Colour vision in primates is mediated by cone opponent ganglion cells in the retina, whose axons project to the dorsal lateral geniculate nucleus in the visual thalamus. It has long been assumed that cone opponent ganglion cells project to the parvocellular layers of the geniculate. Here, we examine the role of a third subdivision of the geniculocortical pathway: the interlaminar or koniocellular geniculate relay cells. We made extracellular recordings in the dorsal lateral geniculate nucleus of the common marmoset Callithrix jacchus, a New World monkey in which the interlaminar cells are well segregated from the parvocellular layers. We found that one group of colour opponent cells, the blue-on cells, was largely segregated to the interlaminar zone. This segregation was common to dichromatic ('red-green colour-blind') and trichromatic marmosets. The result calls into question the traditional notion that all colour information passes through the parvocellular division of the retino-geniculo-cortical pathway in primates.

The lateral geniculate nucleus (LGN) in humans and Old-World monkeys is dominated by the representation of the fovea in the parvocellular (PC) layers, and most PC cells in the foveal representation have red-green cone opponent receptive field properties. It is not known whether these features are both unique to trichromatic primates. Here we measured receptive field properties and the visuotopic organization of cells in the LGN of a New-World monkey, the marmoset Callithrix jacchus. The marmoset displays a polymorphism of cone opsins in the medium-long wavelength (ML) range, which allows the LGN of dichromatic ("red-green color blind") and trichromatic individuals to be compared. Furthermore, the koniocellular-interlaminar layers are segregated from the main PC layers in marmoset, allowing the functional role of this subdivision of the LGN to be assessed. We show that the representation of the visual field in the LGN is quantitatively similar in dichromatic and trichromatic marmosets and is similar to that reported for macaque; the vast majority of LGN volume is devoted to the central visual field. ON- and OFF-type responses are partially segregated in the PC layers so that responses are more commonly encountered near the external border of each layer. The red-green (ML) opponent cells in trichromatic animals were all located in the PC layers, and their receptive fields were within 16 degrees of the fovea. The koniocellular zone between the PC and magnocellular layers contained cells that receive excitatory input from short wavelength sensitive cones ("blue- cells") as well as other nonopponent cells. These results suggest that the basic organization of the LGN is common to dichromatic and trichromatic primates and provide further evidence that ML and SWS opponent signals are carried in distinct subdivisions of the retinogeniculocortical pathway.

We studied the morphology of retinal ganglion cells in a diurnal New World primate, the marmoset Callithrix jacchus. This species is of interest as a model for primate vision because it has good behavioural visual acuity, and the retina and subcortical visual pathways are very similar to those of Old World monkeys and humans. Ganglion cells were labelled by placing small crystals of the carbocyanin dye DiI into the optic fibre layer, or by intracellular injection of neurobiotin. Two main classes of ganglion cell were labelled. We call these Group A cells and Group B cells: they are respectively homologous to parasol and midget cell classes. Group A and Group B cells show similar patterns of dye coupling, dendritic stratification and dendritic field size as their counterparts in Old World monkeys and humans. A third group of cells, which we call Group C, is morphologically heterogeneous. Examples corresponding to wide-field ganglion cell types described in Old World primates were encountered. One subgroup of C cells has a morphology very similar to that of the small bistratified (blue-on) cell described in macaque retina, suggesting that this functional pathway is common to all primates. As for other New World monkeys, the marmoset shows a sex-linked polymorphism of cone pigment expression, such that all males are dichromats and the majority of females are trichromats. No systematic differences in Group B cells were seen between male and female retinas, suggesting that trichromacy is not accompanied by specific changes in ganglion cell morphology.

We have investigated the time course and magnitude of cellular degeneration in the ganglion cell layer and the presumptive amacrine and bipolar regions of the inner nuclear layer during the development of the retina in the rat. Pyknotic profiles are present in the ganglion cell layer during the first 2 postnatal weeks, reaching peak numbers during the first 4 postnatal days (corresponding to the time of greatest loss of ganglion cells and their axons: Potts et al., '82; Lam et al., '82; Perry et al., '83). Two observations suggest that the majority of pyknotic profiles present in the ganglion cell layer during the second postnatal week are not ganglion cells. First, following injection of kainic acid into one superior colliculus, degenerating ganglion cells in the contralateral retina are cleared within 24-48 hours. Therefore, since most ganglion cell and axon loss occurs within the first postnatal week, few of the pyknotic profiles present in the second week are likely to be ganglion cells. Second, the time course of cellular degeneration in the ganglion cell layer during the second postnatal week follows a very similar pattern to that seen in the presumptive amacrine sublayer of the inner nuclear layer. Such a correspondence suggests that two phases of cell death occur in the ganglion cell layer: during the first postnatal week the majority of dying cells are ganglion cells, and in the second, most cell death is due to a loss of displaced amacrine cells. In the inner nuclear layer pyknotic profiles are most numerous in the presumptive amacrine region on postnatal days 6 and 7, and in the presumptive bipolar region on day 10. Synaptogenesis in the inner plexiform layer occurs later but reflects the order of cell death. Thus, conventional (presumed amacrine) synapses were first observed on day 11 and synaptic ribbons (indicative of bipolar synapses) on day 13. These observations suggest that amacrine and bipolar cells initiate synapses only after their numbers have stabilized.

Class I retinal ganglion cells have been identified in wholemounts of rat retinae following injections of horseradish peroxidase (HRP) into retino-recipient nuclei. Class I cells are characterized by relatively large somata, 3–7 fairly frequently branching large-gauge primary dendrites and relatively thick axons. Cells with a very similar morphology have been visualized in the ganglion cell layer of retinal wholemounts using a neurofibrillar stain. The size of the somata and dendritic trees of Class I cells is affected by the density of all classes of ganglion cells: both somata and dendritic trees of Class I cells located in the region of peak density are smaller than those located in medium- and low-density ganglion cell regions. The mean numbers of Class I ganglion cells labelled following massive injections of HRP into retino-recipient nuclei were 876 (in albino rats) and 944 (in hooded rats), while the mean number of cells stained with the neurofibrillar method in albino retinae was 791. Thus, with the total number of positively identified retinal ganglion cells being 110,000–115,000 [Potts eta.1, 1982; Perry et al., 1983], Class I cells in both strains of rat constitute less than 1 % of all retinal ganglion cells. Nevertheless the dendritic fields of Class I cells cover the entire retina. Although Class I cells are distributed relatively evenly across the retina, the density is slightly greater in the lower temporal retina where the bulk of the ipsilaterally projecting fibres originates. While Class I cells represent up to 10% of ipsilaterally projecting retinal ganglion cells in both strains of rat, fewer Class I cells project ipsilaterally in albinos than in hooded rats. All contralaterally projecting Class I cells appear to send branching axons to the superior colliculus and dorsal lateral geniculate nucleus. Class I cells represent a larger proportion of the ganglion cells projecting to the dorsal lateral geniculate nucleus (4–5%) than that of ganglion cells projecting to the superior colliculus (about 1 %). The morphology, numbers, distribution and the pattern of the central projections of Class I retinal ganglion cells in rats suggest that they are likely to be homologues of the alpha-type ganglion cells distinguished in carnivores.