Relationships between Müller cells and neurons in a primitive tetrapod, the Australian lungfish.

Abstract

We recently proposed a model of cytogenesis which assumes that primitive ancestral mammals and premammalian vertebrates had a retinal composition that consisted of about seven neurons per Müller cell, comprising 1-2 cone photoreceptors, 1-2 rod photoreceptors, 2-3 bipolar cells, 1-2 amacrine cells, less than 1 ganglion cell, and less than 1 horizontal cell (Reichenbach & Robinson, 1995). The Australian lungfish (Neoceratodus forsteri) closely resembles the lobe-finned ancestors of land vertebrates, and has an extremely plesiomorphic nervous system. The present study, therefore, has examined the relative frequencies of retinal neurons and Müller cells (identified by immunolabelling for glutamine synthetase) in the lungfish retina. It was found that for each Müller cell there is an average of 1.9 cone photoreceptors, 1.7 rod photoreceptors, 3.1 amacrine/bipolar/horizontal cells, and 0.6 ganglion cells; amounting to a ratio of 7.3 neurons per Müller cell. These results support our conjecture that the sequence of cytogenesis in mammals is constrained by a developmental program that predates the evolution of mammals. The study also provides the first detailed morphological descriptions of lungfish Müller cells and their relationship with adjacent neurons. It was found that individual Müller cells in lungfish have a volume (more than 12,000 microns3) that is an order of magnitude higher than in mammals, yet the proportion of total retinal volume occupied by these cells (20%) is very similar.