Spatial Adaptation of Primate Retinal Ganglion Cells between Artificial and Natural Stimuli

The retina encodes a broad range of stimuli, adapting its computations to features like brightness, contrast, or motion. However, it is unclear to what extent it also adapts to spatial frequency content - as theories of efficient coding would predict - for instance, when switching between natural scenes and white noise. To address this, we analyzed neural activity of marmoset retinal ganglion cells (RGCs) in response to white noise and naturalistic movie stimuli. We trained linear-nonlinear models on both stimuli, evaluated their performance and compared their receptive fields (RFs) across the stimulus domains. We found that the models with spatial filters trained on either one of the stimulus ensembles were not able to predict the neural activity on the other as accurately as the models trained on the target stimulus. This suggests that spatial processing adapts to stimulus statistics. Different RGC types exhibited distinct changes: the midget OFF cells RFs became enlarged under natural movie statistics, resulting in a lower cutoff frequency. Parasol cells did not change their RF size significantly. Large OFF cells RFs decreased in size. All cell types exhibited stronger surrounds under natural movies, resembling the whitening filters predicted by efficient coding. However, quantifying the effect of the filter adaptation on the stimulus power spectrum showed a significant contribution towards whitening only in ON parasol cells. The whitening effect emerged regardless of the training stimulus. These results suggest that while RGCs adapt to the spatial frequency content of the input, efficient coding can only partially account for this adaptation. Significance statementNatural scenes differ from artificial stimuli like white noise, in spatial frequency structure. How the retina adapts to these differences remains unclear. To explore this, we studied responses of four primate retinal ganglion cell types to artificial and natural stimuli. Our results show that some cell types, like midget cells, enlarge their receptive fields and surrounds under natural stimuli, while others, like parasol cells, only enhance surrounds. These changes align qualitatively with the efficient coding theory, which posits redundancy reduction. However, in three cell types, the enhanced surrounds did not significantly whiten responses to natural stimuli, contrary to efficient coding predictions. These findings challenge how fully efficient coding explains retinal adaptation, suggesting that other principles underlie the processing of visual inputs.