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Neurons Show Their True Colours

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Neurons Show Their True Colours RESEARCH NEWS & VIEWS VISION Neurons show 50 Years Ago their true colours How do we tell red from green? Work on the primate retina shows how neural An Introduction to the Logic of the circuitry combines signals from individual cone photoreceptor cells to provide Sciences. By R. Harré — This is a very the basic building blocks for colour vision. See Article p.673 welcome book. It should be said at the outset that the author’s intention to write largely for undergraduates JONATHAN B. DEMB & DAVID H. BRAINARD genes encoding the S and M/L cone opsins — in science may prove a little on the proteins that determine spectral sensitivity modest side, since many students he processing of visual information — diverged more than 500 million years ago4. working for higher degrees would begins in the retina, where special- Moreover, the primate retina contains special- probably produce substantially ized neurons called photoreceptors ized ganglion cells for computing S–(L+M) better theses if they could find time Tabsorb light and stimulate multiple neural opponent signals. The small bistratified to read what Dr. Harré has to relate circuits. Each circuit generates specific ganglion cells, for example, receive excitatory … The grand point is that — from patterns of electrical activity and converges on inputs from S cones through S-cone bipo- the aspect of discovery — disciplined one of about 20 types of retinal ganglion cell. lar cells, and (L+M) cone signals oppose the insight came first, and the These cells’ axons — the optic nerve fibres — S-cone signals by means of two distinct retinal application of mathematical analysis then convey signals to various brain targets. pathways5. Similar cone opponency is medi- afterwards. Essential as the latter is, For colour vision, specific retinal circuits com- ated by ganglion cells in other mammals6,7. momentous advances usually begin pare the activity levels of different types of cone As for L–M opponency, this depends on a with remarkably simple premises. photoreceptor cells that have different spectral third opsin that arose in Old World primates Incidentally, Max Planck is known sensitivities1. On page 673 of this issue, Field less than 40 million years ago4. The neural to have fought long and hard in his et al.2 describe simultaneous recordings from mechanisms underlying L–M opponency have mind against the consequences hundreds of ganglion cells, and a new method remained elusive. It could be that a special- of his own quantum concept. The to map the inputs that these cells receive from ized ganglion-cell type analogous to the small statistical and indiscriminate nature individual cones. The results provide insight bistratified cells collects pure antagonistic of much of modern physics was not into the initial stages of colour vision. signals from L and M cones8. So far, however, to his liking. But that is the penalty Old World primates, including humans, there has been no definitive identification of of greatness. Questions like these are have three types of cone photoreceptors that such cells. ably handled by Dr. Harré, and the are maximally sensitive to long (L), middle (M) Alternatively, L–M opponency might arise moral is driven home. or short (S) wavelengths of light. In isolation, in other cells that existed before the emergence From Nature 8 October 1960 however, each cone is colour-blind because its of the third cone opsin. A favourite candidate activity depends on both the wavelength and is the midget ganglion cell, named for its small intensity of incident light1. For example, an size in the fovea — the central part of the ret- M cone’s activity would be the same for a dim ina1. In the fovea, each of these cells connects 100 Years Ago green light and a bright red light. Neural circuits through a midget bipolar cell to a single cone, derive a colour signal by comparing the activity and thus receives an excitatory ‘centre’ signal Beet Sugar Making and its Chemical of different cone types — cone opponency. In that is selective for L or M. The centre signal Control. By Y. Nikaido — In primate retinas, there are two broad classes of is opposed by a ‘surround’ signal that is driven principle, the production of sugar opponency: S −(L+M) opponency contrasts the by the surrounding cones. Consequently, from beetroots is a simple matter. activity of S cones with the combined activity even if the surround draws randomly on L The sugar and other soluble bodies of L and M cones, whereas L–M opponency and M cones, most foveal midgets will exhibit are extracted from the sliced roots contrasts the activity of L and M cones. a degree of L–M opponency because the centre by diffusion in water; the juice thus Primate cones are arranged in a mosaic, signal is always pure9 (Box 1). obtained is purified from acids presenting several challenges to implement- Each ganglion-cell type tiles the retina com- and other objectionable matter by ing cone opponency (Box 1). First, only a pletely, but is larger in the retinal periphery “defecation” with lime, and after the single cone exists at each location in the mosaic, than in the fovea1. The centre signals of the excess of lime has been removed by so comparing cone signals confounds spatial larger midget cells in the periphery therefore treatment with carbonic acid, the and spectral information. Second, S cones connect to a dozen or more cones, and analysis liquor is concentrated by evaporation are sparse, limiting the spatial resolution of of these connections should provide informa- until the sugar crystallises out. S − (L+M) opponency. Third, the M/L cone tion about the M/L selectivity of peripheral Whilst, however, there is nothing arrangement is random or nearly random, midget cells. The selective-wiring hypoth- complicated about the principle, leading to ‘clumps’ of either cell type2,3. This esis predicts selective connections between successful and profitable production limits the spatial resolution of L–M opponent each midget cell and either M or L cones; the depends upon close attention to a signals. For example, L–M resolution must be random-wiring hypothesis, by contrast, pre- number of points in respect of which coarser at the centre of a clump of L cones than dicts random connections1. Evidence has been the chemist’s help is needed. in a region where L and M cones alternate. reported in favour of both hypotheses10,11, mak- From Nature 6 October 1910 S − (L+M) opponency is an ancient and well- ing it difficult to rule either out definitively. To developed subsystem of colour vision. The date, one roadblock has been that inputs to 670 | NATURE | VOL 467 | 7 OCTOBER 2010 © 2010 Macmillan Publishers Limited. All rights reserved NEWS & VIEWS RESEARCH BOX 1 Cone opponency in the primate retina A schematic representation of the mosaic excitatory input from a dozen cones. There arrangement of cones in the monkey retina is a bias, measurable across the population that are sensitive to long (L, red), middle (M, of cells, in which the centre region of the green) and short (S, blue) wavelengths of light. d receptive field is wired to favour one cone S cones are rare, constituting 5–10% of the type, tending towards cone purity. In this mosaic, and L cones outnumber M cones by a case, for example, the midget cell avoids about 2 to 1. L and M cones are arranged near some M cones near those that comprise randomly. For simplicity, the cone mosaic is the centre (marked with a yellow asterisk) shown as rectangular in arrangement. The b in favour of the L cones that make up the actual mosaics are more hexagonal and also majority. This cell will have L–M opponency. 3 * c less regular : in the central all-cone fovea, * In this example, the S cones are skipped, but cones are tightly packed, whereas in the * a subgroup of midget cells is connected with retinal periphery they are separated by the S cones2. more numerous rod photoreceptors, which d, For S−(L+M) opponency, a small are used for seeing in dim light. bistratified ganglion cell receives an S-cone a, In the central fovea, a midget ganglion input that is opposed by M/L cone inputs. cell combines an excitatory centre-region b, A midget ganglion cell that aligns with Because of the irregular layout of S cones signal driven by a single cone — outlined in a clump of L cones, however, would lack and other features of the underlying neural white — with an opposing signal from the opponency, because the centre and surround circuitry, these cells lack the canonical surrounding region driven by surrounding are driven by the same class of cones. centre–surround structure found in many cones (outlined in black). This cell would c, In contrast to foveal midget ganglion other ganglion-cell types, including midget have M–L opponency. cells, a peripheral midget cell may receive cells1,5,8. J.B.D. & D.H.B. ganglion cells could not be characterized on a study highlights, two are particularly fasci- population of midget cells in a peripheral cone-by-cone basis. nating. First, how does the observed specifi- region of the retina, may help us to more sharply In a technical tour de force, Field et al.2 city of cone inputs come about? Expression analyse such psychophysical data to under- used a multi-electrode array to generate very by gene therapy of a third cone opsin in the stand the precise functional implications of high-resolution centre–surround receptive- retinas of adult New World monkeys that had the bias towards selective wiring.
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