The changing distribution of neurons in the inner nuclear layer from metamorphosis to adult: a morphometric analysis of the anuran retina

Abstract

The generation and changing distribution of neurons of the inner nuclear layer (INL) in the retina of two anuran species, Bufo marinus and Xenopus laevis, were studied from metamorphosis to adult. Morphometric studies were undertaken at six developmental stages in Bufo and four in Xenopus. The number and thickness of neurons in the INL were established in 29 predetermined retinal locations from serial sections of the eyes cut vertically or horizontally. The total number of neurons in the INL increased from metamorphosis to adult from 826,000 +/- 185 to 18,760,000 +/- 562 (mean +/- SD) in Bufo and from 308,000 +/- 25 to 877,000 +/- 31 in Xenopus. Over the same period the surface area of the INL increased about 50-fold from 2 mm2 to 96 mm2 in Bufo and 5-fold from 2.5 mm2 to 13 mm2 in Xenopus. In Bufo the difference between the highest cell number (central-temporal retina) and the lowest cell number in a sample area (dorsal and ventral peripheral retina) was 2.1:1 at metamorphosis. This ratio increased to 3.4:1 in the adult. Both the cell number and cell density per sample area in the INL was found to be higher along the nasotemporal meridian of the eye overlying the visual streak of the ganglion cell layer (GCL) of the retina. The retinal distribution of neurons in the INL did not change significantly during postmetamorphic growth in Xenopus. At metamorphosis a 1.7:1 difference was found between the highest neuron number (retinal ciliary margin) and lowest neuron number (retinal centre) decreasing to 1.5:1 in the adult. Retinae were labelled with 3H-thymidine in 15 mm Bufos and examined 2, 6, 12 and 18 weeks later. Higher rates of cell addition to the nasal and temporal poles of the INL were found compared with that at the dorsal and ventral poles. The retinal radial growth at the ciliary margin of the dorsal, ventral, nasal and temporal poles between the time of isotope injection and 18 weeks survival was found to be uneven; more radial elongation occurred at the nasal, dorsal and ventral poles and less at the temporal pole. These observations suggest that (a) the neuron distribution of the INL in adult animals approximates that of the GCL and (b) the visual streak-like area of the INL in Bufo develops by a sustained differential cell addition at the temporal and nasal poles of the retina.

NADPH-diaphorase positive neurons in the retina of Bufo marinus: Selective staining of bipolar and amacrine cells.

“…The estimated number of 233,000 NADPHd positive bipolar cells, therefore, represents a sizable population but a small percentage of the total numbers of all bipolars in the Bufo marinus retina. The retinal distribution NADPHd positive bipolar cells follows the general cell density profile established for all layers of the adult retina (ZHANG and STRAZNICKY, 1991), in particular the centre to periphery density slope of 3.1:1 of the INL reported recently (ZHU et al, 1990).…”

“…The morphology of the NADPHd positive bipolar cells appear to be very similar across the retina, thus we regard them to be a homogenous population. Recently we have estimated the numbers of neurons in the INL of the retina in adult Bufo marinus to be about 10 million (ZHU et al, 1990). If 30% of these cells were considered as bipolars, the number of them may reach at least to 3 millions.…”

Morphology and retinal distribution of tyrosine hydroxylase-like immunoreactive amacrine cells in the retina of developingXenopus laevis

“…Our present results confirm previous reports of the presence of TH-IR wide-field ACs with bistratified dendritic arbor in the retinae of a number of vertebrate species: fish (Teranishi and Negishi 1988), anura (Humphrey and Beazley 1989;Zhu and Straznicky 1990 a), reptiles (Kolb et al 1987) and mammals (Brecha et al 1984;Mitrofanis et al 1988). We report in this study that these cells are present in the retina from early larval stages, and that they are generated until adult.…”

“…The distribution of neurons in the ganglion cell layer (GCL) and in the inner nuclear layer (INL) of the Xenopus retina has been shown to change during development, with a reduction in cell density (Dunlop and Beazley 1984;Zhu et al 1990). These observations indicate that passive retinal expansion contributes substantially to retinal areal growth, in particular following the decrease in cell generation at the ciliary margin after metamorphosis.…”

Neuropeptide Y-Immunoreactive Neurons in the Retina of Two Australian Lizards.

“…NPY-immunoreactive amacrine cells in the INL of Pogona and Varanus were distributed non-uniformly, with a higher density corresponding to the visual streak of the GCL than in the peripheral retina. However, as in the anuran retina (ZHU et al, 1990;HlscocK and STRAZNICKY, 1989), the non-uniform distribution of NPY-immunoreactive amacrine cells in the lizard retina is likely to be of a lower gradient than that of all cells of the INL. In the INL of the Bufo marinus retina, a gradient of 3 :1 between cells of central and peripheral retina occurs whilst NPY-immunoreactive amacrine cells are evenly distributed.…”