Synergistic center-surround receptive field model of monkey H1 horizontal cells.

Horizontal cells typical of the vertebrate retina are strongly coupled by gap junctions. The resulting horizontal cell network has extremely large receptive fields that extend well beyond the boundaries of a single dendritic tree. This network has been modeled as a syncytium of cytoplasm bounded by cell membrane (Lamb 1976; Naka & Rushton, 1967). Horizontal cells in the primate retina are also coupled by gap junctions, but their receptive fields are relatively small and in some cases may approximate the span of the dendritic tree of an individual cell (Packer & Dacey, 2002). The receptive field of the macaque H1 horizontal cell type has been modeled as the sum of two spatial components: a strong but small diameter excitatory center, and a weak but broad excitatory surround. Here we explore the hypothesis that the receptive field center of H1 cells derives from direct cone synaptic input and that the synergistic surround derives from gap-junctional coupling among H1 cell neighbors. We measured the receptive field structure of H1 cells in the presence of carbenoxolone, a gap junction blocker, to determine the effects of uncoupling center and surround components and compared these data to a neural simulation of the H1 network in which gap-junctional conductance could be manipulated. Carbenoxolone reduced the surround component and eliminated irregularities in spatial structure thought to be associated with the surround. The effects of carbenoxolone could be mimicked by manipulating gap-junctional conductance in an H1 cell network simulation. These results provide strong support for the two-component model of H1 receptive field structure. In addition, carbenoxolone eliminated a slow depolarization following light onset thought to be mediated by cone-H1 feedback (Kamermans & Spekreijse, 1999). Low concentrations of cobalt, a calcium channel blocker that spares gap junctions, had an effect similar to that of carbenoxolone but did not affect receptive field structure. These results are consistent with a calcium-mediated mechanism of feedback from H1 cells to cones that is independent of the synergistic two-component model of receptive field organization.

[1]  Robert G. Smith,et al.  NeuronC: a computational language for investigating functional architecture of neural circuits , 1992, Journal of Neuroscience Methods.

[2]  J. Dowling.  The Ultrastructure of the Human Retina , 1967 .

[3]  K. Naka,et al.  The generation and spread of S‐potentials in fish (Cyprinidae) , 1967, The Journal of physiology.

[4]  J. Pokorny,et al.  Primate horizontal cell dynamics: an analysis of sensitivity regulation in the outer retina. , 2001, Journal of neurophysiology.

[5]  Barry B. Lee,et al.  Horizontal Cells of the Primate Retina: Cone Specificity Without Spectral Opponency , 1996, Science.

[6]  D. Dacey,et al.  Receptive field structure of H1 horizontal cells in macaque monkey retina. , 2002, Journal of vision.

[7]  B. B. Lee,et al.  Receptive fields of primate retinal ganglion cells studied with a novel technique , 1998, Visual Neuroscience.

[8]  D. Baylor,et al.  Receptive fields of cones in the retina of the turtle , 1971, The Journal of physiology.

[9]  K. Mullen,et al.  Losses in Peripheral Colour Sensitivity Predicted from “Hit and Miss” Post-receptoral Cone Connections , 1996, Vision Research.

[10]  David R. Williams,et al.  The design of chromatically opponent receptive fields , 1991 .

[11]  J. L. Schnapf,et al.  Surround Antagonism in Macaque Cone Photoreceptors , 2003, Journal of Neuroscience.

[12]  B. Boycott,et al.  The mosaic of horizontal cells in the macaque monkey retina: With a comment on biplexiform ganglion cells , 2000, Visual Neuroscience.

[13]  P. W. Nye,et al.  Role of horizontal cells in organization of the catfish retinal receptive field. , 1971, Journal of neurophysiology.

[14]  H Spekreijse,et al.  The feedback pathway from horizontal cells to cones A mini review with a look ahead , 1999, Vision Research.

[15]  K. Tornqvist,et al.  Modulation of cone horizontal cell activity in the teleost fish retina. III. Effects of prolonged darkness and dopamine on electrical coupling between horizontal cells , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  S. Barnes,et al.  Carbenoxolone inhibition of voltage-gated Ca channels and synaptic transmission in the retina. , 2004, Journal of neurophysiology.

[17]  P. Gouras,et al.  Functional properties of ganglion cells of the rhesus monkey retina. , 1975, The Journal of physiology.

[18]  D. Dacey,et al.  Colour coding in the primate retina: diverse cell types and cone-specific circuitry , 2003, Current Opinion in Neurobiology.

[19]  K. Mullen,et al.  Differential distributions of red–green and blue–yellow cone opponency across the visual field , 2002, Visual Neuroscience.

[20]  D. A. Burkhardt,et al.  Effects of synaptic blocking agents on the depolarizing responses of turtle cones evoked by surround illumination , 1990, Visual Neuroscience.

[21]  J. Verweij,et al.  L and M Cone Contributions to the Midget and Parasol Ganglion Cell Receptive Fields of Macaque Monkey Retina , 2004, The Journal of Neuroscience.

[22]  A. Goodchild,et al.  Horizontal cell connections with short-wavelength-sensitive cones in macaque monkey retina , 1996, Visual Neuroscience.

[23]  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.

[24]  S. Massey,et al.  Distribution and coverage of A- and B-type horizontal cells stained with Neurobiotin in the rabbit retina , 1994, Visual Neuroscience.

[25]  David Williams,et al.  The arrangement of the three cone classes in the living human eye , 1999, Nature.

[26]  M. Piccolino.  Cross-talk between cones and horizontal cells through the feedback circuit , 1995 .

[27]  J. Mollon,et al.  The spatial arrangement of cones in the primate fovea , 1992, Nature.

[28]  J. L. Schnapf,et al.  Electrical coupling between red and green cones in primate retina , 2004, Nature Neuroscience.

[29]  David J. Calkins,et al.  Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina , 1996, Nature.

[30]  Paul R. Martin,et al.  Chromatic sensitivity of ganglion cells in the peripheral primate retina , 2001, Nature.

[31]  M Kamermans,et al.  Hemichannel-Mediated Inhibition in the Outer Retina , 2001, Science.

[32]  P. Ahnelt,et al.  Telodendrial contacts between foveolar cone pedicles in the human retina , 1986, Experientia.

[33]  E. Yamada,et al.  The fine structure of the horizontal cells in some vertebrate retinae. , 1965, Cold Spring Harbor symposia on quantitative biology.

[34]  Mark Pottek,et al.  Modulation of coupling between retinal horizontal cells by retinoic acid and endogenous dopamine , 2000, Brain Research Reviews.

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

[36]  Peter Sterling,et al.  Electrical Coupling between Mammalian Cones , 2002, Current Biology.

[37]  M Yamada,et al.  Effects of dopamine on spatial properties of horizontal cell responses in the carp retina. , 1988, Neuroscience research. Supplement : the official journal of the Japan Neuroscience Society.

[38]  D. A. Burkhardt,et al.  Responses and receptive-field organization of cones in perch retinas. , 1977, Journal of neurophysiology.

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

[40]  B. Boycott,et al.  Organization of the Primate Retina: Light Microscopy , 1969 .

[41]  S. Wu,et al.  Feedback connections and operation of the outer plexiform layer of the retina , 1992, Current Opinion in Neurobiology.

[42]  A Kaneko,et al.  Electrical connexions between horizontal cells in the dogfish retina , 1971, The Journal of physiology.

[43]  P Lennie,et al.  Distinctive characteristics of subclasses of red–green P-cells in LGN of macaque , 1998, Visual Neuroscience.

[44]  W. Stell.  Correlation of retinal cytoarchitecture and ultrastructure in Golgi preparations , 1965, The Anatomical record.

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

[46]  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.

[47]  J. Davidson,et al.  Glycyrrhetinic acid derivatives: a novel class of inhibitors of gap-junctional intercellular communication. Structure-activity relationships. , 1988, The Journal of pharmacology and experimental therapeutics.

[48]  L. Croner,et al.  Receptive fields of P and M ganglion cells across the primate retina , 1995, Vision Research.

[49]  Joel Pokorny,et al.  Foveal cone detection statistics in color-normals and dichromats , 1991, Vision Research.

[50]  Joel Pokorny,et al.  Characterization and use of a digital light projector for vision research , 2001, Vision Research.

[51]  Drew Williams,et al.  Photopigment transmittance imaging of the primate photoreceptor mosaic , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  Barry B. Lee,et al.  Center surround receptive field structure of cone bipolar cells in primate retina , 2000, Vision Research.

[53]  K I Naka,et al.  Dogfish ganglion cell discharge resulting from extrinsic polarization of the horizontal cells , 1972, The Journal of physiology.

[54]  P. Lennie,et al.  Chromatic mechanisms in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[55]  R. Ruch,et al.  Gap‐junction disassembly and connexin 43 dephosphorylation induced by 18β‐glycyrrhetinic acid , 1996, Molecular carcinogenesis.

[56]  Paul R. Martin,et al.  Chromatic Organization of Ganglion Cell Receptive Fields in the Peripheral Retina , 2005, The Journal of Neuroscience.

[57]  M. Lankheet,et al.  Responses of cat horizontal cells to sinusoidal gratings , 1992, Vision Research.

[58]  S. Bloomfield,et al.  A comparison of receptive field and tracer coupling size of horizontal cells in the rabbit retina , 1995, Visual Neuroscience.

[59]  W. G. Owen,et al.  Gap junctions among the perikarya, dendrites, and axon terminals of the luminosity‐type horizontal cell of the turtle retina , 1983, The Journal of comparative neurology.

[60]  G Buchsbaum,et al.  Cost of cone coupling to trichromacy in primate fovea. , 2000, Journal of the Optical Society of America. A, Optics, image science, and vision.

[61]  R. L. Valois,et al.  Analysis of response patterns of LGN cells. , 1966, Journal of the Optical Society of America.

[62]  T. Tomita.  Electrophysiological study of the mechanisms subserving color coding in the fish retina. , 1965, Cold Spring Harbor symposia on quantitative biology.

[63]  Michael S. Landy,et al.  The Design of Chromatically Opponent Receptive Fields , 1991 .

[64]  T. Lamb,et al.  Spatial properties of horizontal cell responses in the turtle retina. , 1976, The Journal of physiology.

[65]  R. Shapley,et al.  Cat and monkey retinal ganglion cells and their visual functional roles , 1986, Trends in Neurosciences.

[66]  Michael S. Landy,et al.  Computational models of visual processing , 1991 .

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

[68]  J. Williams,et al.  Forskolin enhancement of opioid currents in rat locus coeruleus neurons. , 1996, Journal of neurophysiology.

[69]  W. Paulus,et al.  A new concept of retinal colour coding , 1983, Vision Research.

[70]  P. Lennie,et al.  Packing arrangement of the three cone classes in primate retina , 2001, Vision Research.

[71]  Joel Pokorny,et al.  Foveal cone thresholds , 1989, Vision Research.

[72]  J. C. Nelson,et al.  Neurotransmitter Coupling through Gap Junctions in the Retina , 1998, The Journal of Neuroscience.

[73]  P. Witkovsky,et al.  Sub-millimolar cobalt selectively inhibits the receptive field surround of retinal neurons , 1999, Visual Neuroscience.

[74]  D. Dacey,et al.  The Classical Receptive Field Surround of Primate Parasol Ganglion Cells Is Mediated Primarily by a Non-GABAergic Pathway , 2004, The Journal of Neuroscience.

[75]  R. Shapley,et al.  Space and Time Maps of Cone Photoreceptor Signals in Macaque Lateral Geniculate Nucleus , 2002, The Journal of Neuroscience.

[76]  F M de Monasterio,et al.  Center and surround mechanisms of opponent-color X and Y ganglion cells of retina of macaques. , 1978, Journal of neurophysiology.

[77]  D. Tolhurst,et al.  Trichromatic colour opponency in ganglion cells of the rhesus monkey retina. , 1975, The Journal of physiology.

[78]  L. Missotten,et al.  The ultrastructure of the human retina , 1965 .

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