Expression of cell markers and transcription factors in the avian retina compared with that in the marmoset retina

Abstract

In the vertebrate retina, amacrine and ganglion cells represent the most diverse cell classes. They can be classified into different cell types by several features, such as morphology, light responses, and gene expression profile. Although birds possess high visual acuity (similar to primates that we used here for comparison) and tetrachromatic color vision, data on the expression of transcription factors in retinal ganglion cells of birds are largely missing. In this study, we tested various transcription factors, known to label subpopulations of cells in mammalian retinae, in two avian species: the common buzzard (Buteo buteo), a raptor with exceptional acuity, and the domestic pigeon (Columba livia domestica), a good navigator and widely used model for visual cognition. Staining for the transcription factors Foxp2, Satb1 and Satb2 labeled most ganglion cells in the avian ganglion cell layer. CtBP2 was established as marker for displaced amacrine cells, which allowed us to reliably distinguish ganglion cells from displaced amacrine cells and assess their densities in buzzard and pigeon. When we additionally compared the temporal and central fovea of the buzzard with the fovea of primates, we found that the cellular organization in the pits was different in primates and raptors. In summary, we demonstrate that the expression of transcription factors is a defining feature of cell types not only in the retina of mammals but also in the retina of birds. The markers, which we have established, may provide useful tools for more detailed studies on the retinal circuitry of these highly visual animals.

Satb1 expression in retinal ganglion cells of marmosets, macaques, and humans

“…The ganglion cell density further decreased to ∼2000 cell/mm 2 at 4 mm eccentricity in the temporal retina and ∼3000 cells/mm 2 in the nasal retina. These values are comparable to previous estimates at equivalent eccentricities (Haverkamp et al, 2021;Nasir-Ahmad et al, 2021;Wilder et al, 1996). To conclude, the proportion of Satb1-expressing ganglion cells increases slightly with a distance from the fovea, from approximately 2% at 1 mm to 5−7% in the peripheral retina (Figure 3b).…”

“…The (Haverkamp et al, 2021;Yamagata et al, 2021), and primates (this study). In the mouse retina, Satb1-expressing ganglion cells were identified as on-off DS ganglion cells (Peng et al, 2017;Sweeney et al, 2019).…”

“…In the mouse retina, Satb1-expressing ganglion cells were identified as on-off DS ganglion cells (Peng et al, 2017;Sweeney et al, 2019). In avian retinas, Satb1 is expressed by the large majority of ganglion cells (Haverkamp et al, 2021;Yamagata et al, 2021) and for the buzzard retina, it was suggested that Satb1 is expressed by at least seven ganglion cell types based on coexpression with other transcription factors and differences in soma size and immunostaining intensity (Haverkamp et al, 2021). The specific ganglion cell types expressing Satb1 have not been determined in birds, but in the chicken retina no equivalents to mouse DS cells or to primate midget and parasol cells were detected using single-cell transcriptomics (Yamagata et al, 2021).…”

Immunohistochemical characterization of bipolar cells in four distantly related avian species

“…Here, we labeled the avian retina with an antibody against SCGN and found very different staining pattern (Figure 8), depending on the species and retinal region examined. In chicken and the peripheral pigeon retina (Figure 8a and b), the staining resembled calretinin labeling (Fischer et al, 2007;Haverkamp et al, 2021) with prominent staining of horizontal cells and some amacrine cells. Bipolar cells were only weakly SCGN+.…”

“…The polyclonal calbindin (Calb) antibody from guinea pig recognizes human calbindin D28k and produces a band of 28 kDa in a western blot from rat brain homogenate. It labeled the same cells in the bird retina as a polyclonal calbindin antibody raised in rabbit which we used earlier (Haverkamp et al., 2021).…”