Comparison of topographical patterns of ganglion and photoreceptor cell differentiation in the retina of the zebrafish,Danio rerio

Abstract

Earlier studies suggested retinal differentiation in the zebrafish commences ventrally rather than centrally as is the case in other vertebrates. Here we describe the topographical spread of cell differentiation for ganglion cells, double cones and rods in the zebrafish retina between 36 and 72 hours postfertilization (hpf), by using immunohistochemical markers in retinal wholemounts. Staining for all three cell types commenced within the ventral retina on the nasal side of the optic nerve and choroid fissure, at 38 hpf for ganglion cells and 50 hpf for double cones and rods. Within 3 to 4 hours, the staining of ganglion cells and double cones spread in a continuous wave-like fashion into the nasal region of the ventral retina. After this time, the staining patterns for ganglion cells and double cones progressed dorsally into the central and temporal retina. Finally, stained somata of ganglion cells were observed within the temporal-ventral region by approximately 48 hpf, more than 8 hours later than the first ganglion cells within the nasal retina. The topographical spread of double cone staining was slightly less orderly. After staining had extended into the nasal retina between 50 and 54 hpf, a small group of stained double cones often appeared at the temporal edge of the choroid fissure by 56 hpf, simultaneously with initial staining observed dorsal and temporal to the optic nerve. The topographical spread of rod staining in the ventral retina was more symmetrical. After rod staining appeared near the nasal edge of the choroid fissure at 50 hpf, rods accumulated within a localized patch nasal to the fissure. Approximately 5 hours after initial rod staining, scattered rod staining appeared on the temporal side of the choroid fissure (approximately 55-57 hpf). Rods increased rapidly within the ventral retina, and a dense symmetrical patch extended out from the choroid fissure into the nasal and temporal regions of the ventral retina by 70 hpf. A scattered pattern of rod staining also occurred within the dorsal retina at this time.

Zebrafish: A model system for the study of eye genetics

“…Unlike rodent models, the zebrafish is diurnal and its retina contains a large number of diverse cone subtypes in addition to rods (Branchek, 1984;Branchek and Bremiller, 1984;Larison and Bremiller, 1990;Raymond et al, 1993;Raymond et al, 1995;Schmitt and Dowling, 1996).…”

“…The conservation between the fly and vertebrates of numerous aspects of neurogenesis has lead to the speculation that lateral inhibition plays a role in mosaic formation in the vertebrate retina analogous to the role of lateral inhibition during specification and patterning of photoreceptor cells in the Drosophila ommatidia (Cagan and Ready, 1989;Baker et al, 1990;Raymond et al, 1995;Schmitt and Dowling, 1996). In the retina, lateral inhibition plays a role in the specification of early versus late neuronal cell types and has been suggested to have a second role in mosaic organization of the photoreceptor cells through maintenance of radial patterning (Ahmad et al, 1997;Austin et al, 1995;Bernardos, et al, 2005;Waid and McLoon, 1998).…”

“…The first postmitotic cells and differentiation of ganglion cells are identifiable between 28 hpf and 32 hpf, in the ventral patch, a region of precocious neural development in the ventral-nasal retina (Kljavin, 1987;Dowling, 1994, 1996;Burrill and Easter, 1995;Hu and Easter, 1999). Differentiation then spreads dorsally around to the ventral temporal retina in a wave-like manner reminiscent of the movement of the morphogenetic furrow in Drosophila (Schmitt and Dowling, 1996). Also similar to Drosophila, the wave of differentiation is associated with a wave of sonic hedgehog expression by the differentiating cells (Neumann and Nuesslein-Volhard, 2000;Shkumatava et al, 2004).…”

Analysis of the retina in the zebrafish model

“…The early onset of ganglion cell differentiation is again conserved in many vertebrate phyla (Altshuler et al, 1991). Similar to expression patterns that characterize the genetic regulators of retinal neurogenesis, differentiated ganglion cells first appear in the ventral retina, nasal to the optic nerve (Burrill and Easter, 1995;Schmitt and Dowling, 1996). The rudiments of the ganglion cell layer are recognizable in histological sections by 36 hpf.…”

“…Determination of expression pattern on protein level Schmitt and Dowling (1996) Antibody staining (sections)…”