Fixational eye movements as active sensation for high visual acuity

Abstract

Perception and action are inherently entangled: our world view is shaped by how we explore and navigate our environment through complex and variable self-motion. Even when fixating on a stable stimulus, our eyes undergo small, involuntary movements. Fixational eye movements (FEM) render a stable world jittery on our retinae, which contributes noise to neural coding. Yet, empirical evidence suggests that FEM help rather than harm human perception of fine detail. Here, we elucidate this paradox by uncovering under which conditions FEM improve or impair retinal coding and human acuity. We combine theory and experiment: model accuracy is directly compared to that of healthy human subjects in a visual acuity task. Acuity is modeled by applying an ideal Bayesian classifier to simulations of retinal spiking activity in the presence of FEM. In addition, empirical FEM are monitored using high-resolution eye-tracking by an adaptive optics scanning laser ophthalmoscope. While FEM introduce noise, they also effectively pre-process visual inputs to facilitate retinal information encoding. Based on an interplay of these mechanisms, our model predicts a relation between visual acuity, FEM amplitude, and single-trial stimulus size that quantitatively accounts for experimental observations and captures the beneficial effect of FEM. Moreover, we observe that human subjects’ FEM statistics vary with stimulus size, and our model suggests that changing eye motion amplitude, as the subjects indeed do, enhances acuity as compared to maintaining eye motion size constant. Overall, our findings indicate that perception benefits from action even at the fine and noise-dominated spatio-temporal scale of FEM.Significance StatementPerception is inherently active: we need to move our eyes to see the world around us. Yet our eyes also undergo tiny, unconscious movements that can blur out fine visual details. Paradoxically, previous work suggested that these small movements aid fine detail perception. Here, we investigate this paradox to uncover in which contexts small eye movements help or harm visual acuity. Comparing a model of retinal responses with recordings of human visual acuity, we elucidate the mechanisms by which and conditions in which small eye movements support fine detail discrimination. Our results also suggest that varying eye movement amplitude according to stimulus size enhances retinal coding, highlighting that perception is active even at the level of very fine eye movements.

Visual feature tuning properties of short-latency stimulus-driven ocular position drift responses during gaze fixation

“…This is consistent with our earlier observations about ocular position drifts in peripheral Posner-like cueing tasks (Tian et al, 2018). An important implication of this is that ocular position drifts are not entirely random movements, consistent with other evidence (Murphy et al, 1975; Kowler and Steinman, 1979b, a; Ahissar et al, 2016; Tian et al, 2018; Skinner et al, 2019; Bowers et al, 2021; Reiniger et al, 2021; Clark et al, 2022; Nghiem et al, 2022). This evidence again has parallels in the field of microsaccades, which were thought to be random until two decades ago (Hafed and Clark, 2002; Engbert and Kliegl, 2003).…”

“…In all, the results of Fig. 5 confirm that ocular position drifts are not always random or stochastic (Kowler and Steinman, 1979b, a; Ahissar et al, 2016; Tian et al, 2018; Skinner et al, 2019; Bowers et al, 2021; Reiniger et al, 2021; Clark et al, 2022; Nghiem et al, 2022), and that these drifts can reliably reflect localized stimulus locations in addition to exhibiting a (potentially reflexive) upward drift pulse. Having said that, true dependence of ocular position drifts on localized stimulus locations should include evidence of spatially-directed drift trajectories for the vertical dimension as well.…”

Sub-cone visual resolution by active, adaptive sampling in the human foveola

“…Other aspects are likely to also influence the trial-wise motion, e.g. drift motion might be particularly tuned for stimulus sizes close to the threshold and less crucial for larger gap sizes as suggested in a recent model of early visual signal processing 36 .…”

“…While the neuronal mechanisms that generate fixational drift are still not fully understood 34 , its consequence to visual perception has been demonstrated. Drift was shown to improve visual performance in resolution tasks 26,29,35 , and a recent model of early retinal signals suggests that if drift amplitude is tuned to object size, visual acuity would be enhanced 36 . Indeed, considerable differences in ocular drift between individuals exist 32,37 , and subjects exhibiting less drift were shown to have better acuity 32 .…”

Action potential propagation speed compensates for traveling distance in the human retina

“…However, the underlying organizational principle of these trajectories remains poorly understood, and precise measurements of axonal lengths have not been conducted for the entire human eye. The temporal dispersion of the arrival times at the optic disc of action potentials that have been elicited synchronously in the retina is an unresolved issue of high relevance for central human vision, as the precise timing of action potentials from presynaptic neurons reaching postsynaptic neurons is crucial for neural information processing ( 21, 22 ).…”