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.
Saccades are a fundamental part of natural vision. They interrupt fixations of the visual gaze and rapidly shift the image that falls onto the retina. These stimulus dynamics can cause activation or suppression of different retinal ganglion cells, but how they affect the encoding of visual information in different types of ganglion cells is largely unknown. Here, we recorded spiking responses to saccade-like shifts of luminance gratings from ganglion cells in isolated marmoset retinas and investigated how the activity depended on the combination of pre- and post-saccadic images. All identified cell types, On and Off parasol and midget cells as well as a type of Large Off cells, displayed distinct response patterns, including particular sensitivity to either the pre- or the post-saccadic image or combinations thereof. In addition, Off parasol and Large Off cells, but not On cells, showed pronounced sensitivity to whether the image changed across the transition. Stimulus sensitivity of On cells could be explained based on their responses to step changes in light intensity, whereas Off cells, in particular, parasol and the Large Off cells, seem to be affected by additional interactions that are not triggered during simple light-intensity flashes. Together, our data show that ganglion cells in the primate retina are sensitive to different combinations of pre- and post-saccadic visual stimuli. This contributes to the functional diversity of the retina's output signals and to asymmetries between On and Off pathways and provides evidence of signal processing beyond what is triggered by isolated steps in light intensity.
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