Retinal development in the lamprey (Petromyzon marinus L.): Premetamorphic ammocoete eye

Abstract

Development of the retina of the ammocoete begins early in embryogenesis, with the formation of the optic vesicle, but development of the rudimentary eye is suspended and remains arrested during larval life. Prior to the onset of metamorphosis, the retina of the ammocoete is completely undifferentiated, with the exception of a small area (Zone II) surrounding the optic nerve head, where all of the adult retinal layers are found. The photoreceptors in this area have developed to include synaptic contacts as well as inner and outer segments. The pigment epithelium in this area, too, has differentiated to include well-formed melanin granules, myeloid bodies and endoplasmic reticulum and is closely associated with the receptor cell outer segments. With the approach of metamorphosis, differentiation of the remainder of the retina (Zone I) begins, taking place in a radial fashion from the optic nerve head. Differentiating pigment epithelial cells adjacent to the differentiated retinal zone begin to accumulate melanin granules. In the neural retina, junctional complexes are established in the form of an external limiting membrane, and connecting cilia project into the optic ventricle. Photoreceptor differentiation begins with the formation of a mitochondria-filled ellipsoid within the inner segment. Development and differentiation of the ammocoete retina is unique to vertebrates in that only a small area of differentiated retina is present during the larval stage. The remainder of the retina differentiates and becomes functional during metamorphosis.

Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup

“…Lampreys have a larval form (the ammocoete) that develops slowly, over a period of 5 years or more, before metamorphosing into the adult 50 . The ammocoete is effectively blind, and its eyes are similar to those of the hagfish: they are small, they are buried beneath skin and they possess a relatively undifferentiated retina.…”

“…The ammocoete is effectively blind, and its eyes are similar to those of the hagfish: they are small, they are buried beneath skin and they possess a relatively undifferentiated retina. Although the ammocoete retina contains a narrow central region (~50 μm wide, adjacent to the optic nerve) that is differentiated into the conventional three layers of vertebrate retinal neurons, the bulk of the larval retina remains undifferentiated, with a thick neuroblastic layer [50][51][52][53] . Over a period of years, a slow process of neural differentiation occurs, in the following sequence: ganglion cells, amacrine and horizontal cells, photo-receptors and finally bipolar cells 51,52 .…”

“…-A highly organized three-layered neuronal structure with two intervening plexiform layers develops 50,51 .…”

The evolution of early vertebrate photoreceptors

“…The eyes of larval lampreys or ammocoetes are similar to those of hagfishes, i.e. are buried beneath the skin, where most of the retina is relatively undifferentiated and possesses a thick neuroblastic layer (Dickson & Collard 1979;Rubinson & Cain 1989;Rubinson 1990). Recent reviews by Lamb et al (2007) and Lamb (2009) suggest that lampreys inherited their eyes from an ancestor that they had in common with hagfish, and that this hagfish-like larval eye is present in the lamprey larva but transforms to a vertebratelike eye in the adult.…”

Localization of fibronectin, laminin-entactin, and entactin in Reichert's membrane by immunoelectron microscopy.

“…There is some evidence that it can act as a passive filter, excluding very large molecules such as thorotrast, and allowing the passage of others, such as ferritin (Jollie, 1968). During development, RM increases rapidly in thickness and surface area, before breaking down towards the end of gestation (Clark et at., 1975a;Jensh et at., 1977;Dickson, 1979). It therefore provides a useful model for studying the synthesis, assembly, and turnover of basement membrane components (Hogan and Cooper, 1982).…”