Large retinal ganglion cells in the pipid frog Xenopus laevis form independent, regular mosaics resembling those of teleost fishes

Abstract

Population-based studies of retinal neurons have helped to reveal their natural types in mammals and teleost fishes. In this, the first such study in a frog, labeled ganglion cells of the mesobatrachian Xenopus laevis were examined in flatmounts. Cells with large somata and thick dendrites could be divided into three mosaic-forming types, each with its own characteristic stratification pattern. These are named a a , a ab , and a Q , following a scheme recently used for teleosts. Cells of the a a mosaic (-0.4% of all ganglion cells) had very large somata and trees, arborizing diffusely within sublamina a (the most sclerad). Their distal dendrites were sparsely branched but achieved consistent coverage by intersecting those of their neighbors. Displaced and orthotopic cells belonged to the same mosaic, as did cells with symmetric and asymmetric trees. Cells of the a ab mosaic (-1.2%) had large somata, somewhat smaller trees that appeared bistratified at low magnification, and dendrites that branched extensively. Their distal dendrites arborized throughout sublamina b and the vitread part of a, tessellating with their neighbors. All were orthotopic; most were symmetric. Cells of the a c mosaic (-0.5%) had large somata and very large, sparse, flat, overlapping trees, predominantly in sublamina c. All were orthotopic; some were asymmetric. Nearest-neighbor analyses and spatial correlograms confirmed that each mosaic was regular and independent, and that spacings were reduced in juvenile frogs. Densities, proportions, sizes, and mosaic statistics are tabulated for all three types, which are compared with types defined previously by size and symmetry in Xenopus and potentially homologous mosaic-forming types in teleosts. Our results reveal strong organizational similarities between the large ganglion cells of teleosts and frogs. They also demonstrate the value of introducing mosaic analysis at an early stage to help identify characters that are useful markers for natural types and that distinguish between within-type and between-type variation in neuronal populations.

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

“…In this retina, the α ab population represented 1.03% of the estimated total number of ganglion cells (table 1), fairly close to the proportion in Xenopus laevis (1.21%) [Shamim et al, 1997] ). The somata were always orthotopic and generally polygonal, this shape being set by the presence of several primary dendrites in a single plane around the perimeter (fig.…”

“…IPL depths: F = 87%, G = 67%, H = 29%, I = 19%, Scale bar = 50 µm. these sample retinae were taken, the α a population represented 0.38% of the estimated total number of ganglion cells (table 1), close to the proportion of α a cells in Xenopus laevis (0.37%) [Shamim et al, 1997] The somata of the α ab ganglion cells were all orthotopic. They were larger than those of the α a cells and less uniform in shape, generally appearing either ovoid ( fig.…”

“…Although these are the first ganglion cells to be studied by populationbased methods in a reptile, they share many features with mosaics that have been studied in this way in anamniotes. As many aspects of mosaic structure, function, evolution and development that are relevant to these gecko mosaics have been discussed elsewhere [Cook and Becker, 1991;Cook et al, 1992;Cook and Sharma, 1995;Shamim et al, 1997], only four new issues need be addressed under the following headings.…”

“…Mosaics are useful practical aids in the definition of neuronal types [mammals -Peichl, 1991;nonmammals -Cook and Becker, 1991;Shamim et al, 1997]. All the members of one mosaic are viewed as putative members of one natural type as defined by Rodieck and Brening [1983], sharing a common main function without necessarily being uniform in all respects [Rowe and Stone, 1980;Cook et al, 1992;Cook and Sharma, 1995].…”

“…In six well separated families of bony fishes and aquatic or terrestrial frogs, population-based studies have revealed what seems to be an 'anamniote consensus pattern' of three large ganglion cell mosaics, termed α a , α b /α ab and α c [Cook and Becker, 1991;Cook et al, 1992;Cook and Sharma, 1995;Shamim et al, 1997; K.M. Shamim, P. Tóth, F. Scalia and J.E.…”