Separability of stimulus parameter encoding by on-off directionally selective rabbit retinal ganglion cells

Abstract

The ganglion cell output of the retina constitutes a bottleneck in sensory processing in that ganglion cells must encode multiple stimulus parameters in their responses. Here we investigate encoding strategies of On-Off directionally selective retinal ganglion cells (On-Off DS RGCs) in rabbits, a class of cells dedicated to representing motion. The exquisite axial discrimination of these cells to preferred vs. null direction motion is well documented: it is invariant with respect to speed, contrast, spatial configuration, spatial frequency, and motion extent. However, these cells have broad direction tuning curves and their responses also vary as a function of other parameters such as speed and contrast. In this study, we examined whether the variation in responses across multiple stimulus parameters is systematic, that is the same for all cells, and separable, such that the response to a stimulus is a product of the effects of each stimulus parameter alone. We extracellularly recorded single On-Off DS RGCs in a superfused eyecup preparation while stimulating them with moving bars. We found that spike count responses of these cells scaled as independent functions of direction, speed, and luminance. Moreover, the speed and luminance functions were common across the whole sample of cells. Based on these findings, we developed a model that accurately predicted responses of On-Off DS RGCs as products of separable functions of direction, speed, and luminance (r = 0.98; P < 0.0001). Such a multiplicatively separable encoding strategy may simplify the decoding of these cells' outputs by the higher visual centers.

Specific Wiring of Distinct Amacrine Cells in the Directionally Selective Retinal Circuit Permits Independent Coding of Direction and Size

“…Further statistical analysis of the data confirmed the lack of dependence between spatial and temporal tuning ( Figure S3) giving rise to a velocity tuning index (VTi; see Experimental Procedures) that was near zero for both dim and light conditions ( Figure 6E). The separable spatiotemporal tuning described here for mouse DSGCs is comparable to tuning of rabbit DSGCs (Grzywacz and Amthor, 2007;He and Levick, 2000) and along with the separability of other stimulus dimensions (e.g., contrast; Nowak et al, 2011), is likely to facilitate the decoding of directional and nondirectional signals by higher visual centers (van Hateren, 1990).…”

“…Similarly, DSi was computed as (P À N / P + N), where P and N are response amplitudes measured in the cell's preferred or null direction, respectively. Directional tuning widths were estimated using a Gaussian function (Nowak et al, 2011).…”

“Silent” NMDA Synapses Enhance Motion Sensitivity in a Mature Retinal Circuit

“…ON-OFF DSGCs were distinguished from other ganglion cells based on their direction and speed tuning (Figure 6A; Figure S5; see Methods). A heat map of the average number of spikes/trial measured across the population of DSGCs plotted as a function of direction and contrast (Figure 6C), depicts for the first time the ability of mouse DSGCs to maintain their directional tuning properties across a large contrast range, consistent with the behavior of their counterparts in the rabbit retina (Grzywacz and Amthor, 2007; Nowak et al, 2011). However, small but statistically significant contrast-dependent changes in tuning reflected in direction selectivity index (DSI; see methods) were observed in the low (DSI 10% = 0.46 ± 0.04; DSI 20% = 0.61 ± 0.02; p < 0.005, Wilcoxon signed-rank test) and high-contrast ranges (DSI 150% = 0.57 ± 0.02; DSI 300% = 0.47 ± 0.02; p < 0.05, Wilcoxon signed-rank test).…”

“…The bar was 240 μm wide on the retina and moved at 960 μm/s. The direction-tuning curve was centered at the preferred direction and fit with a cosine or Gaussian equation, as indicated (Nowak et al, 2011). …”

“…In contrast, however, a number of other studies indicate that AMPA/NMDA receptor-mediated inputs to DSGCs scale together as a function of contrast, consistent with observations in other types of ganglion cells, suggesting that AMPA and NMDA receptors are driven by a common source of glutamate (Buldyrev et al, 2012; Diamond and Copenhagen, 1995; Manookin et al, 2010; Poleg-Polsky and Diamond, 2016b; Stafford et al, 2014). These diverging results have given rise to two distinct models that explain how the DS circuit coordinates inhibition/excitation over a range of stimulus contrasts (Figure 1A & D), which underlies the DSGC's robust ability to compute direction (Grzywacz and Amthor, 2007; Nowak et al, 2011; Poleg-Polsky and Diamond, 2016b). …”