How retinal microcircuits scale for ganglion cells of different size

Ganglion cell receptive field centers are small in central retina and larger toward periphery. Accompanying this expansion, the distribution of sensitivity across the centers remain Gaussian, but peak sensitivities decline. To identify circuitry that might explain this physiology, we measured the density of bipolar cell synapses on the dendritic membrane of beta (X) and alpha (Y) ganglion cells and the distribution of dendritic membrane across their dendritic fields. Both central and peripheral beta cells receive bipolar cell synapses at a density of approximately 28/100 microns2 of dendritic membrane; central and peripheral alpha cells receive approximately 13/100 microns2. The distribution of dendritic membrane across the dendritic field is dome- like; therefore, the distribution of bipolar cell synapses is also dome- like. As the dendritic field enlarges, total postsynaptic membrane increases with field radius, but only linearly. Consequently, density of postsynaptic membrane in the dendritic field declines, and so does density of synapses within the field. The results suggest a simple model in which the receptive field center's Gaussian profile and peak sensitivity are both set by the density of bipolar cell synapses across the dendritic field.

[1]  G. Buchsbaum,et al.  Mammalian rod terminal: Architecture of a binary synapse , 1995, Neuron.

[2]  N. Vardi,et al.  Specific cell types in cat retina express different forms of glutamic acid decarboxylase , 1995, The Journal of comparative neurology.

[3]  DI Vaney,et al.  Territorial organization of direction-selective ganglion cells in rabbit retina , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  R H Masland,et al.  Receptive fields and dendritic structure of directionally selective retinal ganglion cells , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  Z J Zhou,et al.  Ligand-gated currents of alpha and beta ganglion cells in the cat retinal slice. , 1994, Journal of neurophysiology.

[6]  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.

[7]  M. Pu,et al.  Structure and function of retinal ganglion cells innervating the cat's geniculate wing: an in vitro study , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  R. Miller,et al.  The role of NMDA and non-NMDA excitatory amino acid receptors in the functional organization of primate retinal ganglion cells , 1994, Visual Neuroscience.

[9]  Shigang He Further investigations of direction-selective ganglion cells of the rabbit retina , 1994 .

[10]  D. Copenhagen,et al.  The contribution of NMDA and Non-NMDA receptors to the light-evoked input-output characteristics of retinal ganglion cells , 1993, Neuron.

[11]  H. Kolb,et al.  OFF‐alpha and OFF‐beta ganglion cells in cat retina. I: Intracellular electrophysiology and HRP stains , 1993, The Journal of comparative neurology.

[12]  H. Kolb,et al.  Off‐alpha and OFF‐beta ganglion cells in cat retina: II. Neural circuitry as revealed by electron microscopy of HRP stains , 1993, The Journal of comparative neurology.

[13]  R. Williams,et al.  Rapid evolution of the visual system: a cellular assay of the retina and dorsal lateral geniculate nucleus of the Spanish wildcat and the domestic cat , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  D. Dacey,et al.  A coupled network for parasol but not midget ganglion cells in the primate retina , 1992, Visual Neuroscience.

[15]  Peter Sterling,et al.  Gap junctions between the pedicles of macaque foveal cones , 1992, Vision Research.

[16]  Peter Sterling,et al.  Parallel Circuits from Cones to the On‐Beta Ganglion Cell , 1992, The European journal of neuroscience.

[17]  P Sterling,et al.  Computational model of the on-alpha ganglion cell receptive field based on bipolar cell circuitry. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[18]  M. McCall,et al.  Synaptic inputs to physiologically identified retinal X‐cells in the cat , 1991, The Journal of comparative neurology.

[19]  R. Pourcho,et al.  Connectivity of glycine immunoreactive amacrine cells in the cat retina , 1991, The Journal of comparative neurology.

[20]  D. I. Vaney,et al.  Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin , 1991, Neuroscience Letters.

[21]  P Sterling,et al.  Microcircuitry related to the receptive field center of the on-beta ganglion cell. , 1991, Journal of neurophysiology.

[22]  Y Tsukamoto,et al.  Spatial summation by ganglion cells: some consequences for the efficient encoding of natural scenes. , 1991, Neuroscience research. Supplement : the official journal of the Japan Neuroscience Society.

[23]  P Sterling,et al.  Convergence and divergence of cones onto bipolar cells in the central area of cat retina. , 1990, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[24]  P. Sterling,et al.  "Collective coding" of correlated cone signals in the retinal ganglion cell. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[25]  S. Massey,et al.  Chapter 11 Cell types using glutamate as a neurotransmitter in the vertebrate retina , 1990 .

[26]  R. Pourcho,et al.  Distribution of GABA immunoreactivity in the cat retina: A light- and electron-microscopic study , 1989, Visual Neuroscience.

[27]  H. Wässle,et al.  GABA‐like immunoreactivity in the cat retina: Electron microscopy , 1989, The Journal of comparative neurology.

[28]  P Sterling,et al.  The ON-alpha ganglion cell of the cat retina and its presynaptic cell types , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  P. Sterling,et al.  Architecture of rod and cone circuits to the on-beta ganglion cell , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  X-cells in the cat retina: relationships between the morphology and physiology of a class of cat retinal ganglion cells. , 1987, Journal of neurophysiology.

[31]  Robert G. Smith Montage: a system for three-dimensional reconstruction by personal computer , 1987, Journal of Neuroscience Methods.

[32]  P. Sterling,et al.  Microcircuitry of beta ganglion cells in cat retina , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  Y. Fukuda,et al.  Electron microscopic analysis of amacrine and bipolar cell inputs on Y-, X- and W-cells in the cat retina , 1985, Brain Research.

[34]  R. Masland,et al.  Local order among the dendrites of an amacrine cell population , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  Stephen C. Massey,et al.  Light evoked release of acetylcholine in response to a single flash: cholinergic amacrine cells receive ON and OFF input , 1985, Brain Research.

[36]  P Sterling,et al.  Microcircuitry of bipolar cells in cat retina , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  R. Masland,et al.  The functions of acetylcholine in the rabbit retina , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[38]  H. Wässle,et al.  The structural correlate of the receptive field centre of alpha ganglion cells in the cat retina. , 1983, The Journal of physiology.

[39]  C. Enroth-Cugell,et al.  Receptive field properties of X and Y cells in the cat retina derived from contrast sensitivity measurements , 1982, Vision Research.

[40]  T. Poggio,et al.  Retinal ganglion cells: a functional interpretation of dendritic morphology. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[41]  J. Adams Heavy metal intensification of DAB-based HRP reaction product. , 1981, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[42]  Peter Sterling,et al.  A systematic approach to reconstructing microcircuitry by electron microscopy of serial sections , 1980, Brain Research Reviews.

[43]  P. Sterling,et al.  Toward a functional architecture of the retina: serial reconstruction of adjacent ganglion cells. , 1980, Science.

[44]  B. Cleland,et al.  Visual resolution and receptive field size: examination of two kinds of cat retinal ganglion cell. , 1979, Science.

[45]  H. Kolb The inner plexiform layer in the retina of the cat: electron microscopic observations , 1979, Journal of neurocytology.

[46]  H. Wässle,et al.  Size, scatter and coverage of ganglion cell receptive field centres in the cat retina. , 1979, The Journal of physiology.

[47]  B. Boycott,et al.  The morphological types of ganglion cells of the domestic cat's retina , 1974, The Journal of physiology.

[48]  R. H. Steinberg,et al.  The distribution of rods and cones in the retina of the cat (Felis domesticus) , 1973, The Journal of comparative neurology.

[49]  B. Sakmann,et al.  Sensitivity distribution and spatial summation within receptive-field center of retinal on-center ganglion cells and transfer function of the retina. , 1970, Journal of neurophysiology.

[50]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[51]  R. W. Rodieck,et al.  Analysis of receptive fields of cat retinal ganglion cells. , 1965, Journal of neurophysiology.

[52]  B. Boycott,et al.  Neural connections of the retina: fine structure of the inner plexiform layer. , 1965, Cold Spring Harbor symposia on quantitative biology.

[53]  T. Wiesel Receptive fields of ganglion cells in the cat's retina , 1960, The Journal of physiology.