Saccadic suppression by way of retinal image processing

Abstract

Humans make eye movements such as saccades four times every second. Saccades disrupt the visual flow on the retina; however, visual perception remains a stable and coherent process. This is a striking achievement of the visual system. Visual stability around the time of these eye movements is partially associated with a reduction in visual sensitivity, a phenomenon known as saccadic suppression. While saccadic suppression has been extensively characterized at the perceptual and neural levels, its underlying mechanisms remain elusive. According to the favored view, eye-movement related signals play a central role in the genesis of saccadic suppression. Despite extensive efforts to substantiate these claims, the neural origin of such signals has not been established.

In this dissertation, we challenge the dominant view that saccadic suppression is triggered by eye-movement related signals. Instead, using electrophysiology in mouse, pig, and macaque retina, 2-photon calcium imaging, computational modeling, and human psychophysics we show evidence that visual mechanisms starting at the retina account for perceptual saccadic suppression. Cellular and circuit level descriptions of these retinal mechanisms are presented in detail. Most notably, we find a novel retinal processing motif underlying retinal saccadic suppression, “dynamic reversal suppression”, which is triggered by sequential stimuli containing contrast reversals. This motif does not involve inhibition but relies on nonlinear transformation of the inherently slow responses of cone photoreceptors by downstream retinal pathways. We also found that eye-movement related signals act to shorten the suppression resulting from visual mechanisms - a diametrically opposite involvement of eye movement signals than proposed in the literature.

Overall, our results establish a neural locus of saccadic suppression, and provide detailed mechanistic insights underlying it. These findings resolve a long-standing open question concerning the origin of saccadic suppression. Given that the retinal saccadic suppression is triggered by sequential visual stimulation, our results also describe retinal processing of dynamic stimuli.