Macaque Retina Contains an S-Cone OFF Midget Pathway

Klug, Karl; Herr, Steve; Ngo, Ivy Tran; Sterling, Peter; Schein, Stan

doi:10.1523/jneurosci.23-30-09881.2003

Cited by 130 publications

(135 citation statements)

References 61 publications

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“…However, the S-cone OFF subdivision may contribute to additional functions other than color vision. OFF-type connections have been traced by electron microscopy from five S-cones to midget bipolar cells in macaques, which would, in principle, provide S-cone OFF input to a parvocellular pathway (13). However, in human peripheral retina (34), as in marmoset retina (14), synapses between S-cones and midget bipolar cells have not been found.…”

Section: Discussionmentioning

confidence: 99%

“…The S cones synapse with a specialized S-cone ON bipolar cell (10) that provides the S + signal to a small bistratified ganglion cell that is opposed by middle-wave-sensitive (M) and long-wave-sensitive (L) cone signals (11). The search for a parallel S-cone OFF bipolar cell has been controversial (12)(13)(14), notwithstanding unequivocal evidence that a small population of ganglion and LGN cells codes an S-cone OFF response (7,15). Recently, an S-cone OFF signal has been shown to provide input to a melanopsin-containing retinal ganglion cell (16).…”

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Aging of human short-wave cone pathways

Shinomori

Werner

2012

Proc. Natl. Acad. Sci. U.S.A.

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The retinal image is sampled concurrently, and largely independently, by three physiologically and anatomically distinct pathways, each with separate ON and OFF subdivisions. The retinal circuitry giving rise to an ON pathway receiving input from the short-wave-sensitive (S) cones is well understood, but the S-cone OFF circuitry is more controversial. Here, we characterize the temporal properties of putative S-cone ON and OFF pathways in younger and older observers by measuring thresholds for stimuli that produce increases or decreases in S-cone stimulation, while the middle-and long-wave-sensitive cones are unmodulated. We characterize the data in terms of an impulse response function, the theoretical response to a flash of infinitely short duration, from which the response to any temporally varying stimulus may be predicted. Results show that the S-cone response to increments is faster than to decrements, but this difference is significantly greater for older individuals. The impulse response function amplitudes for increment and decrement responses are highly correlated across individuals, whereas the timing is not. This strongly suggests that the amplitude is controlled by neural circuitry that is common to S-cone ON and OFF responses (photoreceptors), whereas the timing is controlled by separate postreceptoral pathways. The slower response of the putative OFF pathway is ascribed to different retinal circuitry, possibly attributable to a sign-inverting amacrine cell not present in the ON pathway. It is significant that this pathway is affected selectively in the elderly by becoming slower, whereas the temporal properties of the S-cone ON response are stable across the life span of an individual. O ne of the most basic properties of primate vision is that each point in the retinal image is sampled by at least three physiologically and anatomically distinct pathways (1, 2). These include a fast, high-contrast sensitivity, low-spatial resolution magnocellular pathway; and a slower, high-spatial resolution, chromatic parvocellular pathway. A third pathway, the koniocellular pathway, is color-opponent and slow, and it has poor spatial resolution. Overlaid onto the organization of these pathways are subdivisions into parallel ON and OFF systems (3). This originates at the first retinal synapse between the cone photoreceptor and the bipolar cell to give rise to the magnocellular or parvocellular pathways, resulting in further specialization and response selectivity for spatiotemporal luminance and/or chromatic increments (ON pathway) or decrements (OFF pathway). The assumption that detection of increments and decrements is mediated by separate ON and OFF pathways is supported by the work of Schiller et al. (4) in alert, behaving monkeys. During retinal infusion of the glutamate neurotransmitter analog 2-amino-4-phosphonobutyrate, which blocks synaptic transmission from cones to ON-bipolar cells but not OFFbipolar cells, there is a profound loss in the ability to detect increments but not decrements. A number of oth...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Aging of human short-wave cone pathways

Shinomori

Werner

2012

Proc. Natl. Acad. Sci. U.S.A.

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“…Two classes of ganglion cell in macaque retina show wide-field morphology and display blue-off type signals (15), but some of these cells also show intrinsic photosensitivity, making their role in color processing unclear. Evidence for a different source of blue-off signals was obtained from electron microscopic reconstruction of five S cones and their postsynaptic cells in macaque fovea (16). These experiments revealed off-type connections with midget-PC pathway bipolar cells, implying that blue-off cells (like red-green opponent cells) form part of the PC pathway (but see also ref.…”

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confidence: 97%

Geniculocortical relay of blue-off signals in the primate visual system

Szmajda

Buzás

FitzGibbon

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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A fundamental dichotomy in the subcortical visual system exists between on-and off-type neurons, which respectively signal increases and decreases of light intensity in the visual environment. In primates, signals for red-green color vision are carried by both on-and off-type neurons in the parvocellular division of the subcortical pathway. It is thought that on-type signals for blueyellow color vision are carried by cells in a distinct, diffusely projecting (koniocellular) pathway, but the pathway taken by blue-off signals is not known. Here, we measured blue-off responses in the subcortical visual pathway of marmoset monkeys. We found that the cells exhibiting blue-off responses are largely segregated to the koniocellular pathway. The blue-off cells show relatively large receptive fields, sluggish responses to maintained contrast, little sign of an inhibitory receptive-field surround mechanism, and negligible functional input from an intrinsic (melanopsin-based) phototransductive mechanism. These properties are consistent with input from koniocellular or ''W-like'' ganglion cells in the retina and suggest that blue-off cells, as previously shown for blue-on cells, could contribute to cortical mechanisms for visual perception via the koniocellular pathway.color vision ͉ short-wavelength-sensitive cones ͉ blue cones ͉ koniocellular pathway ͉ lateral geniculate nucleus T his study addresses the properties of sensory afferent pathways for primate color vision. Chromatic information is transmitted from the retina to the cortex via the lateral geniculate nucleus (LGN). Many neurons in the LGN show ''cone opponent'' responses: they are activated by a restricted range of wavelengths in the visible spectrum and inhibited by others. In trichromatic primates, the dorsal (parvocellular) layers of the LGN are dominated by neurons that show red-green cone opponent responses, as a result of antagonistic inputs arising in medium-wavelength-sensitive (M or ''green'') and longwavelength-sensitive (L or ''red'') cones. A smaller proportion of neurons in the retina and LGN shows blue-on responses, as a result of excitatory input arising in short-wavelength-sensitive (S) cones (1-5). Blue-on ganglion cells in the retina show a distinct bistratified morphology (5), and blue-on signals reach the visual cortex via the koniocellular/intercalated layers of the LGN (6, 7). Unlike cells in the parvocellular (PC) and ventral (magnocellular) layers, the constituent cells of koniocellular pathways show diverse functional properties and widespread cortical terminations and are considered to have arisen early in the evolutionary history of the visual system (7-9). The blue-on koniocellular cells thus have been considered as part of a primordial pathway for color vision (10). By contrast, the divergence of M and L cones to yield red-green signals in PC pathway cells occurred relatively recently (Ϸ15 million years ago) in the evolution of the primate visual system (11,12).Receptive fields receiving off-type signals from S cones (''blue-off'') r...

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“…However, these are luminance channels that receive input from all three cone types and appear to be unrelated to the specific S-cone ON and OFF pathway described here and by Klug et al (2003).…”

Section: Correspondence To Psychophysicsmentioning

confidence: 78%

“…Because the patch of foveal retina that we studied has 120 L/M cones for 6 S cones Klug et al, 2003), or 20 for 1, the blur circle centered on a foveal S cone spans ϳ20 L/M cones. From study of the identical patch of foveal retina, we know that the group of OFF diffuse bipolar cells that contact a foveal BY ganglion cell collects input from ϳ20 L/M cones (Calkins et al, 1998).…”

Section: The Critical Locus For By Color Visionmentioning

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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Macaque Retina Contains an S-Cone OFF Midget Pathway

Cited by 130 publications

References 61 publications

Aging of human short-wave cone pathways

Aging of human short-wave cone pathways

Geniculocortical relay of blue-off signals in the primate visual system

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

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