feedback without cone type-selective inhibition mediates “red-green” color opponency in midget ganglion cells of the primate retina,” J. Neurosci. 31, 1762–1772 (2011).
[CrossRef]

Curcio, C. A.

O. Packer, A. E. Hendrickson, and C. A. Curcio, “Photoreceptor topography of the retina in the adult pigtail macaque (macaca nemestrina),” J. Comp. Neurol. 288, 165–183 (1989).
[CrossRef]

Dabrowski, W.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

Dacey, D. M.

J. D. Crook, M. B. Manookin, O. S. Packer, and D. M. Dacey, “Horizontal cell feedback without cone type-selective inhibition mediates “red-green” color opponency in midget ganglion cells of the primate retina,” J. Neurosci. 31, 1762–1772 (2011).
[CrossRef]

H. R. Joo, B. B. Peterson, T. J. Haun, and D. M. Dacey, “Characterization of a novel large-field cone bipolar cell type in the primate retina: evidence for selective cone connections,” Vis. Neurosci. 28, 29–37 (2011).
[CrossRef]

Derrington, A. M.

A. M. Derrington and P. Lennie, “Spatial and temporal contrast sensitivities of neurons in lateral geniculate nucleus of macaque,” J. Physiol. 357, 219–240 (1984).

DeValois, K. K.

R. L. DeValois and K. K. DeValois, Spatial Vision., Oxford Psychology Series, D. E. Broadbent, ed. (Oxford University, 1988).

DeValois, R. L.

R. L. DeValois, “Analysis and coding of color vision in the primate visual system,” Cold Spring Harb. Symp. Quant. Biol. 30, 567–579 (1965).
[CrossRef]

R. L. DeValois and K. K. DeValois, Spatial Vision., Oxford Psychology Series, D. E. Broadbent, ed. (Oxford University, 1988).

Dobkins, K. R.

Dowling, J. E.

B. B. Boycott and J. E. Dowling, “Organization of the primate retina: light microscopy,” Phil. Trans. R. Soc. Lond. B 255, 109–184 (1969).
[CrossRef]

Elepfandt, A.

B. B. Lee, V. Virsu, and A. Elepfandt, “Phase of responses to moving gratings in cells of the cat retina and lateral geniculate nucleus,” J. Neurophysiol. 45, 807–817 (1981).

Enroth-Cugell, C.

C. Enroth-Cugell, J. G. Robson, D. E. Schweitzer-Tong, and A. B. Watson, “Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation,” J. Physiol. 341, 279–307 (1983).

C. Enroth-Cugell and J. G. Robson, “The contrast sensitivity of retinal ganglion cells of the cat,” J. Physiol. 187, 517–552 (1966).

Field, G. D.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

Forte, J. D.

P. R. Martin, E. M. Blessing, P. Buzas, B. A. Szmajda, and J. D. Forte, “Transmission of colour and acuity signals by parvocellular cells in marmoset monkeys,” J. Physiol. 589, 2795–2812 (2011).
[CrossRef]

Gauthier, J. L.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

Greschner, M.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

Grünert, U.

B. B. Lee, P. R. Martin, and U. Grünert, “Retinal connectivity and primate vision,” Prog. Retin. Res. 29, 622–639 (2010).
[CrossRef]

H. Wässle, U. Grünert, P. R. Martin, and B. B. Boycott, “Color coding in the primate retina: predictions and constrants from anatomy,” in Structural and Functional Organization of the Neocortex. A Symposium in the Memory of Otto D. Creutzfeldt, B. Albowitz, K. Albus, U. Kuhnt, H. Ch. Nothdurft, and P. Wahle, eds. (Springer, 1994), pp. 94–104.

Gunning, D. E.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

Haake, P. W.

P. Lennie, P. W. Haake, and D. R. Williams, “The design of chromatically opponent receptive fields,” in Computational Models of Visual Processing, M. S. Landy and J. A. Movshon, eds. (MIT, 1991), pp. 71–82.

Haun, T. J.

H. R. Joo, B. B. Peterson, T. J. Haun, and D. M. Dacey, “Characterization of a novel large-field cone bipolar cell type in the primate retina: evidence for selective cone connections,” Vis. Neurosci. 28, 29–37 (2011).
[CrossRef]

Hendrickson, A. E.

O. Packer, A. E. Hendrickson, and C. A. Curcio, “Photoreceptor topography of the retina in the adult pigtail macaque (macaca nemestrina),” J. Comp. Neurol. 288, 165–183 (1989).
[CrossRef]

Hicks, T. P.

T. P. Hicks, B. B. Lee, and T. R. Vidyasagar, “The responses of cells in macaque lateral geniculate nucleus to sinusoidal gratings,” J. Physiol. 337, 183–200 (1983).

Hubel, D. H.

T. Wiesel and D. H. Hubel, “Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey,” J. Neurophysiol. 29, 1115–1156 (1966).

Jepson, L. H.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

Joo, H. R.

H. R. Joo, B. B. Peterson, T. J. Haun, and D. M. Dacey, “Characterization of a novel large-field cone bipolar cell type in the primate retina: evidence for selective cone connections,” Vis. Neurosci. 28, 29–37 (2011).
[CrossRef]

Kaplan, E.

E. A. Benardete and E. Kaplan, “The receptive field of the primate P retinal ganglion cell I: linear dynamics,” Vis. Neurosci. 14, 169–186 (1997).
[CrossRef]

L. J. Croner and E. Kaplan, “Receptive fields of P and M ganglion cells across the primate retina,” Vis. Res. 35, 7–24 (1995).
[CrossRef]

E. Kaplan and R. Shapley, “The origin of the S (slow) potential in the mammalian lateral geniculate nucleus,” Exp. Brain Res. 55, 111–116 (1984).
[CrossRef]

Kingdom, F. A.

K. T. Mullen and F. A. Kingdom, “Losses in peripheral colour sensitivity predicted from “hit or miss” post-receptoral cone connections,” Vis. Res. 36, 1995–2000 (1996).
[CrossRef]

Kremers, J.

B. B. Lee, J. Kremers, and T. Yeh, “Receptive fields of primate ganglion cells studied with a novel technique,” Vis. Neurosci. 15, 161–175 (1998).
[CrossRef]

Kröger-Paulus, A.

W. Paulus and A. Kröger-Paulus, “A new concept of retinal colour coding,” Vis. Res. 23, 529–540 (1983).
[CrossRef]

Lee, B. B.

B. B. Lee, P. R. Martin, and U. Grünert, “Retinal connectivity and primate vision,” Prog. Retin. Res. 29, 622–639 (2010).
[CrossRef]

B. B. Lee, “Neural models and physiological reality,” Vis. Neurosci. 25, 231–241 (2008).
[CrossRef]

S. G. Solomon, B. B. Lee, A. J. White, L. Ruttiger, and P. R. Martin, “Chromatic organization of ganglion cell receptive fields in the peripheral retina,” J. Neurosci. 25, 4527–4539 (2005).
[CrossRef]

P. R. Martin, B. B. Lee, A. J. White, S. G. Solomon, and L. Rüttiger, “Chromatic sensitivity of ganglion cells in peripheral primate retina,” Nature 410, 933–936 (2001).
[CrossRef]

B. B. Lee, J. Kremers, and T. Yeh, “Receptive fields of primate ganglion cells studied with a novel technique,” Vis. Neurosci. 15, 161–175 (1998).
[CrossRef]

B. B. Lee, P. R. Martin, and A. Valberg, “Sensitivity of macaque retinal ganglion cells to chromatic and luminance flicker,” J. Physiol. 414, 223–243 (1989).

B. B. Lee, V. Virsu, and O. D. Creutzfeldt, “Linear signal transmission from prepotentials to cells in the macaque lateral geniculate nucleus,” Exp. Brain Res. 52, 50–56 (1983).
[CrossRef]

T. P. Hicks, B. B. Lee, and T. R. Vidyasagar, “The responses of cells in macaque lateral geniculate nucleus to sinusoidal gratings,” J. Physiol. 337, 183–200 (1983).

B. B. Lee, V. Virsu, and A. Elepfandt, “Phase of responses to moving gratings in cells of the cat retina and lateral geniculate nucleus,” J. Neurophysiol. 45, 807–817 (1981).

Lennie, P.

A. M. Derrington and P. Lennie, “Spatial and temporal contrast sensitivities of neurons in lateral geniculate nucleus of macaque,” J. Physiol. 357, 219–240 (1984).

P. Lennie, P. W. Haake, and D. R. Williams, “The design of chromatically opponent receptive fields,” in Computational Models of Visual Processing, M. S. Landy and J. A. Movshon, eds. (MIT, 1991), pp. 71–82.

Litke, A. M.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

Machado, T. A.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

Manookin, M. B.

J. D. Crook, M. B. Manookin, O. S. Packer, and D. M. Dacey, “Horizontal cell feedback without cone type-selective inhibition mediates “red-green” color opponency in midget ganglion cells of the primate retina,” J. Neurosci. 31, 1762–1772 (2011).
[CrossRef]

Martin, P. R.

P. R. Martin, E. M. Blessing, P. Buzas, B. A. Szmajda, and J. D. Forte, “Transmission of colour and acuity signals by parvocellular cells in marmoset monkeys,” J. Physiol. 589, 2795–2812 (2011).
[CrossRef]

B. B. Lee, P. R. Martin, and U. Grünert, “Retinal connectivity and primate vision,” Prog. Retin. Res. 29, 622–639 (2010).
[CrossRef]

P. Buzas, E. M. Blessing, B. A. Szmadja, and P. R. Martin, “Specificity of M and L cone inputs to receptive fields in the parvocellular pathway: random wiring with functional bias,” J. Neurosci. 26, 11148–11161 (2006).
[CrossRef]

S. G. Solomon, B. B. Lee, A. J. White, L. Ruttiger, and P. R. Martin, “Chromatic organization of ganglion cell receptive fields in the peripheral retina,” J. Neurosci. 25, 4527–4539 (2005).
[CrossRef]

P. R. Martin, B. B. Lee, A. J. White, S. G. Solomon, and L. Rüttiger, “Chromatic sensitivity of ganglion cells in peripheral primate retina,” Nature 410, 933–936 (2001).
[CrossRef]

B. B. Lee, P. R. Martin, and A. Valberg, “Sensitivity of macaque retinal ganglion cells to chromatic and luminance flicker,” J. Physiol. 414, 223–243 (1989).

H. Wässle, U. Grünert, P. R. Martin, and B. B. Boycott, “Color coding in the primate retina: predictions and constrants from anatomy,” in Structural and Functional Organization of the Neocortex. A Symposium in the Memory of Otto D. Creutzfeldt, B. Albowitz, K. Albus, U. Kuhnt, H. Ch. Nothdurft, and P. Wahle, eds. (Springer, 1994), pp. 94–104.

Mathieson, K.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

Merrill, E. G.

E. G. Merrill and A. Ainsworth, “Glass-coated platinum-plated tungsten microelectrodes,” Med. Biol. Eng. 10, 662–672 (1972).
[CrossRef]

Mullen, K. T.

K. T. Mullen and F. A. Kingdom, “Losses in peripheral colour sensitivity predicted from “hit or miss” post-receptoral cone connections,” Vis. Res. 36, 1995–2000 (1996).
[CrossRef]

Packer, O.

O. Packer, A. E. Hendrickson, and C. A. Curcio, “Photoreceptor topography of the retina in the adult pigtail macaque (macaca nemestrina),” J. Comp. Neurol. 288, 165–183 (1989).
[CrossRef]

Packer, O. S.

J. D. Crook, M. B. Manookin, O. S. Packer, and D. M. Dacey, “Horizontal cell feedback without cone type-selective inhibition mediates “red-green” color opponency in midget ganglion cells of the primate retina,” J. Neurosci. 31, 1762–1772 (2011).
[CrossRef]

Paninski, L.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

Paulus, W.

W. Paulus and A. Kröger-Paulus, “A new concept of retinal colour coding,” Vis. Res. 23, 529–540 (1983).
[CrossRef]

Peterson, B. B.

H. R. Joo, B. B. Peterson, T. J. Haun, and D. M. Dacey, “Characterization of a novel large-field cone bipolar cell type in the primate retina: evidence for selective cone connections,” Vis. Neurosci. 28, 29–37 (2011).
[CrossRef]

Pokorny, J.

A. G. Shapiro, J. Pokorny, and V. C. Smith, “Cone-rod receptor spaces with illustrations that use CRT phosphor and light-emitting-diode spectra,” J. Opt. Soc. Am. A 13, 2319–2328 (1996).
[CrossRef]

V. C. Smith and J. Pokorny, “Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm,” Vis. Res. 15, 161–171 (1975).
[CrossRef]

Polyak, S. L.

S. L. Polyak, The Retina (University of Chicago, 1941).

Reid, R. C.

R. C. Reid and R. M. Shapley, “Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus,” J. Neurosci. 22, 6158–6175 (2002).

R. C. Reid and R. M. Shapley, “Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus,” Nature 356, 716–718 (1992).
[CrossRef]

Robson, J. G.

C. Enroth-Cugell, J. G. Robson, D. E. Schweitzer-Tong, and A. B. Watson, “Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation,” J. Physiol. 341, 279–307 (1983).

C. Enroth-Cugell and J. G. Robson, “The contrast sensitivity of retinal ganglion cells of the cat,” J. Physiol. 187, 517–552 (1966).

Ruttiger, L.

S. G. Solomon, B. B. Lee, A. J. White, L. Ruttiger, and P. R. Martin, “Chromatic organization of ganglion cell receptive fields in the peripheral retina,” J. Neurosci. 25, 4527–4539 (2005).
[CrossRef]

Rüttiger, L.

P. R. Martin, B. B. Lee, A. J. White, S. G. Solomon, and L. Rüttiger, “Chromatic sensitivity of ganglion cells in peripheral primate retina,” Nature 410, 933–936 (2001).
[CrossRef]

Schweitzer-Tong, D. E.

C. Enroth-Cugell, J. G. Robson, D. E. Schweitzer-Tong, and A. B. Watson, “Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation,” J. Physiol. 341, 279–307 (1983).

Shapiro, A. G.

Shapley, R.

E. Kaplan and R. Shapley, “The origin of the S (slow) potential in the mammalian lateral geniculate nucleus,” Exp. Brain Res. 55, 111–116 (1984).
[CrossRef]

Shapley, R. M.

R. C. Reid and R. M. Shapley, “Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus,” J. Neurosci. 22, 6158–6175 (2002).

R. C. Reid and R. M. Shapley, “Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus,” Nature 356, 716–718 (1992).
[CrossRef]

Sher, A.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

Shlens, J.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

Smith, V. C.

A. G. Shapiro, J. Pokorny, and V. C. Smith, “Cone-rod receptor spaces with illustrations that use CRT phosphor and light-emitting-diode spectra,” J. Opt. Soc. Am. A 13, 2319–2328 (1996).
[CrossRef]

V. C. Smith and J. Pokorny, “Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm,” Vis. Res. 15, 161–171 (1975).
[CrossRef]

Solomon, S. G.

S. G. Solomon, B. B. Lee, A. J. White, L. Ruttiger, and P. R. Martin, “Chromatic organization of ganglion cell receptive fields in the peripheral retina,” J. Neurosci. 25, 4527–4539 (2005).
[CrossRef]

P. R. Martin, B. B. Lee, A. J. White, S. G. Solomon, and L. Rüttiger, “Chromatic sensitivity of ganglion cells in peripheral primate retina,” Nature 410, 933–936 (2001).
[CrossRef]

Sterling, P.

D. J. Calkins and P. Sterling, “Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina,” Nature 381, 613–615 (1996).
[CrossRef]

Szmadja, B. A.

P. Buzas, E. M. Blessing, B. A. Szmadja, and P. R. Martin, “Specificity of M and L cone inputs to receptive fields in the parvocellular pathway: random wiring with functional bias,” J. Neurosci. 26, 11148–11161 (2006).
[CrossRef]

Szmajda, B. A.

P. R. Martin, E. M. Blessing, P. Buzas, B. A. Szmajda, and J. D. Forte, “Transmission of colour and acuity signals by parvocellular cells in marmoset monkeys,” J. Physiol. 589, 2795–2812 (2011).
[CrossRef]

Thiele, A.

Valberg, A.

B. B. Lee, P. R. Martin, and A. Valberg, “Sensitivity of macaque retinal ganglion cells to chromatic and luminance flicker,” J. Physiol. 414, 223–243 (1989).

Vidyasagar, T. R.

T. P. Hicks, B. B. Lee, and T. R. Vidyasagar, “The responses of cells in macaque lateral geniculate nucleus to sinusoidal gratings,” J. Physiol. 337, 183–200 (1983).

Virsu, V.

B. B. Lee, V. Virsu, and O. D. Creutzfeldt, “Linear signal transmission from prepotentials to cells in the macaque lateral geniculate nucleus,” Exp. Brain Res. 52, 50–56 (1983).
[CrossRef]

B. B. Lee, V. Virsu, and A. Elepfandt, “Phase of responses to moving gratings in cells of the cat retina and lateral geniculate nucleus,” J. Neurophysiol. 45, 807–817 (1981).

Wässle, H.

H. Wässle, U. Grünert, P. R. Martin, and B. B. Boycott, “Color coding in the primate retina: predictions and constrants from anatomy,” in Structural and Functional Organization of the Neocortex. A Symposium in the Memory of Otto D. Creutzfeldt, B. Albowitz, K. Albus, U. Kuhnt, H. Ch. Nothdurft, and P. Wahle, eds. (Springer, 1994), pp. 94–104.

Watson, A. B.

C. Enroth-Cugell, J. G. Robson, D. E. Schweitzer-Tong, and A. B. Watson, “Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation,” J. Physiol. 341, 279–307 (1983).

White, A. J.

S. G. Solomon, B. B. Lee, A. J. White, L. Ruttiger, and P. R. Martin, “Chromatic organization of ganglion cell receptive fields in the peripheral retina,” J. Neurosci. 25, 4527–4539 (2005).
[CrossRef]

P. R. Martin, B. B. Lee, A. J. White, S. G. Solomon, and L. Rüttiger, “Chromatic sensitivity of ganglion cells in peripheral primate retina,” Nature 410, 933–936 (2001).
[CrossRef]

Wiesel, T.

T. Wiesel and D. H. Hubel, “Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey,” J. Neurophysiol. 29, 1115–1156 (1966).

Williams, D. R.

P. Lennie, P. W. Haake, and D. R. Williams, “The design of chromatically opponent receptive fields,” in Computational Models of Visual Processing, M. S. Landy and J. A. Movshon, eds. (MIT, 1991), pp. 71–82.

Yeh, T.

B. B. Lee, J. Kremers, and T. Yeh, “Receptive fields of primate ganglion cells studied with a novel technique,” Vis. Neurosci. 15, 161–175 (1998).
[CrossRef]

J. Comp. Neurol.

O. Packer, A. E. Hendrickson, and C. A. Curcio, “Photoreceptor topography of the retina in the adult pigtail macaque (macaca nemestrina),” J. Comp. Neurol. 288, 165–183 (1989).
[CrossRef]

Cold Spring Harb. Symp. Quant. Biol.

R. L. DeValois, “Analysis and coding of color vision in the primate visual system,” Cold Spring Harb. Symp. Quant. Biol. 30, 567–579 (1965).
[CrossRef]

Exp. Brain Res.

E. Kaplan and R. Shapley, “The origin of the S (slow) potential in the mammalian lateral geniculate nucleus,” Exp. Brain Res. 55, 111–116 (1984).
[CrossRef]

B. B. Lee, V. Virsu, and O. D. Creutzfeldt, “Linear signal transmission from prepotentials to cells in the macaque lateral geniculate nucleus,” Exp. Brain Res. 52, 50–56 (1983).
[CrossRef]

J. Neurophysiol.

T. Wiesel and D. H. Hubel, “Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey,” J. Neurophysiol. 29, 1115–1156 (1966).

B. B. Lee, V. Virsu, and A. Elepfandt, “Phase of responses to moving gratings in cells of the cat retina and lateral geniculate nucleus,” J. Neurophysiol. 45, 807–817 (1981).

J. Neurosci.

S. G. Solomon, B. B. Lee, A. J. White, L. Ruttiger, and P. R. Martin, “Chromatic organization of ganglion cell receptive fields in the peripheral retina,” J. Neurosci. 25, 4527–4539 (2005).
[CrossRef]

P. Buzas, E. M. Blessing, B. A. Szmadja, and P. R. Martin, “Specificity of M and L cone inputs to receptive fields in the parvocellular pathway: random wiring with functional bias,” J. Neurosci. 26, 11148–11161 (2006).
[CrossRef]

J. D. Crook, M. B. Manookin, O. S. Packer, and D. M. Dacey, “Horizontal cell feedback without cone type-selective inhibition mediates “red-green” color opponency in midget ganglion cells of the primate retina,” J. Neurosci. 31, 1762–1772 (2011).
[CrossRef]

R. C. Reid and R. M. Shapley, “Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus,” J. Neurosci. 22, 6158–6175 (2002).

J. Opt. Soc. Am. A

J. Physiol.

C. Enroth-Cugell and J. G. Robson, “The contrast sensitivity of retinal ganglion cells of the cat,” J. Physiol. 187, 517–552 (1966).

A. M. Derrington and P. Lennie, “Spatial and temporal contrast sensitivities of neurons in lateral geniculate nucleus of macaque,” J. Physiol. 357, 219–240 (1984).

B. B. Lee, P. R. Martin, and A. Valberg, “Sensitivity of macaque retinal ganglion cells to chromatic and luminance flicker,” J. Physiol. 414, 223–243 (1989).

C. Enroth-Cugell, J. G. Robson, D. E. Schweitzer-Tong, and A. B. Watson, “Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation,” J. Physiol. 341, 279–307 (1983).

T. P. Hicks, B. B. Lee, and T. R. Vidyasagar, “The responses of cells in macaque lateral geniculate nucleus to sinusoidal gratings,” J. Physiol. 337, 183–200 (1983).

P. R. Martin, E. M. Blessing, P. Buzas, B. A. Szmajda, and J. D. Forte, “Transmission of colour and acuity signals by parvocellular cells in marmoset monkeys,” J. Physiol. 589, 2795–2812 (2011).
[CrossRef]

Med. Biol. Eng.

E. G. Merrill and A. Ainsworth, “Glass-coated platinum-plated tungsten microelectrodes,” Med. Biol. Eng. 10, 662–672 (1972).
[CrossRef]

Nature

D. J. Calkins and P. Sterling, “Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina,” Nature 381, 613–615 (1996).
[CrossRef]

R. C. Reid and R. M. Shapley, “Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus,” Nature 356, 716–718 (1992).
[CrossRef]

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

P. R. Martin, B. B. Lee, A. J. White, S. G. Solomon, and L. Rüttiger, “Chromatic sensitivity of ganglion cells in peripheral primate retina,” Nature 410, 933–936 (2001).
[CrossRef]

Phil. Trans. R. Soc. Lond. B

B. B. Boycott and J. E. Dowling, “Organization of the primate retina: light microscopy,” Phil. Trans. R. Soc. Lond. B 255, 109–184 (1969).
[CrossRef]

Prog. Retin. Res.

B. B. Lee, P. R. Martin, and U. Grünert, “Retinal connectivity and primate vision,” Prog. Retin. Res. 29, 622–639 (2010).
[CrossRef]

Vis. Neurosci.

B. B. Lee, J. Kremers, and T. Yeh, “Receptive fields of primate ganglion cells studied with a novel technique,” Vis. Neurosci. 15, 161–175 (1998).
[CrossRef]

E. A. Benardete and E. Kaplan, “The receptive field of the primate P retinal ganglion cell I: linear dynamics,” Vis. Neurosci. 14, 169–186 (1997).
[CrossRef]

H. R. Joo, B. B. Peterson, T. J. Haun, and D. M. Dacey, “Characterization of a novel large-field cone bipolar cell type in the primate retina: evidence for selective cone connections,” Vis. Neurosci. 28, 29–37 (2011).
[CrossRef]

B. B. Lee, “Neural models and physiological reality,” Vis. Neurosci. 25, 231–241 (2008).
[CrossRef]

Vis. Res.

L. J. Croner and E. Kaplan, “Receptive fields of P and M ganglion cells across the primate retina,” Vis. Res. 35, 7–24 (1995).
[CrossRef]

V. C. Smith and J. Pokorny, “Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm,” Vis. Res. 15, 161–171 (1975).
[CrossRef]

W. Paulus and A. Kröger-Paulus, “A new concept of retinal colour coding,” Vis. Res. 23, 529–540 (1983).
[CrossRef]

K. T. Mullen and F. A. Kingdom, “Losses in peripheral colour sensitivity predicted from “hit or miss” post-receptoral cone connections,” Vis. Res. 36, 1995–2000 (1996).
[CrossRef]

Other

P. Lennie, P. W. Haake, and D. R. Williams, “The design of chromatically opponent receptive fields,” in Computational Models of Visual Processing, M. S. Landy and J. A. Movshon, eds. (MIT, 1991), pp. 71–82.

S. L. Polyak, The Retina (University of Chicago, 1941).

R. L. DeValois and K. K. DeValois, Spatial Vision., Oxford Psychology Series, D. E. Broadbent, ed. (Oxford University, 1988).

H. Wässle, U. Grünert, P. R. Martin, and B. B. Boycott, “Color coding in the primate retina: predictions and constrants from anatomy,” in Structural and Functional Organization of the Neocortex. A Symposium in the Memory of Otto D. Creutzfeldt, B. Albowitz, K. Albus, U. Kuhnt, H. Ch. Nothdurft, and P. Wahle, eds. (Springer, 1994), pp. 94–104.

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Figures (6)

Fig. 1.
Fig. 1.

A, Sketches of receptive field structure. The receptive field center mechanism is thought to derive from a single cone, but the surround may derive from a single cone type or from a mixture of both cone types. The spatial profile is usually considered as a DOG. B, Hypothetical spatial frequency curves for a DOG profile for luminance modulation. The BPI is defined as R0/Rmax. C, With a cone-selective surround, the spatial frequency tuning curve for a cone-isolating grating targeting the center cone class alone is expected to be low-pass in shape. D, With a mixed surround, a bandpass tuning curve is expected for a cone-isolating grating targeting the center cone class, but with a lesser degree of low spatial frequency roll-off compared to a luminance grating.

Fig. 2.
Fig. 2.

Spatial frequency tuning curves for luminance gratings and gratings isolating the receptive field center cone class for A, two midget ganglion cells and B, two LGN parvocellular cells. Responses for the retinal ganglion cells have been scaled relative to 30% cone contrast. Responses of the parvocellular cells were for ~20% contrast. The degree of bandpass shape for luminance varies from cell to cell, but for the gratings isolating the center cone class the curves have a low-pass shape.

Fig. 3.
Fig. 3.

A, Distributions of BPIlum for luminance gratings and for the gratings isolating the receptive field center cone class (BPIcc) for populations of midget ganglion cells and of parvocellular LGN cells show considerable similarity. For luminance there is much variability of BPIlum, with some cells showing little low-spatial-frequency roll-off (BPIlum=1). B, Comparisons of BPIlum and BPIcc for the two cell samples on a cell-by-cell basis. The solid curves represent the relationship between the BPI for luminance and the center cone expected if the ML ratio were 11. See the text for the derivation.

Fig. 4.
Fig. 4.

Tuning curves for the two ganglion cells of Fig. 2 for luminance and chromatic modulation (upper panels) and the cone-isolating conditions (middle panels). As in Fig. 2, the data have been contrast normalized. The phase plots in the the lower panels refer to the phase difference between the responses to the M and L-cone-isolating gratings and show a 180 deg phase difference. The inset figures indicate the inverse cosine transform of the response amplitude data for the different conditions. For the cell in A, the single cone transforms show sharp peaks set on a broad pedestal. For the cell in B, the curves resemble more closely those expected of a pair of Gaussian distributions. Solid curves are the fits for a model described in the text.

Fig. 5.
Fig. 5.

Parvocellular LGN tuning curves for two example neurons. A, D, Responses to luminance and chromatic gratings; B, E, responses to L- and M-cone-isolating gratings. All data were obtained with 20% cone contrast. C, F, These phase plots refer to the phase difference between the M- and L-cone responses for spatial frequencies where there was a response above the spontaneous for both L- and M-cone-isolating stimuli. There is a 180 deg phase difference at the low spatial frequencies, indicating opponency. The insets in B and E indicate the inverse cosine transform of Gaussian mechanisms fit to the tuning curves for the different conditions. Solid curves through the spatial frequency tuning data are the best fits of a DOG model.

Fig. 6.
Fig. 6.

A, Examples of tuning curves from a neuron with a “notch” effect for one of the cone-isolating conditions (upper panel). The L-cone tuning curve is low-pass, but the M-cone shows a tuning curve with a minimum (arrow), followed by a further peak; such notches were associated with a phase change (>90deg). Curves indicate fits of a DOG model. However, tuning curves for luminance and chromatic gratings were poorly predicted. Further details are in the text. B, Eccentricity distribution of ganglion cells; those showing a notch feature were at eccentricities of 10 deg or above.

Equations (6)

Equations on this page are rendered with MathJax. Learn more.

L(f)=kL1πrL12e(πfrL1)2+kL2πrL22e(πfrL2)2,
M(f)=kM1πrM12e(πfrM1)2+kM2πrM22e(πfrM2)2,
Lum(f)=Clum(L(f)M(f)),
Chr(f)=CLchrL(f)+CMchrM(f),
LC(f)=CLL(f),
MC(f)=CMM(f),

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