Topographic specializations in the retinal ganglion cell layer correlate with lateralized visual behavior, ecology, and evolution in cockatoos.

Abstract

Cockatoos are a unique avian group inhabiting a diversity of arboreal and terrestrial microhabitats. Most species display strong lateralized visual behaviors using their left eye/foot to assist with food manipulation during foraging. In this study, we used retinal wholemounts and stereological methods to investigate whether the topographic distribution of retinal ganglion cells in cockatoos reflects their lateralized behaviors and microhabitat diversity. We found that all species studied possess a horizontal visual streak and a shallow central fovea that afford increased spatial resolution in the lateral visual field. Arboreal cockatoos have a well-defined dorsotemporal area, in contrast to terrestrial cockatoos, in which this specialization is inconspicuous or absent. Terrestrial cockatoos also have a triangular extension of increased ganglion cell density directed toward the dorsotemporal retinal periphery. Both the dorsotemporal area and the triangular extension enhance spatial resolution in the frontal and inferior visual fields, which potentially assists with binocular coordination during foraging. We found significantly higher ganglion cell densities in the left (52,000-72,000 cells/mm2) compared with the right (42,500-50,000 cells/mm2) perifoveal region of species that have strong left eye-left foot lateralized behaviors. In contrast, cockatoo species that show no lateralized behaviors have equivalent retinal ganglion cell densities in both left and right perifoveal regions (42,500-52,500 cells/mm2). Retinal ganglion cell peak densities in the dorsotemporal area showed no significant difference between left and right eyes for any species, suggesting that cockatoos use both eyes to extract information in the binocular visual field, independent of the degree of lateralization.