Morphology of P and M retinal ganglion cells of the bush baby

Abstract

P/midget ganglion cells mediate red-green color opponency in anthropoids. It has been proposed that these cells evolved as a specialization to subserve color vision in primates. If that is correct, they must have evolved about the same time as the long-wavelength ('red') and medium-wavelength ('green') pigment genes diverged, thirty million years ago. Strepsirhines are another group of primates that diverged from the ancestor of the anthropoids at least 55 million years ago. If P/midget ganglion cells evolved to subserve color vision, they should be absent in strepsirhines. We tested this hypothesis in a nocturnal strepsirhine, the greater bush baby Otolemur. The retinal ganglion cells were labeled with the lipophilic tracer Dil and the results show that bush babies have P/midget and M/parasol cells similar to those found in the peripheral retinas of anthropoids. A number of studies have shown that the P and M pathways of bush babies share many similarities with those of anthropoids, and our results show that the same is true for their retinal ganglion cells. These results support the hypothesis that the P system evolved prior to the emergence of red-green color opponency.

Fig. 1

A–C: DiI-labeled P ganglion cells of the bush baby retina in a whole-mount preparation; scale bar = 25 µm. A: dendritic trees of two ON-P cells at 0.6 mm temporal. B: an ON-P cell at 4 mm dorsal. C: an ON-P cell at 8 mm nasal. D: Patch of bush baby retina at 2.5 mm of eccentricity (temporal retina) with neighboring P (arrows) and M cells (MC); scale bar = 50 µm. All images are reconstructed stacks of confocal optical sections.

Fig. 2

Dendritic field (A) and soma (B) diameters of bush baby P cells (circles) and M cells (triangles) as a function of retinal eccentricity.

Fig. 3

Comparison between bush baby, owl monkey (Aotus), capuchin monkey (Cebus), marmoset (Callithrix) and cat retinal ganglion cells. A: Dendritic field area for primate P cells and cat β cells. B: Dendritic field area for primate M cells and cat α cells. Data for Cebus were replotted from Yamada et al. [38] and those for Aotus and Callithrix, from Yamada et al. [39]. Data for cat were from Boycott and Wässle [49] as replotted by Rodieck et al. [60]. Eccentricity is expressed in degrees of visual angle in order to normalize the retinal extent. For bush baby eccentricities, we used 140 µm/° as the conversion factor from linear to angular distance [41].