Retinal adaptation to spatial correlations

AbstractThe classical center-surround retinal ganglion cell receptive field is thought to remove the strong spatial correlations in natural scenes, enabling efficient use of limited bandwidth. While early studies with drifting gratings reported robust surrounds (Enroth-Cugell and Robson, 1966), recent measurements with white noise reveal weak surrounds (Chichilnisky and Kalmar, 2002). This might be evidence for dynamical weakening of the retinal surround in response to decreased spatial correlations, which would be predicted by efficient coding theory. Such adaptation is reported in LGN (Lesica et al., 2007), but whether the retina also adapts to correlations is unknown.We tested for adaptation by recording simultaneously from ~40 ganglion cells on a multi-electrode array while presenting white and exponentially correlated checkerboards and strips. Measuring from ~200 cells responding to 90 minutes each of white and correlated stimuli, we were able to extract precise spatiotemporal receptive fields (STRFs). We found that a difference-of-Gaussians was not a good fit and the surround was generally displaced from the center. Thus, to assess surround strength we found the center and surround regions and the total weight on the pixels in each region. The relative surround strength was then defined as the ratio of surround weight to center weight. Surprisingly, we found that the majority of recorded cells have a stronger surround under white noise than under correlated noise (p<.05), contrary to naive expectation from theory. The conclusion was robust to different methods of extracting STRFs and persisted with checkerboard and strip stimuli.To test, without assuming a model, whether the retina decorrelates stimuli, we also measured the pairwise correlations between spike trains of simultaneously recorded neurons under three conditions: white checkerboard, exponentially correlated noise, and scale-free noise. The typical amount of pairwise correlation increased with extent of input correlation, in line with our STRF measurements.