The distributions of rod and cone photoreceptors have been determined in the retina of the California ground squirrel, Spermophilus beecheyi. Retinas were fixed by perfusion and the rods and cones were detected with indirect immunofluorescence using opsin antibodies. Local densities were determined at 2-mm intervals across the entire retina, from which total numbers of each receptor type were estimated and isodensity distributions were constructed. The ground squirrel retina contains 7.5 million cones and 1.27 million rods. The peak density for the cones (49,550/mm2) is found in a horizontal strip of central retina 2 mm ventral to the elongated optic nerve head, falling gradually to half this value in the dorsal and ventral retinal periphery. Of the cones, there are 14 M cones for every S cone. S cone density is relatively flat across most of the retina, reaching a peak (4500/mm2) at the temporal end of the visual streak. There is one exception to this, however: S cone density climbs dramatically at the extreme dorso-nasal retinal margin (20,000/mm2), where the local ratio of S to M cones equals 1. Rod density is lowest in the visual streak, where the rods comprise less than 5% of the local photoreceptor population, increasing conspicuously in the ventral retina, where the rods achieve 30% of the local photoreceptor population (13,000/mm2). The functional importance of the change in S to M cone ratio at the dorsal circumference of the retina is compromised by the extremely limited portion of the visual field subserved by this retinal region. The significance for vision, if any, remains to be determined. By contrast, the change in rod/cone ratio between the dorsal and ventral halves of the retina indicates a conspicuous asymmetry in the ground squirrel's visual system, suggesting a specialization for maximizing visual sensitivity under dim levels of illumination in the superior visual field.
The mosaic of photoreceptors is regarded as a prime example of the precise control of cellular positioning in the vertebrate nervous system. This study was undertaken with the idea that understanding the intrinsic geometrical features of photoreceptor mosaics is a necessary step to unveil the biological mechanisms governing their formation. We show in the retina of the ground squirrel that the arrays of both the rods and S cones are non-random, but that nothing more than a simple minimal-spacing rule constraining receptor positioning is sufficient to account for the spatial organization of both mosaics. The size of this 'exclusion zone' is an intrinsic characteristic of each cell type, and it is simply the difference in the size of this domain that accounts for the regularity of the S cone array and the irregularity of the rod array at identical density. Consequently, regularity in receptor mosaics is produced by two independent biological events, one embodying the exclusion zone, and another specifying the local density of a given receptor type.
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