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Christian Puller, Michael B Manookin, Maureen Neitz, Jay Neitz; Clustering of syntaxin-4 and cation-chloride transporters beneath S-cones suggests a synaptic specialization for color vision exclusive to human and non-human primates. Invest. Ophthalmol. Vis. Sci. 2014;55(13):4530.
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© ARVO (1962-2015); The Authors (2016-present)
Recently, we found elevated expression levels of the SNARE protein syntaxin-4 in horizontal cells beneath short wavelength sensitive (S-)cones of macaque retina. This phenomenon was not observed beneath S-cones of mouse and ground squirrel retinas (Puller et al., 2012, ARVO 53:6323). Here, we have surveyed the expression patterns of syntaxin-4 and cation-chloride cotransporters in the outer retinas of additional primate species, including representatives of human, Old World and New World monkeys.
Immunohistochemical labeling of syntaxin-4, the sodium-potassium-chloride cotransporter NKCC and the potassium-chloride cotransporter KCC2 was performed on vertical sections and whole-mount preparations of human, macaque, baboon, and marmoset retinas. The labeling was combined with antibodies against cell marker proteins, such as S-opsin, parvalbumin, or calbindin.
Syntaxin-4 was densely clustered beneath S-cones in all primates investigated and it was colocalized with the dendritic tips of HII horizontal cells at these sites. As we have shown previously in macaque, the staining of syntaxin-4 beneath S-cones exceeded staining intensities beneath long (L-) or middle (M-) wavelength sensitive cones. Similarly, discrete and dense NKCC puncta were found to be enriched beneath S-cones when compared to the diffuse and sparse staining at L/M-cones. The expression pattern of KCC2 is currently being investigated.
Syntaxin-4 and chloride transporters are proposed to be components of a GABA-mediated feed-forward circuit from horizontal cells to bipolar cells. Although the corresponding synaptic elements are expressed in mouse and ground squirrel retinas, enrichment at S-cones was not observed in these species. Therefore, our data points to a primate-specific adjustment within the HII horizontal cell circuitry. We hypothesize that GABA directly acts on bipolar cells in support of enhanced processing of spectrally opponent signals.
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