Neural differentiation in the retina of the larval sea lamprey (Petromyzon marinus)

Abstract

The peripheral retina of the sea lamprey develops in a 5-year-long process in which only certain neurons differentiate each year. The growth of cell layers, the differentiation of the neurons, and the morphology of their dendrites and axons were studied with normal, HRP, and Golgi preparations. Ganglion cells are differentiated in 3-year-old larvae, amacrine and horizontal cells in 4-year-old larvae, photoreceptor cells in stage I transformers, and bipolar cells in stage III transformers. Each new development is expressed as a radial gradient of differentiation. As a result of this protracted and stepped process, lamprey retinal neurons, particularly ganglion cells, differentiate in the absence of other cells to which they will ultimately be connected and may express their individual genetic programs more fully than in other vertebrate retinas. This could account for the unusual relationship of the ganglion cell, inner plexiform, and optic nerve layers and for the very high ratio of displaced to orthotopic ganglion cells.

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

“…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 Ocular Morphology of the Southern Hemisphere Lamprey Geotria australis Gray, with Special Reference to Optical Specialisations and the Characterisation and Phylogeny of Photoreceptor Types

“…In G. australis, the ganglion cells are distributed within three discrete layers, namely along the inner limiting membrane, in the middle of the inner plexiform layer and in the inner nuclear layer. The presence of three ganglion cell sublaminae has also been noted in the adult stages of G. australis by , a situation that contrasts with the presence of only two sublaminae in the silver lamprey Ichthyomyzon unicuspis [Fritzsch and Collin, 1990], the sea lamprey Petromyzon marinus [Rubinson and Cain, 1989] and in Mordacia mordax, another southern hemisphere lamprey [S.P. Collin and I.C.…”

“…Although numerous studies have been carried out on the eyes of holarctic lampreys [Dickson and Graves, 1981;Rovainen, 1982;Rubinson and Cain, 1989;DeMiguel et al, 1989;Fritzsch and Collin, 1990;Collin and Fritzsch, 1993], there have been no detailed investigations of the eye of either of the families of southern hemisphere lampreys. Indeed, information on the adult eye of G. australis is restricted to a short, light microscopical description and illustration of the retinal photoreceptors by Walls [1942] and to the brief account of its histological and ultrastructural characteristics by .…”

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.…”