The Smooth Monostratified Ganglion Cell: Evidence for Spatial Diversity in the Y-Cell Pathway to the Lateral Geniculate Nucleus and Superior Colliculus in the Macaque Monkey

Abstract

In the primate visual system approximately 20 morphologically distinct pathways originate from retinal ganglion cells and project in parallel to the lateral geniculate nucleus (LGN) and/or the superior colliculus. Understanding of the properties of these pathways and the significance of such extreme early pathway diversity for later visual processing is limited. In a companion study we found that the magnocellular LGN-projecting parasol ganglion cells also projected to the superior colliculus and showed Y-cell receptive field structure supporting the hypothesis that the parasol cells are analogous to the well studied alpha-Y cell of the cat's retina. We here identify a novel ganglion cell class, the smooth monostratified cells, that share many properties with the parasol cells. Smooth cells were retrogradely stained from tracer injections made into either the LGN or superior colliculus and formed inner-ON and outer-OFF populations with narrowly monostratified dendritic trees that surprisingly appeared to perfectly costratify with the dendrites of parasol cells. Also like parasol cells, smooth cells summed input from L-and M-cones, lacked measurable S-cone input, showed high spike discharge rates, high contrast and temporal sensitivity, and a Y-cell type nonlinear spatial summation. Smooth cells were distinguished from parasol cells however by smaller cell body and axon diameters but ϳ2 times larger dendritic tree and receptive field diameters that formed a regular but lower density mosaic organization. We suggest that the smooth and parasol populations may sample a common presynaptic circuitry but give rise to distinct, parallel achromatic spatial channels in the primate retinogeniculate pathway.

Linear and Nonlinear Contributions to the Visual Sensitivity of Neurons in Primate Lateral Geniculate Nucleus

“…All P-and M-cells show receptive fields of the center-surround type and can be reasonably well characterized by linear models Kaplan 1997a,b, 1999;: each neuron responds as if it computes a weighted sum of the intensity of the pattern imaged on its receptive field. Deviations from linearity are most clearly evident in M-cells, all of which exhibit contrast gain controls (Benardete et al 1992;Kaplan and Shapley 1986;Solomon et al 2002) and some of which show more severe nonlinearities (Crook et al 2008b;Kaplan and Shapley 1982;Petrusca et al 2007;Solomon et al 2006). Despite these functional differences, the responses of P-and M-cells to achromatic images often appear redundant (Levitt et al 2001;van Hateren et al 2002).…”

The Primate Retina Contains Distinct Types of Y-Like Ganglion Cells: Figure 1.

“…For example, in the cat retina, "nonlinear W-cells" display frequency doubling and have wide dendritic fields but are distinguished from Y-cells by their smaller somas and thinner axons (Stone, 1983;Crook et al, 2008a). The primate retina also possesses a second Y-like RGC, the smooth monostratified (SM) cell (Crook et al, 2008b). SM cells, which may be the primate "upsilon cell" identified by Petrusca et al (2007), can be distinguished from parasol cells morphologically (Crook et al, 2008b).…”

“…The primate retina also possesses a second Y-like RGC, the smooth monostratified (SM) cell (Crook et al, 2008b). SM cells, which may be the primate "upsilon cell" identified by Petrusca et al (2007), can be distinguished from parasol cells morphologically (Crook et al, 2008b). The dendritic fields of SM cells are more sparsely branched and approximately two times wider than those of parasol cells.…”

“…SM cell somas are also slightly smaller and their axons approximately half as wide. Anatomically, SM cells project to both the LGN and the superior colliculus (Crook et al, 2008b). Although morphologically different, SM and parasol cell dendritic fields are precisely costratified, suggesting that they may share a common input.…”

“…In addition, W-cells in the cat tend to have narrower dendritic fields than Y-cells, but SM cells in the primate have wider dendritic fields than parasol cells (Stone, 1983;Crook et al, 2008a,b). Cat Y-cells and primate SM cells also represent more similar percentages of the total number of RGCs (each ϳ3%), whereas parasol cells represent a larger percentage (ϳ8%) (Wässle et al, 1975;Crook et al, 2008b). To establish homology more conclusively, it may be necessary to first develop molecular markers specific to retinal ganglion Y-cells.…”