Characterization of a novel large-field cone bipolar cell type in the primate retina: Evidence for selective cone connections

Abstract Parallel processing of visual information begins at the first synapse in the retina between the photoreceptors and bipolar cells. Ten bipolar cell types have been previously described in the primate retina: one rod and nine cone bipolar types. In this paper, we describe an 11th type of bipolar cell identified in Golgi-stained macaque retinal whole mount and vertical section. Axonal stratification depth, in addition to dendritic and axonal morphology, distinguished the “giant” cell from all previously well-recognized bipolar cell types. The giant bipolar cell had a very large and sparsely branched dendritic tree and a relatively large axonal arbor that costratified with the DB4 bipolar cell near the center of the inner plexiform layer. The sparseness of the giant bipolar’s dendritic arbor indicates that, like the blue cone bipolar, it does not contact all the cones in its dendritic field. Giant cells contacting the same cones as midget bipolar cells, which are known to contact single long-wavelength (L) or medium-wavelength (M) cones, demonstrate that the giant cell does not exclusively contact short-wavelength (S) cones and, therefore, is not a variant of the previously described blue cone bipolar. This conclusion is further supported by measurement of the cone contact spacing for the giant bipolar. The giant cell contacts an average of about half the cones in its dendritic field (mean ± s.d. = 52 ± 17.6%; n = 6), with a range of 27–82%. The dendrites from single or neighboring giant cells that converge onto the same cones suggest that the giant cell may selectively target a subset of cones with a highly variable local density, such as the L or M cones.

[1]  H. Kolb,et al.  Organization of the outer plexiform layer of the primate retina: electron microscopy of Golgi-impregnated cells. , 1970, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[2]  R W Rodieck,et al.  Starburst amacrine cells of the primate retina , 1989, The Journal of comparative neurology.

[3]  E. V. Famiglietti,et al.  Functional architecture of cone bipolar cells in mammalian retina , 1981, Vision Research.

[4]  H. Wässle,et al.  Expression of the vesicular glutamate transporter vGluT2 in a subset of cones of the mouse retina , 2006, The Journal of comparative neurology.

[5]  U. Grünert,et al.  Immunocytochemical identification and analysis of the diffuse bipolar cell type DB6 in macaque monkey retina , 2001, The European journal of neuroscience.

[6]  H. Kolb,et al.  Midget ganglion cells of the parafovea of the human retina: A Study by electron microscopy and serial section reconstructions , 1991, The Journal of comparative neurology.

[7]  A. Mariani Giant bistratified bipolar cells in monkey retina , 1983 .

[8]  U. Grünert,et al.  Spatial density and immunoreactivity of bipolar cells in the macaque monkey retina , 1992, The Journal of comparative neurology.

[9]  R. W. Rodieck,et al.  Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus, and parvicellular laminae of the lateral geniculate nucleus , 1993, The Journal of comparative neurology.

[10]  Leon Lagnado,et al.  The retina , 1999, Current Biology.

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

[12]  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.

[13]  H. Kolb,et al.  Neurons of the human retina: A Golgi study , 1992, The Journal of comparative neurology.

[14]  B. Boycott,et al.  The cone synapses of cone bipolar cells of primate retina , 1997, Journal of neurocytology.

[15]  H. Wässle,et al.  Cone Contacts, Mosaics, and Territories of Bipolar Cells in the Mouse Retina , 2009, The Journal of Neuroscience.

[16]  J. Sahel,et al.  Glycine receptors in a population of adult mammalian cones , 2006, The Journal of physiology.

[17]  R. Pourcho,et al.  A combined Golgi and autoradiographic study of 3H-glycine-accumulating cone bipolar cells in the cat retina , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  David J. Calkins,et al.  M and L cones in macaque fovea connect to midget ganglion cells by different numbers of excitatory synapses , 1994, Nature.

[19]  S. Schein,et al.  Density profile of blue-sensitive cones along the horizontal meridian of macaque retina. , 1985, Investigative ophthalmology & visual science.

[20]  R. Masland,et al.  A population of wide‐field bipolar cells in the rabbit's retina , 1995, The Journal of comparative neurology.

[21]  S. Fisher,et al.  Retinal neurons of the California ground squirrel, Spermophilus beecheyi: A Golgi study , 1996, The Journal of comparative neurology.

[22]  S. Schein,et al.  Staining of blue-sensitive cones of the macaque retina by a fluorescent dye. , 1981, Science.

[23]  Richard H Masland,et al.  The population of bipolar cells in the rabbit retina , 2004, The Journal of comparative neurology.

[24]  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.

[25]  D. Marshak,et al.  Bipolar cells specific for blue cones in the macaque retina , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  H. Wässle,et al.  Glutamate Responses of Bipolar Cells in a Slice Preparation of the Rat Retina , 1996, The Journal of Neuroscience.

[27]  A. Cowey,et al.  The lengths of thefibres of henle in the retina of macaque monkeys: Implications for vision , 1988, Neuroscience.

[28]  Helga Kolb,et al.  Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study , 1981, Vision Research.

[29]  H. Wässle,et al.  Immunocytochemical identification of cone bipolar cells in the rat retina , 1995, The Journal of comparative neurology.

[30]  R. Dacheux,et al.  Rabbit cone bipolar cells: Correlation of their morphologies with whole-cell recordings , 2001, Visual Neuroscience.

[31]  A. Mariani,et al.  Biplexiform cells: ganglion cells of the primate retina that contact photoreceptors. , 1982, Science.

[32]  B. Boycott,et al.  Morphological Classification of Bipolar Cells of the Primate Retina , 1991, The European journal of neuroscience.

[33]  A. Hendrickson,et al.  A comparison of immunocytochemical markers to identify bipolar cell types in human and monkey retina , 2003, Visual Neuroscience.

[34]  R. West Bipolar and horizontal cells of the gray squirrel retina: Golgi morphology and receptor connections , 1978, Vision Research.

[35]  Heinz Wässle,et al.  Immunocytochemical analysis of bipolar cells in the macaque monkey retina , 1994, The Journal of comparative neurology.

[36]  H. Wässle,et al.  Types of bipolar cells in the mouse retina , 2004, The Journal of comparative neurology.

[37]  U. Grünert,et al.  S‐cone connections of the diffuse bipolar cell type DB6 in macaque monkey retina , 2004, The Journal of comparative neurology.

[38]  A. Mariani Bipolar cells in monkey retina selective for the cones likely to be blue-sensitive , 1984, Nature.

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

[40]  S. Massey,et al.  Morphology of bipolar cells labeled by DAPI in the rabbit retina , 1992, The Journal of comparative neurology.

[41]  H. Kolb,et al.  The neurons of the ground squirrel retina as revealed by immunostains for calcium binding proteins and neurotransmitters , 2002, Journal of neurocytology.