Natural stimuli drive concerted nonlinear responses in populations of retinal ganglion cells

The role of the vertebrate retina in early vision is generally described by the efficient coding theory, which predicts that the retina discards spatiotemporal correlations in natural scenes. It is unclear, however, whether the predicted decorrelation in the activity of ganglion cells, the retina’s output neurons, holds under gaze shifts, which dominate the natural visual input. We here show that species-specific gaze patterns in natural stimuli can drive strong and correlated spiking responses both within and across distinct types of ganglion cells in marmoset as well as mouse retina. These concerted responses violate efficient coding and signal fixation periods with locally high spatial contrast. Finally, novel model-based analyses of ganglion cell responses to natural stimuli reveal that the observed response correlations follow from nonlinear pooling of ganglion cell inputs. Our results reveal how concerted population activity can surpass efficient coding to detect gaze-related stimulus features.