Direction-selective retinal ganglion cells encode motion direction uniformly, despite having discretely distributed cardinal preferences

On-Off direction-selective retinal ganglion cells (DS RGCs) exhibit broad tuning curves, responding robustly to motion aligned with or near their preferred direction. These cells comprise four major subtypes, each tuned to motion along one of the four cardinal axes: nasal, superior, temporal, or inferior. However, natural stimuli can move in any direction, and it remains unclear whether intermediate directions are encoded less effectively, or whether this cardinal organization nevertheless supports uniform direction encoding. Here, we combined previous electrophysiological recordings of DS cells presented with a moving light bar stimulus with an information-theoretic measure, the Stimulus Specific Information, to estimate the directional sensitivity of small populations of recorded neurons. This analysis revealed that DS RGC populations are uniformly sensitive across all directions of motion. We then asked whether the observed homogeneous sensitivity was a consequence of DS RGCs maximizing the average stimulus information. Simulations with artificially modified tuning curve widths revealed that DS cells prioritize avoiding pronounced drops in sensitivity over maximizing the average transmitted information. This property reduces large deficits in sensitivity for certain directions, thereby limiting potential “blind spots” in the encoding of motion. More generally, our results raise the possibility that maintaining a high minimum sensitivity could be one factor influencing the organization of sensory representations.Author summary: The detection of moving objects by the visual system starts in the retina. A special set of retinal ganglion cells, called direction-selective cells, respond most strongly when objects move along one of four main directions (up, down, left, or right). But in real life, motion can occur in any direction. What does the sensitivity of this system look like for individual directions of motion? For example, does the retina miss some information for diagonally moving stimuli?