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DM Dacey, BB Peterson, FR Robinson; Identification of an S-cone Opponent OFF Pathway in the Macaque Monkey Retina: Morphology, Physiology and Possible Circuitry . Invest. Ophthalmol. Vis. Sci. 2002;43(13):2983.
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© ARVO (1962-2015); The Authors (2016-present)
Purpose: A pathway for the transmission of S-cone signals to the primate lateral geniculate nucleus (LGN) has been previously identified. An S-cone selective 'blue'-cone bipolar cell provides synaptic input to a distinct bistratified ganglion cell type. This pathway transmits an S-cone ON, L+M cone OFF signal. By contrast, human psychophysical studies predict the existence of an S-cone OFF pathway, and there is evidence for such a signal at the level of the LGN and the primary visual cortex. We have now identified the origin of an S-OFF pathway in the macaque retina in vitro by using retrograde tracing to identify and intracellularly record from LGN-projecting ganglion cell types. Methods: The LGN was physiologically mapped and injections of biotinylated fluorescent dextrans were made at multiple loci. After retrograde transport of the tracer, retinas with attached choroid were dissected and maintained in vitro. Surprisingly, we found that when labeled cells were observed with episcopic illumination, sequestered specks of fluorescent tracer confined to the soma and proximal dendrites suddenly appeared to burst; released tracer then rapidly diffused throughout the entire dendritic tree revealing the complete morphology of novel LGN-projecting ganglion cell populations. The retrograde label and 'photofilling' were used to identify and target these cells in vitro for intracellular recording. Results: One of the LGN-projecting cell types showed a large, sparsely branched dendritic tree that was narrowly stratified in the inner portion of the inner plexiform layer (IPL) at approximately the same depth as the blue-cone bipolar. Surprisingly these sparse-monostratified cells revealed an S-cone OFF/L+M-cone ON color opponent light response. Bath application of ON-pathway blocker 2-amino-4-phosphonobutyric acid (AP-4) completely blocked both S-OFF and L+M components of the light response suggesting strongly that the S-OFF response is transmitted via the blue-cone bipolar, a presumed ON cell type. Conclusion: An S-cone OFF opponent signal originates from a sparse monostratified ganglion cell type that projects to the LGN in parallel with the S-cone ON small bistratified cell. The apparent costratification of the S-OFF cell with the blue-cone bipolar in the IPL and the block of the S-OFF light response with AP-4 suggest that both ON and OFF S-cone signals are transmitted to the inner retina via the ON S-cone bipolar cell and that a sign inversion of the ON signal in the inner retinal circuitry is critical for generation of this color opponent OFF pathway.
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