Abstract
Purpose:
Research on infantile nystagmus syndrome (INS) and velocity discrimination is limited, and no research has examined velocity discrimination in subjects with INS at their null position and away from it. This study aims to investigate how individuals with INS perform, compared with controls, when carrying out velocity discrimination tasks. Particularly, the study aims to assess how the null position affects their performance.
Methods:
INS subjects (N = 21, mean age 24 years; age range, 15–34 years) and controls (N = 16, mean age 26 years; age range, 22–39 years) performed horizontal and vertical velocity discrimination tasks at two gaze positions. Eighteen INS subjects were classified as idiopathic INS and three had associated visual disorders (two had oculocutaneous albinism, and one had congenital cataract). For INS subjects, testing was done at the null position and 15° away from it. If there was no null, testing was done at primary gaze position and 15° away from primary. For controls, testing was done at primary gaze position and 20° away from primary. Horizontal and vertical velocity discrimination thresholds were determined and analyzed.
Results:
INS subjects showed significantly higher horizontal and vertical velocity discrimination thresholds compared with controls at both gaze positions (P < 0.001). Horizontal thresholds for INS subjects were elevated more than vertical thresholds (P < 0.0001) for INS subjects but not for controls. Within the INS group, 12 INS subjects who had an identified null position showed significantly lower horizontal and vertical thresholds at the null than at 15° away from it (P < 0.05).
Conclusions:
Velocity discrimination was impaired in INS subjects, with better performance at the null. These findings could assist in understanding how INS affects the daily activities of patients in tasks involving moving objects, and aid in developing new clinical visual function assessments for INS.
Infantile nystagmus syndrome (INS) is an involuntary, constant, rhythmic eye oscillation which usually presents at or near birth and persists throughout life. Its waveform parameters can vary with gaze angle, leading many patients to the adoption of an abnormal head posture to enhance their vision.
1 The gaze position with minimal nystagmus intensity and better visual performance is known as the null position.
1–7 Nearly all the research on vision in INS has focused on static visual acuity and the time needed to get the eyes onto the desired target (i.e., target acquisition time).
8–13 While these are important properties, they are not sufficient to reveal more complex visual functions entailed in real-life visual activities. Therefore, it is important to study how individuals with INS perform when they carry out a range of visual tasks and to examine how performance is influenced by the variability of INS at different gaze positions.
4,10,11,14
In everyday life, we are constantly presented with objects in motion. These moving objects require us to identify them and to estimate their speed of motion. For example, when driving a car merging into traffic, accurate estimation of velocity difference between vehicles on the main road is crucial to avoid accidents. This real-life visual activity demands accurate velocity discrimination.
To date, only one previous study by Shallo-Hoffmann et al.
15 has investigated motion perception deficits in INS using a (vertical) discrimination task and a (horizontal and vertical) detection task. In the discrimination task, subjects were asked to indicate if test and reference gratings that moved vertically had the same or different velocities. The reference velocity was fixed (1, 3, or 6°/s), while the test velocities varied (either matched the reference velocity or being slower or faster by 15% or 30% of the reference velocity). The discrimination thresholds of accuracy were recorded and analyzed. In the detection task, subjects were required to identify the drift direction of either a vertically or horizontally moving grating. The detection thresholds were recorded and compared. Overall, findings from the study suggested that subjects with congenital nystagmus showed poorer discrimination performance (i.e., higher discrimination accuracy thresholds) compared to controls, and they had higher motion detection thresholds when the motion was parallel to nystagmus eye movements. However, in their study, the investigators did not measure the velocity difference discrimination threshold, which is essential for accurate velocity estimation. In addition, they did not evaluate the effect of gaze at subjects’ null positions or elsewhere on velocity discrimination performance.
The null position in INS is of interest since it is possible to have different performance at the null position or at some specific distance away from it. A recent study by Fadardi et al.
14 demonstrated that increased cognitive demands can affect visual acuity of INS subjects, and the performance differed between different gaze positions. From low to high cognitive demand, the deterioration of acuity was greater for INS subjects at the null position compared to 15° away from it. The authors suggested that the larger effects at the null position might be due to the maximal foveation period duration at the null position, which allows more scope to deteriorate than at 15° away from it, where foveation may already be minimal. Thus, the null position in INS allows better performance at it than elsewhere.
In the present study, we investigated how individuals with INS perform velocity discrimination tasks. Particularly, we assessed how the null position affects their performance. To achieve this, we analyzed velocity discrimination thresholds at two different gaze positions for INS and control subjects. Three hypotheses were tested: 1) INS subjects will perform poorly compared to controls in velocity discrimination tasks; that is, INS subjects have higher velocity discrimination thresholds than controls; 2) Thresholds will be elevated more when the velocity discrimination task was performed in the same plane as the nystagmus; that is, INS subjects have higher horizontal than vertical velocity discrimination thresholds; 3) The null position in INS subjects will have a positive effect on velocity discrimination performance.
At the beginning of the task, a five-point pop-up calibration sequence (four around the periphery and one at the center of the screen) was performed binocularly. No validation procedure was performed. A chinrest and forehead rest were used to stabilize the head of subjects. Investigators also monitored the participants during the whole testing procedure to ensure that their heads were stabilized. For subjects with INS, it is not always possible to have their calibrations validated since they are unable to fixate the targets stably for a sufficient period of time. In this case, the calibration was performed by a normally sighted calibrator. This has been reported to be a simple and easily applicable way to get relatively more accurate results compared with other alternative calibration methods.
21 The calibration performed is sufficient for this study because the eye movement recordings were mainly used to confirm the diagnosis of INS, and to identify the presence and location of the null position. Once calibration was completed, the INS subject was required to fixate on a dot presented horizontally across ±20° from the center in 5° steps on the computer screen. Each gaze position was tested twice from right to left and then vice versa, with each presentation lasting for five seconds. Characteristics of INS waveform at the null position and 15° away from it are shown in
Table 2. The gaze position with the least nystagmus intensity during this test was determined as the null position.
22,23 Following this, all subjects were required to perform the velocity discrimination tasks.
Table 2. Characteristics of INS Waveform
Table 2. Characteristics of INS Waveform
Two velocity discrimination tasks were performed to measure the subject's velocity discrimination thresholds: 1) horizontal velocity discrimination task (gratings moving leftward or rightward); 2) vertical velocity discrimination task (gratings moving upward or downward). Within each task, velocity discrimination thresholds were measured at two gaze positions. For INS subjects with identified null positions, they performed at their null position and 15° away from it (either toward left or right). If the null position was in lateral gaze (±10°, ±15°, or ±20°), the 15° away position was in the opposite direction to it. If the null position was at or near primary gaze (0° or ±5°), the 15° away from null position was either toward left or right. For INS subjects without identified null positions, they performed at primary (straight-ahead) gaze position and 15° eccentric position (either toward left or right). For control subjects, testing was done at primary (straight-ahead) gaze position and a 20° eccentric position (either toward left or right). The order of the two tasks was randomized, and within each task, the gaze positions were randomized.
For both tasks, each trial began when subjects were asked to fixate a black fixation dot (1.44° × 1.44° of visual angle). Following the fixation dot, subjects viewed a pair of gratings moving in the same direction, which were presented successively at different velocities. Each grating was presented for 650 ms, and the interval between the two gratings was 500 ms. After viewing the two gratings, subjects were asked to indicate which of the two gratings moved faster by pressing one of two designated buttons on the keyboard. Each response elicited an audio tone from the program. A correct response generated a high tone, and an incorrect response generated a low tone. Subjects were instructed about these tones so that they could be encouraged to be accurate and be alert. The threshold of each subject's motion perception was measured by a three-down/one-up two-alternative forced-choice staircase procedure to estimate the 79.4% correct velocity difference discrimination.
24 The velocity of the reference grating was 5°/s. The initial velocity of the faster grating was set at 10°/s, which was a 100% velocity difference. The velocity difference between successive stimuli then was decreased by 30% of the current level if the subjects made three consecutive correct responses or increased by 30% of the current level if a single incorrect response was made. The experimental session terminated after eight reversals of staircase directions. The velocity discrimination thresholds were determined by a Weber fraction (ΔV/V), of which ΔV is defined as the just-noticeable difference between two gratings and V is the reference velocity of the stimuli. The threshold was calculated by the last six of eight reversal point values of the Weber fraction (ΔV/V).
Before formal testing began, each subject received several practice trials to ensure they understood the task procedure. The practice trials started from 100% velocity difference of which the faster grating was easy to detect. Subjects were also told the task would become harder, and that it was important that they tried their utmost to identify which one moved faster and pressed the key as accurately as possible. However, if some trials of the task were too difficult for them to discriminate which one moved faster, they were instructed to guess.
The velocity discrimination thresholds measured by horizontal and vertical tasks were analyzed for control subjects (primary gaze (straight-ahead) and 20° eccentricity), and INS subjects (primary gaze (null or straight-ahead if no null present), and 15° eccentricity). One outlier was removed from leftward discrimination threshold data at primary gaze position for INS subjects. The thresholds are shown in percentage of Weber fraction (ΔV/V (%)). Data were presented as mean ± SD%.
When comparing the discrimination thresholds between control and INS subjects, a 2-way mixed ANOVA showed that the INS subjects had significantly higher horizontal (right and left) (37.59 ± 18.56%) and vertical (up and down) (28.12 ± 12.40%) thresholds than the control subjects (horizontal: 19.85 ± 10.06%, vertical: 19.75 ± 9.39%) at both primary and eccentric gaze positions (
Fig. 3 and
Fig. 4) (Primary:
F [1, 35] = 16.30,
P = 0.0003; Eccentric:
F [1, 35] = 15.34,
P = 0.0004).
As this study aimed to investigate the effect of the null position on velocity discrimination in INS, the INS group was further divided into two subgroups: 1) 12 INS subjects with a null (subgroup A), 2) Nine INS subjects without a null (subgroup B). A 2-way repeated-measures ANOVA showed that subgroup A had significantly lower horizontal (27.00 ± 7.90%) and vertical (23.08 ± 8.58%) thresholds at the null position than at 15° away from it (horizontal: 37.61 ± 18.08%, vertical: 28.89 ± 9.23%) (
Fig. 3 and
Fig. 4) (Horizontal:
F [1, 11] = 7.859,
P = 0.0172); Vertical:
F [1, 11] = 8.035,
P = 0.0162). For subgroup B and the control group, 2-way repeated-measures ANOVAs showed no differences between different gaze positions (Subgroup B:
F [1, 8] = 1.407,
P = 0.2695, Control group:
F [1, 15] = 2.656,
P = 0.1240).
When comparing horizontal and vertical thresholds within INS and control subjects, a 2-way repeated-measures ANOVA revealed the INS subjects had significantly higher horizontal thresholds compared to vertical thresholds at both primary and eccentric gaze positions (
Fig. 5) (
F [1, 41] = 24.99,
P < 0.0001). There were no differences for the control subjects (
F [1, 31] = 0.006949,
P = 0.9341).
Since the INS subjects had their nystagmus only in the horizontal plane, thresholds measured in the horizontal task (right and left) were compared with regard to the nystagmus slow phase direction for INS subjects. Thirteen INS subjects at primary gaze and 16 INS subjects at eccentric gaze had pure jerk left or right nystagmus that were analyzable (see
Table 2 for data presentation). A two-tailed paired
t-test showed that when stimulus motion was in the same direction as the nystagmus slow phase, thresholds (38.34 ± 19.67%) were not significantly different from the thresholds of when stimulus motion direction was opposite to the nystagmus slow phase direction (38.08 ± 21.38%) (
Fig. 6) (
t[28] = 0.09718,
P = 0.9233).
The effect of visual acuity on velocity discrimination thresholds was investigated. Pearson correlation and linear regression analyses showed no correlation between acuity and velocity discrimination thresholds in INS subjects (horizontal thresholds: r = 0.1676, P = 0.4801, vertical thresholds: r = 0.3034, P = 0.1934). This result demonstrated that visual acuity of INS subjects did not affect their velocity discrimination thresholds.
As hypothesized, INS subjects showed poorer velocity discrimination performance (i.e., elevated velocity discrimination thresholds) compared to controls for both horizontal and vertical motion directions.
Though the findings in the present study were partly in agreement with Shallo-Hoffmann et al.,
15 the method of obtaining the discrimination thresholds was different. Shallo-Hoffmann et al.
15 measured the accuracy of group responses of velocity discrimination and estimated discrimination thresholds by fitting a Gaussian curve to group responses. In the present study, we measured the Weber fraction for each subject and assessed discrimination thresholds by using a staircase psychophysical method.
In the study by Shallo-Hoffmann et al.,
15 they suggested that the poorer performance of congenital nystagmus subjects compared to controls may be attributed to a mechanism that may be used to avoid oscillopsia at a cost of sensitivity to motion in INS subjects. Hence, it can be speculated that the mechanism of oscillopsia suppression could be a possible explanation for the elevated velocity discrimination thresholds of INS subjects in our study.
For INS subjects, despite having incessant retinal image motion, they rarely report oscillopsia. Several mechanisms have been proposed to account for this perceptual stability in INS subjects. A most widely accepted mechanism of oscillopsia suppression is that retinal image motion is canceled by an efferent copy of the extraretinal signal.
26,27 Extraretinal signals have been demonstrated to accompany involuntary eye movements in individuals with INS.
27 These extraretinal signals were proposed to play a role in alleviating motion smear in subjects with INS and contribute to the absence of oscillopsia in INS.
27
Bedell et al.
26 assessed the extraretinal signal in four subjects with nystagmus by requiring them to point in the direction of a flashed target in darkness when presented at various phases of the nystagmus waveform. They reported that extraretinal signals were available for approximately 75% of the eye position changes in INS and suggested that the extraretinal signals contributed to the oscillopsia suppression. In another study, Bedell
27 evaluated visual performance in persons with INS and normal observers when presented with similar retinal image motion (e.g., target moved at 8°/s). Normal observers reported profound target movement and motion smear, while persons with congenital nystagmus perceived a relatively stable and clear visual world. These differences were attributed to the extraretinal signals that accompany the involuntary eye oscillations reducing the motion smear in subjects with INS.
Another proposed mechanism of oscillopsia suppression is the elevation of the motion detection threshold.
28 It has been reported by Dieterich et al.
29 that individuals with INS had elevated thresholds for detecting motion at peripheral and central locations compared to controls. Shallo-Hoffmann et al.
15 also demonstrated that, when identifying the drift direction of a horizontally moving grating, INS subjects showed elevated detection thresholds. Leigh et al.
28 induced oscillopsia in four INS subjects by stabilizing images on the retina under different conditions and suggested that several mechanisms operate to maintain perceptual stability in INS. Possible mechanisms included the use of extraretinal signals to cancel out the effects of eye motion and the elevation of the motion detection threshold.
In summary, the various proposed mechanisms of oscillopsia suppression are suggested to operate together to reduce the sensitivity of externally caused retinal motion in INS subjects. This would lead to difficulty in detecting the difference in target velocity, hence resulting in elevated velocity discrimination thresholds in INS subjects.
Poorer Horizontal Than Vertical Velocity Discrimination Performance in INS Subjects
The authors thank Taliesyn Nicholas for writing the software for the psychophysics tasks in this study.
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Disclosure: B. Dai, None; K.M. Cham, None; L.A. Abel, None