Microscopic Eye Movements Compensate for Nonhomogeneous Vision within the Fovea

Abstract

Summary Humans rely on the fovea, the small region of the retina where receptors are most densely packed, for seeing fine spatial detail. Outside the fovea, it is well established that a variety of visual functions progressively decline with eccentricity [1–5]. In contrast, little is known about how vision varies within the central fovea, as incessant microscopic eye movements prevent isolation of adjacent foveal locations [6–8]. Using a new method for restricting visual stimulation to a selected retinal region, we examined the discrimination of fine patterns at different eccentricities within the foveola. We show that high-acuity judgments are impaired when stimuli are presented just a few arcminutes away from the preferred retinal locus of fixation. Furthermore, we show that this dependence on eccentricity is normally counter-balanced by the occurrence of precisely directed microsaccades, which bring the preferred fixation locus onto the stimulus. Thus, contrary to common assumptions, vision is not uniform within the foveola, but targeted microscopic eye movements compensate for this lack of homogeneity. Our results reveal that microsaccades, like larger saccades, enable examination of the stimulus at a finer level of detail and suggest that a reduced precision in oculomotor control may be responsible for the visual acuity impairments observed in various disorders.

Oculomotor inhibition covaries with conscious detection

“…In contrast to many other studies, we did not demonstrate a sustained effect of a cognitive state on microsaccade rates (Cui et al 2009;Poletti et al 2013;Steinman et al 1967; or an influence of microsaccades on perceptual performance (Deubel and Eisner 1986;Martinez-Conde et al 2006). Rather, we showed that trial-by-trial variations in perception are linked (within 1/10 of a second after the stimulus onset) to these involuntary eye movements.…”

“…Therefore, physically weak or adapted stimuli are detected relatively infrequently, but when they are detected they cause strong oculomotor freezing. Similarly, some researchers have posited that conscious detection is an all-or-none phenomenon (Dehaene and Changeux 2011;Dehaene et al 2003;Quiroga et al 2008). We argue that across-trial aggregate measures of perceptual sensitivity (d=) and the oculomotor response show similar effects of stimulus parameters (such as contrast, as shown in our experiment 1 and by Bonneh et al 2015 andScholes at al.…”

“…For instance, a microsaccade that occurs 250 ms after the time of potential stimulus onset would provide strong evidence that no stimulus was present or perceived, because microsaccadic inhibition on present trials is strongest around 250 ms. We computed classification accuracy using the criterion-free measure A=, the area under the ROC curve. For a similar analysis applied to single neuron firing rates to classify perception on individual trials, see Quiroga et al (2008).…”

Microsaccades Are Coupled to Heartbeat

“…It seems that microsaccades fulfill the same purpose as large saccades, precisely shifting gaze to the most relevant locations to achieve the goal of a task (Kowler and Collewijn, 2010). This claim is further supported by the finding that visual sensitivity is not homogenous across the fovea and microsaccades bring the stimulus onto the preferred retinal locus of fixation (Poletti et al, 2013). Moreover, an excess of microsaccades is observed during inspection of informative scene regions, suggesting a role of microsaccades in the sampling of visual information (McCamy et al, 2014b).…”

Foveated Nonlocal Self-Similarity

“…In particular, it was shown that not only these movements prevent retinal image fatigue and visual fading, but play also a crucial role in controlling the fixation position (Engbert and Kliegl 2004). Experiments (see, e.g., Donner and Hemilä 2007;Rucci et al 2007;McCamy et al 2012;Poletti et al 2013) reveal that the retinal responses caused by microsaccadic movements reduce aliasing effects in the peripheral retina, lead to improved spatiotemporal accuracy of the neural responses, and provide additional information that allows resolving fine spatial details out of optically blurred images.…”