Developmental variation in the structure of the retina

Abstract

Events traditionally called "developmental errors" are known to occur in both vertebrate and invertebrate nervous systems. This study was concerned with the frequency and mode of generation of such events in the mammalian retina. We studied three anomalous structures observed in the rabbit's retina after staining of the cell populations that accumulate indoleamines: type 3 cells, stray processes in the optic fiber layer, and displaced cells. They were counted in rabbit retinas prepared as whole-mounts, and in most cases topological maps were made. For comparison, the conventional indoleamine-accumulating amacrine cells and the tyrosine hydroxylase (TH)-positive cells, which are members of the mammalian retina's recognized complement of amacrine cells, were also counted. A further comparison was made with the number and distribution of TH-positive amacrine cells in highly inbred mice. The ordinary amacrine cells did not vary much in number from animal to animal. Especially in inbred mice, the reproducibility was striking: the extreme variation in number of TH amacrine cells between any two of the 14 retinas studied was 22%, and the mean difference between two eyes of individual mice was 2.5 ± 1.7%. The three anomalous structures were rare and variable. Their numbers varied more than fourfold from animal to animal. However, their numbers in two eyes from the same animal varied by an overall average of only 14 ± 10%. The anomalous structures were present in all rabbits, and their morphology was the same in all cases: they are under precise control by the developmental program. The anomalous cells share many phenotypic features with the regular amacrine cells of the indoleamine-accumulating class. They thus appear to be the result of minor variations in the developmental control program, such that the final shape of the cell is anomalous but most other features remain the same. It appears that slight variations in the program of neuronal development can create new neuronal structures that are both intricate and highly reproducible. Copyright © 1993 Society for Neuroscience.