Horizontal Cells of the Primate Retina: Cone Specificity Without Spectral Opponency

The chromatic dimensions of human color vision have a neural basis in the retina. Ganglion cells, the output neurons of the retina, exhibit spectral opponency; they are excited by some wavelengths and inhibited by others. The hypothesis that the opponent circuitry emerges from selective connections between horizontal cell interneurons and cone photoreceptors sensitive to long, middle, and short wavelengths (L-, M-, and S-cones) was tested by physiologically and anatomically characterizing cone connections of horizontal cell mosaics in macaque monkeys. H1 horizontal cells received input only from L- and M-cones, whereas H2 horizontal cells received a strong input from S-cones and a weaker input from L- and M-cones. All cone inputs were the same sign, and both horizontal cell types lacked opponency. Despite cone type selectivity, the horizontal cell cannot be the locus of an opponent transformation in primates, including humans.

[1]  Henk Spekreijse,et al.  Spectral behavior of cone-driven horizontal cells in Teleost Retina , 1995, Progress in Retinal and Eye Research.

[2]  J. L. Schnapf,et al.  Photovoltage of rods and cones in the macaque retina. , 1995, Science.

[3]  R. G. Smith,et al.  Simulation of an anatomically defined local circuit: The cone-horizontal cell network in cat retina , 1995, Visual Neuroscience.

[4]  J. Pokorny,et al.  Mechanisms subserving temporal modulation sensitivity in silent-cone substitution. , 1995, Journal of the Optical Society of America. A, Optics, image science, and vision.

[5]  D. I. Vaney,et al.  Patterns of neuronal coupling in the retina , 1994, Progress in Retinal and Eye Research.

[6]  H. Kolb,et al.  Horizontal cells and cone photoreceptors in human retina: A Golgi‐electron microscopic study of spectral connectivity , 1994, The Journal of comparative neurology.

[7]  Barry B. Lee,et al.  The 'blue-on' opponent pathway in primate retina originates from a distinct bistratified ganglion cell type , 1994, Nature.

[8]  D. A. Burkhardt,et al.  Synaptic feedback, depolarization, and color opponency in cone photoreceptors , 1993, Visual Neuroscience.

[9]  B. B. Lee,et al.  Responses of macaque ganglion cells to movement of chromatic borders. , 1992, Journal of Physiology.

[10]  J. Pokorny,et al.  Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights. , 1992, The Journal of physiology.

[11]  R. Shapley,et al.  Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus , 1992, Nature.

[12]  A. Milam,et al.  Distribution and morphology of human cone photoreceptors stained with anti‐blue opsin , 1991, The Journal of comparative neurology.

[13]  S. Mangel,et al.  Analysis of the horizontal cell contribution to the receptive field surround of ganglion cells in the rabbit retina. , 1991, The Journal of physiology.

[14]  R. Dacheux,et al.  Physiology of H I horizontal cells in the primate retina , 1990, Proceedings of the Royal Society of London. B. Biological Sciences.

[15]  B. Boycott,et al.  Horizontal Cells in the Monkey Retina: Cone connections and dendritic network , 1989, The European journal of neuroscience.

[16]  V C Smith,et al.  Temporal modulation sensitivity and pulse-detection thresholds for chromatic and luminance perturbations. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[17]  J. M. Hopkins,et al.  Cone connections of the horizontal cells of the rhesus monkey’s retina , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[18]  D. Baylor,et al.  Spectral sensitivity of human cone photoreceptors , 1987, Nature.

[19]  A. Mariani,et al.  A second type of horizontal cell in the monkey retina , 1980, The Journal of comparative neurology.

[20]  J. Pokorny,et al.  Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm , 1975, Vision Research.

[21]  P. Gouras Identification of cone mechanisms in monkey ganglion cells , 1968, The Journal of physiology.

[22]  D. Hubel,et al.  Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. , 1966, Journal of neurophysiology.

[23]  R. L. de Valois,et al.  Responses of Single Cells in Visual System to Shifts in the Wavelength of Light , 1964, Science.

[24]  R. L. de Valois,et al.  Response of single cells in monkey lateral geniculate nucleus to monochromatic light. , 1958, Science.