Inner S‐cone bipolar cells provide all of the central elements for S cones in macaque retina

Herr, Steve; Klug, Karl; Sterling, Peter; Schein, Stan

doi:10.1002/cne.10553

Cited by 46 publications

(62 citation statements)

References 63 publications

(113 reference statements)

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“…Our material had only 12 inner S-cone bipolar cells, so their density, 2702 cells mm Ϫ2 , might not have been perfectly accurate as well. As shown by Herr et al (2003) for this patch of retina, in agreement with findings of Kouyama and Marshak (1997), there are ;2 inner S-cone bipolar cells for each S cone. Our density values were compatible with that finding.…”

Section: Comparison Of the Densities Of Inl Cells And Cone Pediclessupporting

confidence: 89%

“…There and elsewhere (Klug et al, 1992;Herr et al, 2003) we have reported that L and M cones contacted their own inner midget bipolar cells, whereas S cones did not. By contrast, S cones as well as other cones contacted outer midget bipolar cells (Klug et al, 1992).…”

Section: Midget Bipolar Cells-the Rule and The Exceptionsupporting

confidence: 55%

“…Even this small difference was for a reason: S cones do not have an inner midget bipolar cell (Herr et al, 2003).] In addition, the photomicrograph shown in Fig.…”

Section: Comparison Of the Densities Of Inl Cells And Cone Pediclesmentioning

confidence: 99%

“…Specifically, foveal cone pedicles are presynaptic to slightly more than 20 central elements (Chun et al, 1996). Eighty percent of these central elements (;16) are provided by an inner midget bipolar cell, leaving just 20% (;4) for inner diffuse bipolar cells (Herr et al, 2003; see also Kolb, 1970 andHopkins, 1991). With so few central-element slots left, some putative inner diffuse bipolar cells may not be able to fulfill their quota of central elements (Hopkins & Boycott, 1995Calkins et al, 1996) and may not differentiate into or survive as inner diffuse bipolar cells.…”

Section: Psychophysical Evidence For Asymmetrymentioning

confidence: 99%

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Cell density ratios in a foveal patch in macaque retina

Ahmad

Klug²,

Herr³

et al. 2003

Vis Neurosci

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We examine the assumptions that the fovea contains equal numbers of inner (invaginating or ON) and outer (flat or OFF) midget bipolar cells and equal numbers of inner and outer diffuse bipolar cells. Based on reconstruction from electron photomicrographs of serial thin sections through the fovea of a macaque monkey, we reject both assumptions. First, every foveal L and M cone is presynaptic to one inner and one outer midget bipolar cell; however, S cones are presynaptic to one outer but no inner midget bipolar cell. Second, we measure the density of all foveal cells in the same patch of fovea, affording accurate cell density ratios. For each foveal cone pedicle, at a density of 26,500 mm Ϫ2 , there is close to one (0.88) outer diffuse bipolar cell but only 0.40 inner diffuse bipolar cells. This asymmetry may be related to differences in resolution and sensitivity for light increments and decrements. We also find one (1.01) Müller cell, one (1.01) amacrine cell in the inner nuclear layer, and close to one (0.83) horizontal cell for each cone pedicle. In addition, for each S cone, there are two inner S-cone bipolar cells and two small bistratified ganglion cells. In total, there are 3.4 cone bipolar cells per cone but only 2.6 ganglion cells per cone. The latter ratio is enough to accommodate one midget ganglion cell for each midget bipolar cell.

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Section: Comparison Of the Densities Of Inl Cells And Cone Pediclessupporting

confidence: 89%

Section: Midget Bipolar Cells-the Rule and The Exceptionsupporting

confidence: 55%

“…Even this small difference was for a reason: S cones do not have an inner midget bipolar cell (Herr et al, 2003).] In addition, the photomicrograph shown in Fig.…”

Section: Comparison Of the Densities Of Inl Cells And Cone Pediclesmentioning

confidence: 99%

Section: Psychophysical Evidence For Asymmetrymentioning

confidence: 99%

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Cell density ratios in a foveal patch in macaque retina

Ahmad

Klug²,

Herr³

et al. 2003

Vis Neurosci

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show abstract

“…1 A) and S cone 52 (see Fig. 1 B), as described by Herr et al (2003). First, from each section, we traced the contour of the presynaptic face of the S-cone terminal by hand onto a clear plastic sheet (Herr et al, 2003, compare their Fig.…”

Section: Methodsmentioning

confidence: 99%

Evidence That Each S Cone in Macaque Fovea Drives One Narrow-Field and Several Wide-Field Blue-Yellow Ganglion Cells

Schein¹,

Sterling²,

Ngo³

et al. 2004

J. Neurosci.

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A rule of retinal wiring is that many receptors converge onto fewer bipolar cells and still fewer ganglion cells. However, for each S cone in macaque fovea, there are two S-cone ON bipolar cells and two blue-yellow (BY) ganglion cells. To understand this apparent rule reversal, we reconstructed synaptic patterns of divergence and convergence and determined the basic three-tiered unit of connectivity that repeats across the retina. Each foveal S cone diverges to four S-cone ON bipolar cells but contacts them unequally, providing 1-16 ribbon synapses per cell. Next, each bipolar cell diverges to two BY ganglion cells and also contacts them unequally, providing ϳ14 and ϳ28 ribbon synapses per cell. Overall, each S cone diverges to approximately six BY ganglion cells, dominating one and contributing more modestly to the others. Conversely, of each pair of BY ganglion cells, one is dominated by a single S cone and one is diffusely driven by several. This repeating circuit extracts blue/yellow information on two different spatiotemporal scales and thus parallels the circuits for achromatic, spatial vision, in which each cone dominates one narrow-field ganglion cell (midget) and contributes some input to several wider-field ganglion cells (parasol). Finally, because BY ganglion cells have coextensive ϩS and Ϫ(LϩM) receptive fields, and each S cone contributes different weights to different BY ganglion cells, the coextensive receptive fields must be already present in the synaptic terminal of the S cone. The S-cone terminal thus constitutes the first critical locus for BY color vision.

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Two ribbon synaptic units in rod photoreceptors of macaque, human, and cat

Migdale

Herr

Klug

et al. 2002

J of Comparative Neurology

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The rod photoreceptor's synaptic terminal (or spherule) uses an elaborate synaptic structure to signal absorption of one or more photons to its postsynaptic targets. This structure includes one or two synaptic ribbons inside the terminal and a pouch-like "invagination" outside the terminal, into which enter a widely variable number of incoming fibers and postsynaptic targets-central elements supplied by rod bipolar cells and lateral elements supplied by horizontal cells. Nonetheless, our three-dimensional reconstructions of this synaptic structure in foveal retina of macaque monkey and peripheral retina of human and cat reveal several features that are highly conserved across species and with eccentricity: 1). every spherule has one invagination; 2). with rare exceptions, every spherule has two ribbon synaptic units with these features: a). on the presynaptic side, each ribbon synaptic unit has a ribbon or part of a ribbon and one trough-shaped arciform density that demarcates its active zone; b). on the postsynaptic side, each ribbon synaptic unit has two apposed lateral elements and one or more central elements; 3). the volume of the extracellular space in the single invagination is small, approximately 0.1 microm(3); and 4). the largest distance from active zone to receptor regions on bipolar cells is small, less than approximately 1.5 microm. With such small dimensions, release of one quantum of transmitter can pulse glutamate to a concentration comparable to the EC(50) of the metabotropic glutamate receptors on the central elements associated with both synaptic units. We speculate that two ribbon synaptic units are required to sustain the high quantal release rate needed to signal a single photon.

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Inner S‐cone bipolar cells provide all of the central elements for S cones in macaque retina

Cited by 46 publications

References 63 publications

Cell density ratios in a foveal patch in macaque retina

Cell density ratios in a foveal patch in macaque retina

Evidence That Each S Cone in Macaque Fovea Drives One Narrow-Field and Several Wide-Field Blue-Yellow Ganglion Cells

Two ribbon synaptic units in rod photoreceptors of macaque, human, and cat

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