Synaptic Inputs to ON Parasol Ganglion Cells in the Primate Retina

In primates, the retinal ganglion cells that project to the magnocellular layers of the lateral geniculate nucleus have distinctive responses to light, and one of these has been identified morphologically as the parasol ganglion cell. To investigate their synaptic connections, we injected parasol cells with Neurobiotin in lightly fixed baboon retinas. The five ON-center cells we analyzed by electron microscopy received ∼20% of their input from bipolar cells. The major synaptic input to parasol cells was from amacrine cells via conventional synapses and, in this respect, they resembled α ganglion cells of the cat retina. We also found the gap junctions between amacrine cells and parasol ganglion cells that had been predicted from tracer-coupling experiments. To identify the presynaptic amacrine cells, ON-center parasol cells were injected with Neurobiotin and Lucifer yellow in living macaque retinas, which were then fixed and labeled by immunofluorescence. Two kinds of amacrine cells were filled with Neurobiotin via gap junctions: a large, polyaxonal cell containing cholecystokinin and a smaller one without cholecystokinin. There were also appositions between cholecystokinin-containing amacrine cell processes and parasol cell dendrites. Cholinergic amacrine cell processes often followed parasol cell dendrites and made extensive contacts. In other mammals, the light responses of polyaxonal amacrine cells like these and cholinergic amacrine cells have been recorded, and the effects of acetylcholine and cholecystokinin on ganglion cells are known. Using this information, we developed a model of parasol cells that accounts for some properties of their light responses.

[1]  S. Bloomfield,et al.  Tracer coupling pattern of amacrine and ganglion cells in the rabbit retina , 1997, The Journal of comparative neurology.

[2]  Paul R. Martin,et al.  Comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat, and the marmoset Callithrix jacchus , 1996, The Journal of comparative neurology.

[3]  A. Goodchild,et al.  Morphology of retinal ganglion cells in a New World monkey, the marmoset Callithrix jacchus , 1996, The Journal of comparative neurology.

[4]  W. Singer,et al.  Long-range synchronization of oscillatory light responses in the cat retina and lateral geniculate nucleus , 1996, Nature.

[5]  Correlated firing among different classes of ganglion cells in rabbit retina , 1996 .

[6]  S. Massey,et al.  ON α ganglion cells receive potential inputs from calbindin cone bipolar cells in the rabbit retina , 1996 .

[7]  H. Kolb,et al.  ON‐OFF amacrine cells in cat retina , 1996, The Journal of comparative neurology.

[8]  R. Masland,et al.  Responses to light of starburst amacrine cells. , 1996, Journal of neurophysiology.

[9]  H. Wässle,et al.  Receptive Field Properties of Starburst Cholinergic Amacrine Cells in the Rabbit Retina , 1995, The European journal of neuroscience.

[10]  G Buchsbaum,et al.  How retinal microcircuits scale for ganglion cells of different size , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  Heinz Wässle,et al.  The rod pathway of the macaque monkey retina: Identification of AII‐amacrine cells with antibodies against calretinin , 1995, The Journal of comparative neurology.

[12]  A. Hendrickson,et al.  Quantitative analysis of synaptogenesis in the inner plexiform layer of macaque monkey fovea , 1995, The Journal of comparative neurology.

[13]  A. Kaneko,et al.  Neuronal nicotinic acetylcholine receptors of ganglion cells in the cat retina. , 1995, The Japanese journal of physiology.

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

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

[16]  D. Marshak,et al.  Amino acid receptors of midget and parasol ganglion cells in primate retina. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[17]  A. Weber,et al.  Synaptology of physiologically identified ganglion cells in the cat retina: A comparison of retinal X‐ and Y‐cells , 1994, The Journal of comparative neurology.

[18]  Barry B. Lee,et al.  Physiology of indentified ganglion-cell types in an invitro preparation of macaque retina , 1994 .

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

[20]  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.

[21]  R. Masland,et al.  Responses of the starburst amacrine cells to moving stimuli. , 1993, Journal of neurophysiology.

[22]  B. Boycott,et al.  Parasol (Pα) ganglion-cells of the primate fovea: Immunocytochemical staining with antibodies against GABAA-receptors , 1993, Vision Research.

[23]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[24]  D. Dacey,et al.  Dendritic field size and morphology of midget and parasol ganglion cells of the human retina. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[27]  S. Bloomfield,et al.  Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. , 1992, Journal of neurophysiology.

[28]  R. W. Rodieck,et al.  Spatial density and distribution of choline acetyltransferase immunoreactive cells in human, macaque, and baboon retinas , 1992, The Journal of comparative neurology.

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

[30]  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.

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

[32]  PR Martin,et al.  Rod bipolar cells in the macaque monkey retina: immunoreactivity and connectivity , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  L. Peichl,et al.  Alpha ganglion cells in mammalian retinae: Common properties, species differences, and some comments on other ganglion cells , 1991, Visual Neuroscience.

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

[35]  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.

[36]  A. Mariani,et al.  Amacrine cells of the rhesus monkey retina , 1990, The Journal of comparative neurology.

[37]  C. Curcio,et al.  Topography of ganglion cells in human retina , 1990, The Journal of comparative neurology.

[38]  J. Del Valle,et al.  Localization of immunoreactive cholecystokinin precursor to amacrine cells and bipolar cells of the macaque monkey retina , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  A. Hendrickson,et al.  Distribution of GABA-immunoreactive amacrine cell synapses in the inner plexiform layer of macaque monkey retina , 1990, Visual Neuroscience.

[40]  Barry B. Lee,et al.  Chapter 7 New views of primate retinal function , 1990 .

[41]  P. Sterling,et al.  Structure of the starburst amacrine network in the cat retina and its association with alpha ganglion cells , 1989, The Journal of comparative neurology.

[42]  J. Dowling,et al.  Horizontal cell gap junctions: single-channel conductance and modulation by dopamine. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[43]  J. Naito Retinogeniculate projection fibers in the monkey optic nerve: A demonstration of the fiber pathways by retrograde axonal transport of WGA‐HRP , 1989, The Journal of comparative neurology.

[44]  W. Krebs,et al.  Quantitative morphology of the central fovea in the primate retina. , 1989, The American journal of anatomy.

[45]  R W Rodieck,et al.  Parasol and midget ganglion cells of the primate retina. , 1989, The Journal of comparative neurology.

[46]  R. Marc,et al.  Gap junctions in the inner plexiform layer of the goldfish retina , 1988, Vision Research.

[47]  B. Boycott,et al.  Neurofibrillar long-range amacrine cells in mammalian retinae , 1988, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[48]  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.

[49]  L. C. L. Silveira,et al.  Functional lamination in the ganglion cell layer of the macaque's retina , 1988, Neuroscience.

[50]  B. B. Lee,et al.  Visual resolution of macaque retinal ganglion cells. , 1988, The Journal of physiology.

[51]  L. Hersh,et al.  Synaptic organization of cholinergic amacrine cells in the rhesus monkey retina , 1988, The Journal of comparative neurology.

[52]  A. Hendrickson,et al.  Stratified distribution of synapses in the inner plexiform layer of primate retina , 1987, The Journal of comparative neurology.

[53]  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.

[54]  J. Bolz,et al.  Cholecystokinin in the cat retina. Action of exogenous CCK8 and localization of cholecystokinin-like immunoreactivity. , 1985, Investigative ophthalmology & visual science.

[55]  P. Gouras,et al.  Neurocircuitry of the retina : a Cajal memorial , 1985 .

[56]  R. W. Rodieck,et al.  Parasol and midget ganglion cells of the primate retina , 2004 .

[57]  R H Masland,et al.  The shape and arrangement of the cholinergic neurons in the rabbit retina , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[58]  A. Cowey,et al.  Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey , 1984, Neuroscience.

[59]  A. Cowey,et al.  Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey , 1984, Neuroscience.

[60]  D. Mastronarde Interactions between ganglion cells in cat retina. , 1983, Journal of neurophysiology.

[61]  D. Haines The Lesser Bushbaby (Galago) as an Animal Model: Selected Topics , 1982 .

[62]  E. Raviola,et al.  Structure of the synaptic membranes in the inner plexiform layer of the retina: A freeze‐fracture study in monkeys and rabbits , 1982, The Journal of comparative neurology.

[63]  K. Itoh,et al.  Retinal ganglion cell projections to individual layers of the lateral geniculate body in Galago crassicaudatus , 1982, The Journal of comparative neurology.

[64]  Helga Kolb,et al.  Amacrine cells of the cat retina , 1981, Vision Research.

[65]  R. Scobey Movement sensitivity of retinal ganglion cells in monkey , 1981, Vision Research.

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

[67]  R. W. Rodieck,et al.  Retinal ganglion cell classes in the Old World monkey: morphology and central projections. , 1981, Science.

[68]  F. M. D. Monasterio Center and surround mechanisms of opponent-color X and Y ganglion cells of retina of macaques. , 1978 .

[69]  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.

[70]  R. Scobey,et al.  Detection of image displacement by phasic cells in peripheral visual fields of the monkey , 1976, Vision Research.

[71]  Sanford L. Palay,et al.  The fine structure of the nervous system , 1976 .

[72]  J. Lund,et al.  Monkey retinal ganglion cells: Morphometric analysis and tracing of axonal projections, with a consideration of the peroxidase technique , 1975, The Journal of comparative neurology.

[73]  M. Dubin The inner plexiform layer of the vertebrate retina: A quantitative and comparative electron microscopic analysis , 1970, The Journal of comparative neurology.

[74]  V. Tennyson The Fine Structure of the Nervous System. , 1970 .

[75]  P Gouras,et al.  Antidromic responses of orthodromically identified ganglion cells in monkey retina , 1969, The Journal of physiology.

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

[77]  J. Dowling,et al.  Synaptic organization of the frog retina: an electron microscopic analysis comparing the retinas of frogs and primates , 1968, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[78]  P Gouras,et al.  The effects of light‐adaptation on rod and cone receptive field organization of monkey ganglion cells , 1967, The Journal of physiology.

[79]  B. Boycott,et al.  Organization of the primate retina: electron microscopy , 1966, Proceedings of the Royal Society of London. Series B. Biological Sciences.