The Lens Has a Specific Influence on Optic Nerve and Tectum Development in the Blind Cavefish <i>Astyanax</i>

Abstract

We used the teleost Astyanaxmexicanus to examine the role of the lens in optic nerve and tectum development. This speciesis unusually suited for studies of nervous system development and evolution because of its two extant forms: an eyed surface dwelling (surface fish) and several blind cave dwelling (cavefish) forms. Cavefish embryos initially form eye primordia, but the lens eventually dies by apoptosis, then the retina ceases to grow, and finally the degenerating eyes sink into the orbits. Transplantation of an embryonic surface fish lens into a cavefish optic cup restores eye development. We show here that retinal nerve fibers are formed and project to the optic tectum in cavefish embryos. In adult cavefish that have completed lens degeneration, however, the number of retinal axons in the optic nerve is substantially reduced compared to surface fish. The presumptive brain domains of embryonic cavefish are not altered relative to surface fish based on expression of the regional marker genes Pax6, Pax2.1, and engrailed2. In contrast, the adult cavefish brain is elongated, the optic tectum is diminished in volume, and the number of tectal neurons is reduced relative to surface fish. Unilateral transplantation of an embryonic surface fish lens into a cavefish optic cup increases the size of the optic nerve, the number of retinotectal projections from the restored eye, and the volume and neuronal content of the contralateral optic tectum. The results suggest that the lens has a specific influence on optic nerve and tectum development during eye growth in Astyanax.

Developmental mechanisms for retinal degeneration in the blind cavefish Astyanax mexicanus

“…Previous analysis has shown massive apoptosis in the lens of CF, starting at 25 hpf (Jeffery and Martasian, 1998) and still present at 5 dpf and 10 dpf (Soares et al, 2004), which appears to be Shh dependent . Here, we investigated and compared apoptosis in sections of the neural retina through earlier development (Fig.…”

Shadow response in the blind cavefishAstyanaxreveals conservation of a functional pineal eye

“…Thus, other factors, such as increased opacity in the cranium that may impede light penetration, may responsible for the diminishment of light detection by the pineal eye. Alternatively, minimal development of an organized retina, photoreceptor cells, and a ganglion layer with functional projections to the optic tectum prior to subsequent degeneration (Voneida and Sligar, 1976;Yamamoto and Jeffery, 2000;Soares et al, 2004), may be sufficient to inhibit pineal eye function during development.…”

“…During larval development, however, the cavefish eye begins to degenerate, gradually sinks into the orbit, and is covered by an overgrowth of epidermis and connective tissue (Wilkens, 1988;Langecker et al, 1993;Jeffery and Martasian, 1998). Although a few optic nerve fibers are formed, there is a substantial reduction in the cavefish optic tectum (Soares et al, 2004). Thus, vision does not develop, and cavefish instead rely on other senses, including the lateral line (Teyke, 1990;Montgomery et al, 2001), the gustatory system (Schemmel, 1967) and possibly olfaction (Yamamoto et al, 2003), to survive in the dark cave environment.…”

Diversity of Brain Morphology in Teleosts: Brain and Ecological Niche

“…The restored eye exhibited well-organized layers of the retina. More recent experiments by Soares et al [2004] demonstrated that unilateral transplantation of the embryonic surface fish lens into the cavefish optic cup increases the size of the optic nerve and the volume of the optic tectum connected to the restored eye in adults.…”