Saccades during visual search in macular degeneration

Abstract

Macular degeneration (MD) compromises both high-acuity vision and eye movements when the foveal regions of both eyes are affected. Individuals with MD adapt to central field loss by adopting a preferred retinal locus (PRL) for fixation. Here, we investigate how individuals with bilateral MD use eye movements to search for targets in a visual scene under realistic binocular viewing conditions. Five individuals with binocular scotomata, 3 individuals with monocular scotomata and 6 age-matched controls participated in our study. We first extensively mapped the binocular scotoma with an eyetracker, while fixation was carefully monitored (Vullings & Verghese, 2020). Participants then completed a visual search task where 0, 1, or 2 Gaussian blobs were distributed randomly across a natural scene. Participants were given 10 s to actively search the display and report the number of blobs. An analysis of saccade characteristics showed that individuals with binocular scotomata made more saccades in the direction of their scotoma than controls for the same directions. Saccades in the direction of the scotoma were typically of small amplitude, and did not fully uncover the region previously hidden by the scotoma. Rather than make more saccades to explore this hidden region, participants frequently made saccades back toward newly uncovered regions. Backward saccades likely serve a similar purpose to regressive saccades exhibited during reading in MD, by inspecting previously covered regions near the direction of gaze. Our analysis suggests that the higher prevalence of backward saccades in individuals with binocular scotomata might be related to the PRL being adjacent to the scotoma.

Keywords: Backward/regressive saccade; Binocular scotoma; Macular degeneration; Visual search.

Figure 1:

Timeline of a trial. Trial start required the observer to fixate the central marker and press a button. A full-screen image was presented for 10 s, during which observers searched for Gaussian blobs while eye movements were recorded. This particular trial shows 2 blobs (marked by circular outlines for purposes of illustration only; the outlines did not appear in the display). After the trial ended, participants reported the number of blobs.

Figure 2.

A. Accuracy at the visual search task for all participants (orange: Controls, blue: monocular MDs, green: Binocular MDs). The horizontal dashed line corresponds to 33%, the probability of guessing the answer by chance. The solid line represents the average within a participant group and the dotted lines represent the bootstrapped 95% confidence intervals (CI). B. The individual plots display the size of the scotoma for our binocular scotoma participants. Their fixation stability is estimated by a kernel density plot of fixation distribution during binocular scotoma mapping. The monocular scotoma participants and controls have no measurable field defect (binocular scotoma).

Figure 3.

The median saccade amplitude for the control (orange), monocular (cyan) and binocular (green) scotoma groups, that includes saccades in all directions. For the binocular saccade group, saccades are further broken down by saccades away from the scotoma (gray) and those toward the scotoma (gold) as shown in the schematic. Error bars indicated 95% confidence intervals of the median.

Figure 4.

A polar histogram of saccade directions for our 5 MD participants with Binocular scotomata (green) and 3 MD participants with monocular scotomata (cyan). B2 is the same individuals as M1, following wet AMD in one eye, creating a binocular scotoma. The superimposed gray regions indicate the size of the scotoma for the binocular MD participants, relative to a PRL at the origin. The orange contour marks the average saccade direction for control participants. The dark and light gray arcs indicate direction where the saccade frequency is significantly higher or lower than the 95% confidence limits of the frequency for controls. The saccade distribution appears to be skewed toward the scotoma for these participants.

Figure 5.

A. Saccade distribution with respect to the fovea for control participants. B. Saccade distribution with respect to the PRL for binocular MD participants. The closed contour outlines the extent of the scotoma with respect to the PRL for each participant. Gold points mark saccades that were directed to locations within the scotoma and gray points mark saccades to visible points.

Figure 6

A. Schematic showing the starting position of the PRL and scotoma (light grey), the position of these after a saccade toward the scotoma (dark grey) and the fraction of the original scotoma region that is uncovered by the saccade. B. Distribution of control saccades with one observer’s scotoma profile superimposed to show what MD saccades within would look like if they followed the same distribution as controls. C. Predictions of the “Uncover” Model showing the proportion of the scotoma uncovered by saccades to various points. D. Predicted map of the Control Model where MD observers’ saccades follow the distribution estimated from control observers. E. Predicted map of a model that is hybrid between the Uncover and Control Models. F. Observer B4’s data for saccades that are directed toward the scotoma. Maps and data in Panels C through F are represented as tertiles. See text for explanation.

Figure 7.

Frequency of consecutive saccades that either stay in the visible region (gray), or are directed toward the region covered by the scotoma (gold). The count of consecutive saccades that stay in either of these regions progressively decreases, but consecutive saccades to covered regions typically occur less frequently than consecutive saccades to visible regions.

Figure 8

A. Schematic showing a saccade toward the scotoma on the left (gold arrow) and a saccade away from the scotoma on the right (gray arrow). In both cases, the subsequent saccade is toward the region uncovered by the preceding saccade (black arrow). B. Comparison of backward saccades when they are preceded by saccades toward the scotoma or by saccades to visible regions. The first two columns compare backward saccades to recently uncovered regions following a saccade toward the scotoma. Green bars show the data for individual binocular MD participants and orange bars show the proportion of such saccades occurring among controls with simulated scotomata (see text for details). The last two columns compare backward saccades to uncovered regions following a saccade to an already visible region for MD participants (green) and simulated controls (orange). Errors bars are standard errors of the mean.

Figure 9.

A. The dashed cross and the dashed outline shows the original position of the PRL and scotoma. The gold and gray arrows and corresponding scotoma profiles mark PRL and scotoma locations after saccades toward and away from the scotoma, respectively. The black arrow shows a sample saccade to the recently uncovered information in both cases. It is clear that there is newly uncovered information in both cases, but this information is close to the PRL (black cross) after a saccade towards a scotoma, but is further from the PRL after a saccade away from the scotoma. B. Histograms of the distribution of first saccade amplitudes that were followed by a saccade to a recently uncovered region. Yellow and gray depict preceding saccades that went toward and away from the scotoma (regions of overlap appear darker yellow). Alongside the individual histograms are the scotoma profiles for each observer.