Evidence that Circuits for Spatial and Color Vision Segregate at the First Retinal Synapse
Authors: David J Calkins, Peter Sterling
Journal: Neuron (1999)

Different psychophysical "channels" mediate our perception of fine spatial patterns and color. The spatial channel compares the photon catch between adjacent cones, regardless of type, and thus supports perception of patterns as fine as the cone mosaic (96Williams D.R Seeing through the photoreceptor mosaic.Trends Neurosci. 1986; 9: 193-198Abstract Full Text PDF Scopus (56) Google Scholar). Color channels compare the photon catch between different cone types (46Hurvich L.M Jameson D An opponent-process theory of color vision.Psychol. Rev. 1957; 64: 384-404Crossref PubMed Scopus (643) Google Scholar, 51Krauskopf J Williams D.R Heeley D.W Cardinal directions in color space.Vision Res. 1982; 22: 1123-1131Crossref PubMed Scopus (594) Google Scholar). The "blue/yellow" channel compares the catch in cones sensitive to short (S) wavelengths with the catch in neighboring cones sensitive to middle (M) and long (L) wavelengths (71Pugh Jr., E.N Mollon J.D A theory of the P1 and P3 color mechanisms of stiles.Vision Res. 1979; 19: 293-312Crossref PubMed Scopus (173) Google Scholar). The "red/green" channel compares the photon catch in L and S cones with that in neighboring M cones (87Thornton J.E Pugh Jr., E.N Red/green color opponency at detection threshold.Science. 1983; 219: 191-193Crossref PubMed Scopus (90) Google Scholar, 8Calkins D.J Thornton J.E Pugh E.N Monochromatism determined at a long-wavelength/middle-wavelength coneantagonistic locus.Vision Res. 1992; 32: 2349-2367Crossref PubMed Scopus (38) Google Scholar). Each comparison is equivalent to a subtraction: for blue/yellow, S−(M+L); for red/green, L−M+(S). The color channels are rather coarse, with an acuity about one-third that of the spatial channel (1Anderson S.J Mullen K.T Hess R.F Human peripheral spatial resolution for achromatic and chromatic stimuli limits imposed by optical and retinal factors.J. Physiol. 1991; 442: 47-64PubMed Google Scholar, 78Sekiguchi N Williams D.R Brainard D.H Efficiency in detection of isoluminant and isochromatic interference fringes.J. Opt. Soc. Am. A. 1993; 10: 2118-2133Crossref Scopus (96) Google Scholar). What neural circuits serve the psychophysical channels for spatial acuity and color? The standard view is that messages for both channels are conveyed by one type of ganglion cell, termed "P," because it projects to a parvocellular neuron in the lateral geniculate nucleus. The parvocellular neuron would relay both messages to primary visual cortex where, finally, spatial and color information would begin to segregate (47Ingling Jr., C.R Martinez-Uriegas E The relationship between spectral sensitivity and spatial sensitivity for the primate r-g X-channel.Vision Res. 1983; 23: 1495-1500Crossref PubMed Scopus (100) Google Scholar, 54Lennie P D'Zmura M Mechanisms of color vision.Crit. Rev. Neurobiol. 1988; 3: 333-400PubMed Google Scholar, 45Hubel D Livingstone M Color puzzles.Cold Spring Harbor Symp. Quant. Biol. 1990; 55: 643-649Crossref PubMed Scopus (20) Google Scholar, 31De Valois R.L De Valois K.K A multi-stage color model.Vision Res. 1993; 23: 1053-1065Crossref Scopus (386) Google Scholar). This circuit design, by compressing two messages on one axon, would minimize the number of axons in the optic nerve and geniculo-striate radiation. But it would also compromise the filtering of one or both messages and would reduce their shares of bandwidth (2Atick J.J Could information theory provide an ecological theory of sensory processing?.Network. 1992; 3: 213-251Crossref Scopus (346) Google Scholar). Although this "double duty" hypothesis for the P cell still predominates (e.g.4Boycott B.B Wässle H Parallel processing in the mammalian retina. The Proctor Lecture.Invest. Ophthalmol. Vis. Sci. 1999; 40: 1313-1327PubMed Google Scholar), its anatomical and physiological basis has recently eroded. Meanwhile, new evidence has accumulated for an alternative view, that the densely distributed P cell serves only the fine spatial channel and that sparsely distributed ganglion cells serve the color channels (73Rodieck R.W Which cells code for color?.in: Valberg A Lee B From Pigments to Perception. Plenum Press, New York1991Google Scholar). This circuit design would optimize filtering and bandwidth at the cost of additional axons. Here, we summarize current evidence for both views, starting with the origin of the P cell hypothesis. Recording from single neurons in the parvocellular geniculate layers95Wiesel T.N Hubel D.H Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey.J. Neurophysiol. 1966; 29: 1115-1156PubMed Google Scholar mapped responses such as those illustrated in Figure 1A and Figure 1B. This cell increased firing to long wavelengths restricted to a small center and was unaffected when the long wavelengths extended into the surround. However, it decreased firing when middle wavelengths covered both center and surround. Complementary types were also found: centers tuned to middle wavelengths with surrounds tuned to long wavelengths, and centers tuned to short wavelengths with surrounds tuned to middle and long wavelengths. Similar response types were found for retinal ganglion cells (24de Monasterio F.M Properties of concentrically organized X and Y ganglion cells of macaque retina.J. Neurophysiol. 1978; 41 (a): 1394-1417PubMed Google Scholar, 25de Monasterio F.M Center and surround mechanisms of opponent-color x and y ganglion cells of retina of macaques.J. Neurophysiol. 1978; 41 (b): 1418-1434PubMed Google Scholar). To explain these measurements, Wiesel and Hubel proposed a simple circuit: for the center, selective convergence of one cone type onto an excitatory neuron (bipolar cell); for the surround, selective convergence of the opposing cone type(s) onto an inhibitory neuron (horizontal or amacrine cell; Figure 1C; also 72Reid R.C Shapley R.M Spatial structure of cone inputs to receptive fields in primate geniculate nucleus.Nature. 1992; 356: 716-718Crossref PubMed Scopus (190) Google Scholar). The P cell's extremely small center in the fovea was attributed to the private pathway from one cone to a "midget" bipolar cell and midget ganglion cell (Figure 1D; 70Polyak S.L The Retina. University of Chicago Press, Chicago1941Google Scholar, 3Boycott B.B Dowling J.E Organization of the primate retina light microscopy.Philos. Trans. R. Soc. Lond. B Biol. Sci. 1969; 255: 109-184Crossref Google Scholar, 69Perry V.H Oehler R Cowey A Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey.Vision Res. 1984; 12: 1101-1123Google Scholar, 49Kolb H Dekorver L Midget ganglion cells of the parafovea of the human retina a study by electron microscopy and serial section reconstructions.J. Comp. 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Were this assessment correct, then the P cell mosaic would seem well suited to carry both spatial and spectral-difference signals to V1 where they are supposed to segregate (45Hubel D Livingstone M Color puzzles.Cold Spring Harbor Symp. Quant. Biol. 1990; 55: 643-649Crossref PubMed Scopus (20) Google Scholar). This idea seemed to be supported by behavioral experiments in which monkeys were trained to perform spatial and color discriminations. When specific lesions were placed in the lateral geniculate nucleus, damage to the parvocellular layers impaired both spatial acuity and color vision (59Merigan W.H Chromatic and achromatic vision of Macaques role of the P pathway.J. Neurosci. 1989; 9: 776-783PubMed Google Scholar, 77Schiller P.H Logothetis N.K Charles E.R Functions of the colour-opponent and broad-band channels of the visual system.Nature. 1990; 343: 68-70Crossref PubMed Scopus (299) Google Scholar). Thus, the hypothesis that the P/midget ganglion cell relays both spatial signals and also spectral-difference signals to the cortex seemed proven. Yet evidence has accumulated that the P cell is not selectively wired for spectral opponency. The Wiesel-Hubel model assumed a regular alternation of M and L cones (Figure 1C), but the mosaic actually turns out to be "patchy" with M and L cones forming clusters of like type (60Mollon J.D Bowmaker J.K The spatial arrangement of cones in the primate fovea.Nature. 1992; 360: 677-679Crossref PubMed Scopus (123) Google Scholar, 9Calkins D.J Schein S Tsukamoto Y Sterling P M and L cones in Macaque fovea connect to midget ganglion cells via different numbers of excitatory synapses.Nature. 1994; 371: 70-72Crossref PubMed Scopus (159) Google Scholar, 67Packer O.S Williams D.R Bensinger D.G Photopigment transmittance imaging of the primate photoreceptor mosaic.J. Neurosci. 1996; 16: 2251-2260PubMed Google Scholar, 75Roorda A Williams D.R The arrangement of the three cone classes in the living human eye.Nature. 1999; 397: 520-522Crossref PubMed Scopus (756) Google Scholar). A map of the foveal cone mosaic in a human shows L cones are mostly surrounded by other L cones, and only rarely is an L cone mostly surrounded by M cones (Figure 2). M cones, though sparser in this mosaic, are also more likely to be neighbored by other M cones than to be completely surrounded by L cones. Such clustering has a function: to conserve the spectral tuning of cone signals that would otherwise be reduced by electrical coupling between different types (44Hsu A Smith R Buchsbaum G Sterling P Cost of cone coupling to trichromacy in primate fovea.J. Opt. Soc. Am. 2000; in pressGoogle Scholar). However, clustering implies that if P cell surrounds were wired for spectral opponency, most surrounds would have significant "holes" where cones of the center type are skipped. This would be especially true in Figure 2 for L center P cells: to form the surround, inhibitory interneurons would need to skip large patches of L cones. It is clear that horizontal cells, representing the first stage of lateral inhibition, do not skip M or L cones but rather connect to all of them (Figure 3A; 5Boycott B.B Hopkins J.M Sperling H.G Cone connections of the horizontal cells of the rhesus monkey's retina.Proc. R. Soc. Lond. B Biol. Sci. 1987; 229: 345-379Crossref PubMed Scopus (128) Google Scholar, 21Dacey D.M Lee B.B Stafford D.K Pokorny J Smith V.C Horizontal cells of the primate retina cone specificity without spectral opponency.Science. 1996; 271: 656-659Crossref PubMed Scopus (200) Google Scholar, 35Goodchild A.K Chan T.L Grunert U Horizontal cell connections with short-wavelength-sensitive cones in macaque monkey retina.Vis. Neurosci. 1996; 13 (a): 833-845Crossref PubMed Scopus (64) Google Scholar). 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Subsequent recordings confirmed this in detail, showing that a horizontal cell's response accurately reflects the local composition of the M and L cone mosaic (22Dacey D.M Diller L.C Verweij J Williams D.R Physiology of L and M cone inputs to H1 horizontal cells in primate retina.J. Opt. Soc. Am. A. 2000; in pressGoogle Scholar). Thus, the P cell's first stage of lateral inhibition is spectrally unselective. Conceivably, amacrine cells could provide the P cell with a spectrally selective surround. However, the actual connections reconstructed from electron micrographs indicate that this is unlikely. An amacrine cell process contacted by a midget bipolar cell usually returns a contact to the same bipolar cell and also contacts the midget ganglion cell (Figure 3A and Figure 4). Therefore, local amacrine cell inhibition to the P cell is spectrally identical to local excitation. Amacrine cell processes traced laterally from their contacts at a midget bipolar-to-ganglion cell junction collect from all bipolar cell terminals within their reach (7Calkins D Sterling P Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina.Nature. 1996; 381: 613-615Crossref PubMed Scopus (84) Google Scholar). Thus, the P cell's second stage of lateral inhibition is also spectrally unselective. In central retina, out to about 7° eccentricity, the P ganglion cell's receptive field center is spectrally selective because its excitatory input derives from a single cone (Figure 1D). But beyond this, the P cell's dendritic arbor expands. Initially, it forms two dendritic clusters, coupling to two midget bipolar cell terminals, and finally it spans more than 100 μm, encompassing about 20 midget bipolar cell terminals (Figure 5; 17Dacey D.M The mosaic of midget ganglion cells in the human retina.J. Neurosci. 1993; 13 (a): 5334-5355PubMed Google Scholar). The P cell's dendritic field in the periphery contains "holes" that were thought to represent sites where bipolar cell terminals from one cone type might avoid contact (Figure 5B; 17Dacey D.M The mosaic of midget ganglion cells in the human retina.J. Neurosci. 1993; 13 (a): 5334-5355PubMed Google Scholar). But it is apparent that the holes separate dendritic clusters that reach out to adjacent midget bipolar cell terminals. The holes merely reflect the wider spacing of peripheral cones (Figure 5C; see also 36Goodchild A.K Ghosh K.K Martin P.R Comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat, and the marmoset Callithrix jacchus.J. Comp. Neurol. 1996; 366 (b): 55-75Crossref PubMed Scopus (141) Google Scholar). Where convergence onto the P cell remains small, the cone mosaic's patchiness might allow some P cell centers to be spectrally tuned. But as convergence rises to more than 40 cones (Figure 5E), the P cell's center should increasingly reflect the average composition of the cone mosaic, and recordings from peripheral midget ganglion cells support this (19Dacey D.M Circuitry for color coding in the primate retina.Proc. Natl. Acad. Sci. USA. 1996; 93: 582-588Crossref PubMed Scopus (161) Google Scholar). Thus, across large expanses of retina, the P cell's center is spectrally unselective. We conclude that the initial model (Figure 1C) is incorrect. The P/midget ganglion cell does not select one cone type for its center and a different cone type for its surround. Rather, it sums a spatially weighted average of all the cones encompassed by the dendritic field and subtracts a spatially weighted average of all the cones encompassed by a much broader surround region. In the receptive field center, cone signals tend to be strongly correlated because of correlations in the visual image, and summing these signals improves the cell's signal-to-noise ratio (88Tsukamoto Y Smith R.G Sterling P "Collective coding" of correlated cone signals in the retinal ganglion cell.Proc. Natl. Acad. Sci. USA. 1990; 87: 1860-1864Crossref PubMed Scopus (33) Google Scholar). In the surround, cone signals are partially correlated with the center, especially for low spatial frequencies, and subtracting these signals reduces the spatially redundant information (80Srinivasan M.V Laughlin S.B Dubs A Predictive coding a fresh view of inhibition in the retina.Proc. R. Soc. Lond. B Biol. Sci. 1982; 216: 427-459Crossref PubMed Scopus (690) Google Scholar). This dual filtering of high (center) and low (surround) frequencies optimizes a spatial signal to fill the P cell's coding capacity. This circuit design makes perfect sense for a ganglion cell that samples with the highest spatial density at all retinal locations and thus sets the limit to spatial acuity (86Thibos L.N Cheney F.E Walsh D.J Retinal limits to the detection and resolution of gratings.J. Opt. Soc. Am. A. 1987; 4: 1524-1529Crossref PubMed Scopus (198) Google Scholar, 17Dacey D.M The mosaic of midget ganglion cells in the human retina.J. Neurosci. 1993; 13 (a): 5334-5355PubMed Google Scholar). The foveal P cell, although optimized for spatial signals (Figure 3B), does exhibit some spectral opponency because the unselective surround antagonizes a single cone center (55Lennie P Haake P.W Williams D.R The design of chromatically opponent receptive fields.in: Landy M.S Movshon J.A Computational Models of Visual Processing. MIT Press, Cambridge, MA1991Google Scholar). 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Alternatively, the P cell's spectrally opponent information may simply be inseparable from its achromatic information and therefore unusable by the color opponent channels. Outside of the fovea, as the number of cones rises in the P cell center (Figure 5E), its spectral opponency declines (see Figure 5.10 in 55Lennie P Haake P.W Williams D.R The design of chromatically opponent receptive fields.in: Landy M.S Movshon J.A Computational Models of Visual Processing. 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A. 1993; 10: 2118-2133Crossref Scopus (96) Google Scholar), but at 25° eccentricity detection requires a much coarser grating, about 1 cycle/° (65Noorlander C Koenderink J.J Den Ouden R.J Edens B.W Sensitivity to spatiotemporal colour contrast in the peripheral visual field.Vision Res. 1983; 23: 1-11Crossref PubMed Scopus (104) Google Scholar, 41Hess R.F Mullen K.T Zrenner E Human photopic vision with only short wavelength cones post-receptoral properties.J. Physiol. 1989; 417: 151-172PubMed Google Scholar). Similarly, the red/green channel in the fovea detects an isoluminant grating down to 20–27 cycles/°, but at 30° eccentricity detection requires a much coarser grating, about 0.7 cycle/° (1Anderson S.J Mullen K.T Hess R.F Human peripheral spatial resolution for achromatic and chromatic stimuli limits imposed by optical and retinal factors.J. Physiol. 1991; 442: 47-64PubMed Google Scholar, 78Sekiguchi N Williams D.R Brainard D.H Efficiency in detection of isoluminant and isochromatic interference fringes.J. Opt. Soc. Am. A. 1993; 10: 2118-2133Crossref Scopus (96) Google Scholar). Spatial acuity in a given channel is generally set by the sampling density of its dedicated ganglion cell (Boycott and Wässle, 1991). For example, achromatic acuity is set all across the retina by the P cell's sampling density (86Thibos L.N Cheney F.E Walsh D.J Retinal limits to the detection and resolution of gratings.J. Opt. Soc. Am. A. 1987; 4: 1524-1529Crossref PubMed Scopus (198) Google Scholar, 17Dacey D.M The mosaic of midget ganglion cells in the human retina.J. Neurosci. 1993; 13 (a): 5334-5355PubMed Google Scholar). Therefore, one might expect spatial acuity for the color channels to be set by ganglion cell types with low sampling density. A circuit optimized to serve an opponent color channel should subtract the signals of one cone type from those of the other types (Figure 3C; 6Buchsbaum G Gottschalk A Trichromacy, opponent colours coding and optimum colour information transmission in the retina.Proc. R. Soc. Lond. B Biol. Sci. 1983; 220: 89-113Crossref PubMed Scopus (329) Google Scholar, 28Derrico J.B Buchsbaum G A computational model of spatiochromatic image coding in early vision.J. Vis. Commun. Image Represent. 1991; 2: 31-38Crossref Scopus (33) Google Scholar). Because the receptive field would be spectrally opponent but not spatially opponent, there would be no luminance signal to be discarded later. Critically, the pure spectral-difference signal could be maximally amplified to fill the ganglion cell's dynamic range. 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