Signals of eye-muscle proprioception modulate perceived motion smear

Abstract

Achieving clear perception during eye movements is one of the major challenges that the human visual system has to face every day. Like most light sensitive mechanisms, the human visual system has a finite integration time that may cause moving images to appear smeared. By comparing the perceived motion smear during ongoing eye movements and fixation, previous studies indicated that smear is reduced by a neural compensation mechanism that uses "extra-retinal information" about eye movements. However, it is not clear whether eye-muscle proprioception (afferent input), internal copies of efferent oculomotor commands (efference copy), or both contribute to the smear reduction. The present study found that similar reductions of perceived motion smear occur during passive eye movement (which is signaled only by eye-muscle proprioception) and during active pursuit tracking (for which efference copy signals exist as well). These results reveal a novel neural contribution for maintaining visual clarity and stand in contrast to previous reports that eye-muscle proprioception makes only a minor contribution to visual perception.

Keep your eyes on the ball: smooth pursuit eye movements enhance prediction of visual motion

“…We hypothesize that E_hat may be computed from different sources during pursuit and fixation and that this difference might account for the performance difference. Whereas pursuit eye velocity may be compensated by extraretinal signals, for instance, to reduce perceived motion smear (Tong et al 2008), velocity compensation during fixational eye movements seems to rely on retinal signals alone (Poletti et al 2010). Our paradigm contained no visual references aside from the ball and the goal, presumably making a possible retinal-motion-based estimation of E during fixation imprecise.…”

Auditory/Visual Integration Assessment and Treatment in Brain Injury Rehabilitation

“…In fact, ocular proprioception is a major player in spatial localization and maintaining clear central eyesight [44,45], dovetailing with other research demonstrating that problems after brain injury can affect signaling in the peripheral retina. A recent study found evidence that retinal ganglion cells in the peripheral retina showed more activity in people with attention deficit disorder, as compared to a normal control group [46].…”

The perception of motion smear during eye and head movements

“…These extra-retinal signals are based on a combination of internal efference copy information and inflowing signals of muscle proprioception (Gauthier, Nommay & Vercher, 1990; Bridgeman & Stark, 1991). The extent of perceived motion smear is reduced when a visual target is presented in darkness during a passive smooth eye movement (Tong, Stevenson & Bedell, 2008), which was induced when the observer pushed laterally on a circular wire loop that was held against the upper and lower lids of one eye. This outcome indicates that proprioceptive signals alone are sufficient for a reduction of perceived motion smear to occur.…”