Topographic specializations in the retinal ganglion cell layer of Australian passerines

Thornbills, honeyeaters, and silvereyes represent an abundant group of Australian passerines, whose diversity in niche differentiation suggests a pivotal role for vision. Using stereological methods and retinal wholemounts, we studied the topographic distribution of neurons in the ganglion cell layer of insectivorous, nectarivorous, and frugivorous species occupying terrestrial and arboreal microhabitats. All species studied have a central convexiclivate fovea (peak densities from 130,000 to 160,000 cells/mm²), which is shallow in the terrestrial/insectivorous yellow-rumped thornbill and deep in the arboreal/nectarivorous honeyeaters and frugivorous silvereye. Surrounding the fovea, neuronal densities in the ganglion cell layer form a broadly ovoid and asymmetric plateau in the yellow-rumped thornbill and a more restricted, circular and symmetric plateau in the other species. These differences in the plateau organization may reflect specific needs to locate food on the ground or among dense vegetation. We also found a temporal area (peak densities from 43,000 to 54,000 cells/mm²) across species, which increases spatial resolution in the frontal visual field and assists with foraging. Using microtubule-associated protein 2 (MAP2) immunohistochemistry, we detected a higher concentration of giant ganglion cells forming an area gigantocellularis in the temporal retina of all species. Giant ganglion cell densities also form a horizontal streak in all species, except in the yellow-rumped thornbill, which has an unusual increase toward the retinal periphery. In the yellow-rumped thornbill and silvereye, giant ganglion cells also peak in the nasal retina. We suggest that these topographic variations afford differential sampling of motion signals for the detection of predators.