Dendritic distribution of two populations of ganglion cells and the retinopetal fibers in the retina of the silver lamprey (Ichthyomyzon unicuspis)

Abstract

The distribution of ganglion cells in the retina of the silver lamprey, Ichthyomyzon unicuspis, was revealed by retrograde labeling from the optic nerve with horseradish peroxidase (HRP) and fluorescent-labeled dextrans in live animals and with the fluorescent dye Dil in aldehyde-fixed tissue. The majority of ganglion cells (74%) termed the "outer ganglion cells," are multipolar and are located at the vitread boundary of the inner nuclear layer. The remaining ganglion cells (26%), termed the "inner ganglion cells" are bipolar and are distributed in a sublamina within the inner plexiform layer. The dense, dendritic meshwork of the outer ganglion cells is largely restricted to the sclerad half of the inner plexiform layer with some cells possessing dendrites which pass through the inner nuclear layer to terminate within the outer plexiform layer. The dendrites of the inner ganglion cells form a thin, dendritic network apposing the inner limiting membrane. Axons from both populations of ganglion cells originate from dendrites or the soma and form fascicles lying adjacent to the outer ganglion cell somata.Retinopetal fibers, originating from bilaterally distributed neurons of the tegmental midbrain, were thin and varicose and ran parallel to the ganglion cell axons to terminate either with a varicose enlargement or a few short sidebranches in the sclerad third of the inner plexiform layer. The unusual organization of the lamprey retina and outgroup comparison with hagfish suggests that agnathans share a presumably primitive type of retinal ganglion cell organization compared to that of gnathostomes.

The Ocular Morphology of the Southern Hemisphere Lamprey <i>Mordacia mordax</i> Richardson with Special Reference to a Single Class of Photoreceptor and a Retinal Tapetum

“…Although not confirmed by retrograde labeling from the optic nerve, the presence of two ganglion cell sublaminae is indicated by tracing the path of the nerve fiber layer at the level of the optic nerve head in 1 µm resin sections stained with toluidine blue . The nerve fiber layer is located at the border of the inner plexiform and inner nuclear layers rather than along the inner limiting membrane as is found in gnathostome vertebrates [Fritzsch and Collin, 1990]. The substratum restricted to the middle region of the inner plexiform layer found in the retina of Geotria australis was not observed.…”

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

“…The lamprey's camera-like eye has a lens, an iris and extra-ocular muscles (five of them, unlike the eyes of jawed vertebrates, which have six), although it lacks intra-ocular muscles 11 . Its retina also has a structure very similar to that of the retinas of other vertebrates, with three nuclear layers comprised of the cell bodies of photoreceptors and bipolar, horizontal, amacrine and ganglion cells 36,37 . The southern hemisphere lamprey, Geotria australis, possesses five morphological classes of retinal photoreceptor and five classes of opsin, each of which is closely related to the opsins of jawed vertebrates 38 (see below).…”

“…Biplexiform ganglion cells are a class of retinal projection neuron that seem to exist in all vertebrate species from lamprey to primate 37,[130][131][132][133] , and which receive synaptic input from photoreceptors as well as from bipolar cells. In addition, the lamprey has a class of ganglion cell that might contact only photoreceptors 132 .…”

“…The lamprey retina is also interesting in that the majority of ganglion cells (and nerve fibres) lie distal to, rather than proximal to, the IPL (see figure 7 of REF. 37). This might represent the primordial layering arrangement of the vertebrate retina, in which case an inversion of layers through altered patterns of radial migration might have occurred in the gnathostome retina.…”

Why rods and cones?

“…The lamprey retina has a three-layered structure closely resembling that in gnathostomes, 31 and lamprey photoreceptors utilise the same five classes of visual opsin as used by gnathostomes. 32 One class of lamprey photoreceptor expresses rhodopsin and exhibits comparable sensitivity to gnathostome rods, 33,34 despite exhibiting cone-like morphology.…”