Somatic and Dendritic Mosaics Formed by Large Ganglion Cells in the Retina of the Common House Gecko <i>(Hemidactylus frenatus)</i>

Abstract

Recent studies of large ganglion cells in fishes and frogs have identified a shared inventory of three basic types, with characteristic forms and spatially independent mosaic distributions. These anamniote types and mosaics are hard to match to the large ganglion cell types and mosaics of mammals, implying that the underlying developmental programmes have diverged during evolution. Reptiles and mammals both belong to the amniote lineage, so the point of divergence can be investigated by comparing the large ganglion cells of reptiles with those of mammals, taking fishes and frogs as outgroups. With this aim, ganglion cells of the common house gecko, Hemidactylus frenatus, were labelled with horseradish peroxidase by an in vitro method and studied in retinal flatmounts. Two prominent, regular, spatially independent mosaics were consistently present. One (α_a) was characterized by somata displaced into the inner nuclear layer and dendrites forming planar trees in sublamina a; the other (α_ab) comprised large orthotopic somata and distinctive, bistratified dendrites that formed discrete planar subtrees in sublaminae a and b. These subtrees were joined by up to 40 vertical link segments, whose distribution was found to correlate with the underlying photoreceptor mosaic. Some specimens also contained patches of a third mosaic (α_c), characterized by large orthotopic somata and very large flat trees in sublamina c, but the labelling of this type was inconsistent. These reptilian mosaics share several distinctive characters with anamniote α-cell mosaics but differ markedly from the ganglion cell mosaics of any known mammal. The most parsimonious conclusion is that those mosaic features that are shared by the ganglion cells of all nonmammals are homologous and primitive (symplesiomorphic), while those that are shared by all therian mammals are homologous and derived (synapomorphic). This is consistent with other differences between mammalian and nonmammalian eyes. Mosaic formation itself, however, seems to be a universal characteristic of large ganglion cells.

Retinal ganglion cells in the Pacific redfin, Tribolodon brandtii dybowski, 1872: Morphology and diversity

“…In the present case, the pattern of GC labeling was patchy, preventing analysis of the spatial arrangement of cells assigned to different types. However, the relative dendritic field size, pattern of dendrite course, and stratification of type 1 and 2 cells are similar to their counterparts in other nonmammalian species (often named α a and α c , respectively), supporting the hypothesis of symplesiomorphy and the potential homology of large GCs in nonmammals (Cook and Noden, ).…”

Structure and diversity of retinal ganglion cells in steller's sculpin Myoxocephalus stelleri tilesius, 1811

“…All three types are arranged as regular mosaics spatially independent from each other, providing strong evidence for their being natural GC types (Cook et al, ; Cook, ). Cell types similar to α a , α c , and biplexiform cells are also found in nonmammalian species (e.g., Cook and Noden, ; Pushchin and Karetin, ). Their presence in the Steller's sculpin supports the hypothesis of the symplesiomorphy and potential homology of large GCs in nonmammals (Cook et al, ).…”

“…The major drawback of the present approach is that it cannot distinguish between cell similarity due to shared ancestry (homology) and that due to structural and functional convergence or parallelism. Like nearly all neuronal classification schemes to date, therefore, this approach is “Linnaean” (Cook, ), taking into account only observed similarities. To circumvent this limitation, studies comparing the differentiation and gene‐expression histories of specific cell types and their ontogenetic lineage relationships in different species could be used to disconfirm hypotheses of homology, and the embryonic lineages themselves could be used as additional characters for cladistic ("Darwinian") classification.…”

“…Identifying homologous neuron types in related species is essential for understanding the evolution of nervous structures. It has been taken for granted that neuronal types should be discovered and not defined (Cook, ). It would be advantageous to classify nerve cells using a wide variety of characteristics related to their structure, physiology, and development.…”

Changes in Somal Growth and Dendritic Patterns of the Retinal Ganglion Cells in the Chicks and Chick Embryos

“…Sci. 65(10): 1135-1137, 2003 On the basis of several morphological features such as the size and shape of soma, dendritic branching pattern, stratification of dendrites, axon caliber, and central projections, the classification of the mature retinal ganglion cells (RGCs) was attempted in the various vertebrates, mammals [1,2,6,12,13,16], birds [4,11,17], reptiles [9], amphibians [14], and fish [7]. However, little is known about when and how the RGCs achieved their characteristic features during development.…”