Functional Asymmetries in ON and OFF Ganglion Cells of Primate Retina

Abstract

Functional asymmetries in the ON and OFF pathways of the primate visual system were examined using simultaneous multi-electrode recordings from dozens of retinal ganglion cells (RGCs) in vitro. Light responses of RGCs were characterized using white noise stimulation. Two distinct functional types of cells frequently encountered, one ON and one OFF, had non-opponent spectral sensitivity, relatively high response gain, transient light responses, and large receptive fields (RFs) that tiled the region of retina recorded, suggesting that they belonged to the same morphological cell class, most likely parasol. Three principal functional asymmetries were observed. (1) Receptive fields of ON cells were 20% larger in diameter than those of OFF cells, resulting in higher full-field sensitivity. (2) ON cells had faster response kinetics than OFF cells, with a 10-20% shorter time to peak, trough and zero crossing in the biphasic temporal impulse response. (3) ON cells had more nearly linear light responses and were capable of signaling decrements, whereas OFF cells had more strongly rectifying responses that provided little information about increments. These findings suggest specific mechanistic asymmetries in retinal ON and OFF circuits and differences in visual performance on the basis of the activity of ON and OFF parasol cells.

Cell density ratios in a foveal patch in macaque retina

“…sawtooth stimuli; (3) the receptive fields of the effect are much larger than that of the midget cells (Anstis & Harris, 1987); and (4) the high contrast sensitivity of individual parasol-but not midgetganglion cells is similar to human contrast sensitivity as studied in these experiments (Kremers et al, 1993). Individual ON and OFF ganglion cells in macaque are equally sensitive to increments and decrements, respectively, so the psychophysical asymmetry appears to reflect a greater density of outer than inner parasol ganglion cells, not the properties of individual cells (Kremers et al, 1991(Kremers et al, , 1993Benardete & Kaplan, 1999; but see Chichilnisky & Kalmar, 2002). Consistent with this interpretation, human observers exhibit finer spatial resolution for light decrements than for light increments (Zemon et al, 1988).…”

“…In macaque retina, Chichilnisky and Kalmar (2002) report receptive fields for macaque ON parasol ganglion cells that are 1.2 times the diameter of OFF, hence 1.44 times the area. If coverage by ON and OFF ganglion cells were equal, the density of outer parasol ganglion cells would have to be 1.44 times the density of inner parasol ganglion cells.…”

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

“…As a measure of the RF center response latency for an RGC, we used the zero crossing time (t zero ) of the STA time filters (Chichilnisky and Kalmar, 2002). In a linear-nonlinear response model (Chichilnisky, 2001), when the cell is stimulated by a small-amplitude light step presented over the RF center, t zero corresponds to the time from the onset of the light step to the peak of the response.…”

“…The shape of each time filter was parameterized by the two most significant principal components, obtained by performing principal components analysis on the combined time filters of all OFF neurons (see Materials and Methods). Two of the clusters were identified as parasol and midget cells by their RF diameters and their response kinetics (Chichilnisky and Kalmar, 2002). The two remaining clusters, C 1 and C 2 , were of unknown cell type.…”

“…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].…”