Ganglion cells of a short-wavelength-sensitive cone pathway in New World monkeys: morphology and physiology.

We have studied the morphology and physiology of retinal ganglion cells of a short-wavelength-sensitive cone (SWS-cone) pathway in dichromatic and trichromatic New World anthropoids, the capuchin monkey (Cebus apella) and tufted-ear marmoset (Callithrix jacchus). In Old World anthropoids, in which males and females are both trichromats, blue-ON/yellow-OFF retinal ganglion cells have excitatory SWS-cone and inhibitory middle- and long-wavelength-sensitive (MWS- and LWS-) cone inputs, and have been anatomically identified as small-field bistratified ganglion cells (SB-cells) (Dacey & Lee, 1994). Among retinal ganglion cells of New World monkeys, we find SB-cells which have very similar morphology to such cells in macaque and human; for example, the inner dendritic tree is larger and denser than the outer dendritic tree. We also find blue-on retinal ganglion cells of the capuchin to have physiological responses strongly resembling such cells of the macaque monkey retina; for example, responses were more sustained, with a gentler low frequency roll-off than MC-cells, and no evidence of contrast gain control. There was no difference between dichromatic and trichromatic individuals. The results support the view that SWS-cone pathways are similarly organized in New and Old World primates, consistent with the hypothesis that these pathways form a phylogenetically ancient color system.

Post-receptoral mechanisms of colour vision in New World primates.

Diurnal platyrrhines, both di- and trichromats, have magnocellular (M-) and parvocellular (P-) retinal ganglion cells which are morphologically very similar to those found in catarrhines. Catarrhine central P ganglion cells contact single midget bipolar cells, which contact single cones. Physiological recordings of retinal ganglion cells of dichromatic Cebus monkeys showed very similar cell properties to the catarrhine macaque, except that P ganglion cells lacked colour-opponency. We describe the presence of single-headed midget bipolar cells in the Cebus retina. These midget bipolar cells have axon terminal sizes in the same range as the dendritic tree sizes of P ganglion cells as far as 2 mm of retinal eccentricity. This result supports the view that, as in catarrhines, central P ganglion cells of platyrrhines receive input from single midget bipolar cells which in turn, receive input from single cones. This finding is consistent with the idea that a P pathway with one-to-one connectivity was present in the anthropoid ancestor before the divergence between catarrhines and platyrrhines.

Parallel pathways in the retina of Old and New World primates.

Old-world simians are all trichromats, but in most new-world primates there is a polymorphism; males are dichromats but most females are trichromats. In the old world simian, luminance and red-green chromatic channels defined by psychophysical experiments have as a basis parasol ganglion cells of the magnocellular (MC) pathway and midget ganglion cells of the parvocellular (PC) pathway respectively. Small bistratified ganglion cells provide a basis for a blue-yellow chromatic channel, which should probably be considered a separate entity. In both dichromatic and trichromatic new-world animals, the MC pathway and the small bistratified, blue-yellow system seem anatomically and physiologically similar to those in their old-world relatives. The midget ganglion cells of the parvocellular pathway in trichromats are anatomically and physiologically similar to the old-world pattern. In dichromatic animals, they are anatomically similar and physiologically resemble those of trichromatic animals, except for the lack of chromatic opponency. We conclude that these three systems may from a basic pattern for the visual pathway of primates. However, the results from dichromats indicate that the evolution of trichromacy may be found to be more complex than presently supposed.

The retinal ganglion cell classes of New World primates.

In the primate retina there are distinct ganglion cell classes, exhibiting particular morphologies and central projections, each responsible for conveying particular types of visual information to the brain. The chief retinal inputs to the cortex arise from specific ganglion cell classes, M-ganglion cells, responsible for carrying the luminance signal, and P-ganglion cells, that convey the red-green color opponent signal, as well as high contrast luminance signal. There are other ganglion cell classes, such as small-field bistratified cells, exhibiting dendrites that stratify at two different levels in the inner plexiform layer, which convey the blue-yellow color opponent signal. Most published data concerning primate retinal ganglion cell anatomy and physiology have been obtained from Old World species. Studies on New World monkeys have recently become of interest since they differ from the Old World monkeys with respect to the color vision inheritance pattern. On reviewing retinal ganglion cell layer organization in New World monkeys, it seems that there are more similarities than differences in relation to the Old World monkeys. Diurnal genera of New World monkeys exhibit a well-developed fovea centralis and ganglion cell density peak, as well as peripheral density values which are in the range reported for Old World monkeys and human. Moreover, all the major ganglion cell classes identified in Old World monkeys are also present in New World primates. Up to now, no obvious anatomical differences between dichromats and trichromats have been reported. The only genus that is significantly different from the others is the Aotus. It exhibits lower ganglion cell density in the central retina, and apparently lacks the small-field bistratified cells.