ON-OFF DS ganglion cells detect motion and suppress luminance responses during natural viewing

Abstract

Purpose: Directionally selective (DS) retinal ganglion cells generate robust spiking in response to movement of a stimulus in one (preferred) direction but spike little or none to movement of the same stimulus in the opposite (null) direction. Although numerous studies have investigated the performance and mechanism of DS cells using artificial stimuli such as high-contrast moving bars, the ability of DS cells to extract motion from complex natural stimuli is not well understood. ON-OFF DS cells also respond strongly to sudden changes in luminance raising the question of how the brain distinguishes between spikes arising from motion and spikes arising from luminance changes. Here, we measured the response of DS cells to natural movies that contained complex motion as well as a wide range of luminance changes. Methods: Cell-attached patch clamping was used to record spikes from ganglion cells in the isolated rabbit retina. Ganglion cells were classified as ON or OFF cells by their response to stationary flashes, and as DS or non-DS by their response to moving bars in 12 directions. After cell type classification, a natural scenes movie (2 mm diameter, 20 frames/sec, and 18 sec duration) was presented 12 times to a targeted ganglion cell

between each presentation the movie was rotated by 30 degrees. We recorded the movie responses of ON-OFF DS cells (n=14), non-DS ON cells (n=7), and non-DS OFF cells (n=8). Results: The response of DS cells varied considerably with the angle of rotation of the movie. Responses were strongest for a given scene when the rotation of the movie was such that the motion (within that scene) was aligned with the cell’s preferred direction. Directional indices for such scenes were comparable to those elicited by laboratory stimuli. In contrast, responses of ON and OFF cells changed little for rotations of the movie. Surprisingly, the responses to movie scenes that contained luminance change