Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus, and parvicellular laminae of the lateral geniculate nucleus

Abstract

In common with other vertebrates, the primate retina contains a number of different ganglion cell types that project to different regions in the brain. We wanted to determine how the different ganglion cell types, distinguished morphologically, mapped to these regions of the brain. We injected a fluorescent dye into one of three regions of a macaque brain: the superior colliculus (SC), the pretectal region, and the parvicellular laminae of the lateral geniculate nucleus. By means of an in vitro preparation, the retrogradely labelled ganglion cells were intracellularly injected with horseradish peroxidase, so as to reveal their dendritic morphology. When the dendritic-field diameters of the injected cells were plotted against retinal eccentricity, each of the three regions was found to receive input from a distinctive population of cells. The pretectal projection was dominated by cells with large dendritic fields. The SC projection was composed of a number of distinct types, with smaller dendritic fields. Parasol cells project to SC but are extremely rare. In addition to midget ganglion cells, the parvicellular laminae receive inputs from at least two additional groups. Parvicellular bistratified (PB) cells have bistratified dendritic fields, slightly larger than those of parasol cells. Parvicellular giant (PG) cells have dendritic-field diameters larger than that of any parasol cell, ranging from 250 microns to greater than 850 microns--the largest of any primate ganglion cells. In contrast to the retinal projections of the cat, in which a specific ganglion cell type can project to different regions of the brain, each of the regions in this survey appears to receive inputs from its own distinct group of ganglion cells.

Identification and Characterization of a Y-Like Primate Retinal Ganglion Cell Type

“…Based on the measured upsilon cell properties, we can speculate as to which morphological RGC type (Rodieck and Watanabe, 1993;Dacey et al, , 2005Dacey, 2004;Yamada et al, 2005) they may correspond to. Because the upsilon cells are OFF-type cells with no evidence for ON-OFF responses (i.e., no significant responses to both light intensity increments and decrements) (Fig.…”

“…Although decades of work have been devoted to the study of primate retinal architecture, fewer than one-half of the 22 or more anatomically identified types of retinal ganglion cells (RGCs) (Rodieck and Watanabe, 1993;Dacey et al, , 2005Dacey, 2004;Yamada et al, 2005) have been characterized physiologically, namely the ON and OFF midget and parasol cells (Dacey, 1999;Chichilnisky and Kalmar, 2002), the small bistratified cells (Dacey and Lee, 1994;Chichilnisky and Baylor, 1999), the recently discovered giant sparse (melanopsin-expressing) cells (Dacey et al, , 2005Dacey, 2004), and, to some extent, the large bistratified cells and the cells of type "sparse" Dacey, 2004). One of the possible reasons for this discrepancy is that the morphological RGC types awaiting physiological characterization constitute only a small fraction of all the primate ganglion cells (1-4%) [see Dacey (2004), their table 20.1].…”

Microcircuitry for Two Types of Achromatic Ganglion Cell in Primate Fovea

“…Spatial summation of photoisomerizations across cones and transmitter quanta across synapses confers greater contrast sensitivity and faster kinetics: M cells are approximately eightfold more sensitive than P cells and respond to higher temporal frequencies (Derrington and Lennie, 1984;Croner et al, 1993;Frechette et al, 2005). The retinal origin of the M pathway was generally assigned to a single anatomical class of ganglion cell termed "parasol" (Polyak, 1941;Wässle and Boycott, 1991;Grünert et al, 1993), but there are multiple types of diffuse bipolar cell with different kinetics (DeVries, 2000); furthermore, there are multiple types of non-midget ganglion cell that could project to the geniculate M layers (Kolb et al, 1992;Rodieck and Watanabe, 1993;Dacey et al, 2003;Calkins et al, 2005). This raises key questions regarding their synaptic circuitry.…”

Molecular Phenotyping of Retinal Ganglion Cells

“…Subsets of mammalian ganglion cell classes project to an array of central targets (Fukuda and Stone, 1974;Farmer and Rodieck, 1982;Leventhal et al, 1985;Rodieck and Watanabe, 1993;Pu et al, 1994;Rodieck, 1998), but a unified description of all classes and distributions in the ganglion cell layer has remained elusive. Several summaries of how neuronal typologies might be abstracted have emerged, some accompanied by debates regarding methods, definitions, and results (Rowe and Stone, 1977;Hughes, 1979;Holden, 1981;Rodieck and Brening, 1982;Famiglietti, 1992;Wingate et al, 1992;Cook, 1998;Masland and Raviola, 2000).…”