Eye, head, and gaze contributions to smooth pursuit in macular degeneration

Abstract

Macular degeneration (MD) often leads to the loss of the fovea and surrounding central visual field. This type of visual loss is very common and can present particular challenges for oculomotor tasks that may rely on the fovea. For certain tasks, individuals develop a new, eccentric fixational locus. Our previous work has shown that smooth pursuit is impaired in MD. However, extent of retinal lesion size and eccentricity of fixation do not directly contribute to changes in smooth pursuit gain. Oculomotor limitations due to eccentric eye position in the orbit may be another culprit. Here we test the hypothesis that deficits in smooth pursuit in MD would be reduced under head-unrestrained conditions. To that end, we examined eye, head, and gaze movements in eight individuals with MD and seven age-matched controls in response to a step-ramp pursuit stimulus. We found that despite variability across participants, both groups had similar smooth pursuit head movements (P = 0.76), while both had significantly higher pursuit gains in the head-restrained condition (P < 0.0001), suggesting that in older populations, head movements may lead to a decrease in pursuit gain. Furthermore, we did not find a correlation between eccentricity of fixation and amount of head displacement during the trial (P = 0.25), suggesting that eccentric eye position does not lead to higher reliance on head movements in smooth pursuit. Our finding that individuals with MD have lower pursuit gains, despite similar head movements as controls, suggests a difference in how MD affects mechanisms underlying eye versus head movements in smooth pursuit.NEW & NOTEWORTHY This article is the first to look at eye and head movements in observers with macular degeneration. It is the first to show that in older individuals, regardless of central field defect, freedom of head movement may reduce pursuit gain. Despite oculomotor limitations due to eccentric fixation, individuals with macular degeneration do not rely on head movements more than age-matched controls, with both groups having a similarly heterogenous eye and head movement strategy for pursuit.

Keywords: eccentric viewing; eye/head coordination; head-free; macular degeneration; smooth pursuit.

Fig. 1.

Example eye and head position and velocity data for 1 control (A and B, participant C2) and 1 participant with age-related macular degeneration (MD) (C and D, participant P5). A and C: head-unrestrained condition. B and D: head-restrained condition. The target ramp was in the rightward direction (0°) on all 4 trials. Top: position. Bottom: velocity data. Dashed black line: head, dotted black line: eye in head, solid black line: eye in space (gaze), and gray line: target. Regions designated by gray rectangles are those chosen as periods of longest continuous pursuit for the particular trial. All metrics are along the horizontal direction.

Fig. 2.

Smooth pursuit gaze gain of individuals with macular degeneration (black circles) and controls (gray circles) under head-unrestrained (outlined, left) and head-restrained (filled, right) conditions. Light gray dashed line represents gain = 1 (gaze velocity = target velocity). Error bars represent SE. Arrows along x-axis show target trajectories.

Fig. 3.

Mean eye and head velocity during longest period of continuous pursuit plotted across target directions. A: mean eye and head velocity is plotted for the head-unrestrained condition (columns 1 and 2) and mean eye velocity is plotted for the head restrained condition (column 3). Gray dashed line indicates target velocity. Black and gray horizontal bars indicate median velocity for each group/condition. B: mean eye and head velocity data from Head-Unrestrained columns in A are plotted against each other. Black dashed line represents perfect smooth pursuit gaze velocity. Each dot represents a control (gray) or macular degeneration (MD) participant (black). Data for trials in the head-unrestrained condition are designated with open symbols. Black arrows indicate target direction. C: single head-unrestrained horizontal smooth pursuit trial for participant P6 (gray dashed arrow in B). Top: position. Bottom: velocity data. Dashed black line: head, dotted black line: eye in head, solid black line: eye in space (gaze), and gray line: target. Region designated by gray rectangles was chosen as period of longest continuous pursuit for the given trial.

Fig. 4.

Head movement during smooth pursuit. A: total mean head displacement across the entire trial normalized by total target displacement. B: mean peak head velocity during the period of longest continuous pursuit. Sign corresponds to target direction; gray dashed lines demarcate target velocity. Black circles: participants with macular degeneration; gray: controls. Black and gray horizontal bars mark median values for each distribution.

Fig. 5.

Eye displacement during pursuit. A and C: macular degenerations (MDs; A) and controls (C) show eye displacement across the entire ramp portion of the trial during head-unrestrained smooth pursuit. Columns correspond to: total eye displacement (Eye_Tot), eye displacement due to saccades only (Eye_Sac), eye displacement due to smooth pursuit only (Eye_Pur), head displacement (Head_Tot), and total displacement due to eye and head motion (Total), respectively. B and D: MDs (B) controls (D) show eye displacement during head-restrained smooth pursuit. Columns correspond to: total eye displacement, eye displacement due to saccades only, and eye displacement due to smooth pursuit only. Each color corresponds to a given participant. Data are averaged across all trials, all directions; error bars are SE. E: comparison of total gaze (eye and head) displacement due to smooth pursuit alone during head-unrestrained (open) and head-restrained (solid) conditions across target trajectories for individuals with macular degeneration (black) and controls (gray). F: comparison of total eye-in-space displacement (smooth pursuit + saccades), organized as described in E. All data are normalized by target displacement. Dashed gray lines in E and F indicate equal eye and target displacement.

Fig. 6.

Relationship between preferred retinal locus (PRL) eccentricity and head (black circle) and total eye and head (gray square) displacement across the trial. Error bars are SD.