Abstract
The retinas of many species show regional specialisations that are evident in the differences in the processing of visual input from different parts of the visual field. Regional specialisation is thought to reflect an adaptation to the natural visual environment, optical constraints, and lifestyle of the species. Yet, little is known about regional differences in synaptic circuitry. Here, we were interested in the topographical distribution of connexin-36 (Cx36), the major constituent of electrical synapses in the retina. We compared the retinas of mice, rats, and cats to include species with different patterns of regional specialisations in the analysis. First, we used the density of Prox1-immunoreactive amacrine cells as a marker of any regional specialisation, with higher cell density signifying more central regions. Double-labelling experiments showed that Prox1 is expressed in AII amacrine cells in all three species. Interestingly, large Cx36 plaques were attached to about 8–10% of Prox1-positive amacrine cell somata, suggesting the strong electrical coupling of pairs or small clusters of cell bodies. When analysing the regional changes in the volumetric density of Cx36-immunoreactive plaques, we found a tight correlation with the density of Prox1-expressing amacrine cells in the ON, but not in the OFF sublamina in all three species. The results suggest that the relative contribution of electrical synapses to the ON- and OFF-pathways of the retina changes with retinal location, which may contribute to functional ON/OFF asymmetries across the visual field.
Highlights
The retinas of most species show some type of regional specialisation that is evident in the distribution of photoreceptors and other cell types
We have observed a centre-periphery gradient in the density of Cx36 immunolabelled puncta in the ON-sublamina of the inner plexiform layer of cats [47]. We extend these observations to any eccentricity-driven variation of inner retinal gap junction distribution in cats, rats and mice that represent species with different patterns of retinal specialisations
The homeodomain protein Prox1 is expressed in horizontal cells, bipolar cells and AII amacrine cells of the adult mouse retina [51,52]
Summary
The retinas of most species show some type of regional specialisation that is evident in the distribution of photoreceptors and other cell types. Regional specialisations are thought to reflect an adaptation to the natural visual environment, optical constraints, and lifestyle of the species [1,2]. The neural circuitry is specialised for high-acuity vision, which in primates is reflected by the number of cones converging on bipolar cells and eventually, on ganglion cells [6,7]. In the outer retina, gap junctions formed by Cx36 connect cone photoreceptors [13,23,24,25,26] with each other. Cx36 gap junctions connecting rods to cones form the secondary rod pathway [10,11], which is thought to be responsible for light detection at mid-scotopic intensity levels [14,27]
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