Abstract
Purpose.:
To investigate oculomotor strategies in strabismic amblyopia and evaluate abnormalities during monocular and binocular reading.
Methods.:
Eye movements were recorded with a head-mounted infrared video eye-tracker (250 Hz, <0.01° resolution) in 20 strabismic amblyopes (mean age, 44.9 ± 10.7 years) and 20 normal control subjects (mean age, 42.8 ± 10.9 years) while they silently read paragraphs of text. Monocular reading comparisons were made between the amblyopic eye and the nondominant eye of control subjects and the nonamblyopic eye and the dominant eye of the control subjects. Binocular reading between the amblyopic and control subjects was also compared.
Results.:
Mean reading speed, number of progressive and regressive saccades per line, saccadic amplitude (of progressive saccades), and fixation duration were estimated. Inter- and intrasubject statistical comparisons were made. Reading speed was significantly slower in amblyopes than in control subjects during monocular reading with amblyopic (13.094 characters/s vs. 22.188 characters/s; P < 0.0001) and nonamblyopic eyes (16.241 characters/s vs. 22.349 characters/s, P < 0.0001), and binocularly (15.698 characters/s vs. 23.425 characters/s, P < 0.0001). In amblyopes, reading was significantly slower with the amblyopic eye than with the nonamblyopic eye in binocular viewing (P < 0.05). These differences were associated with significantly more regressive saccades and longer fixation durations, but not with changes in saccadic amplitudes.
Conclusions.:
In strabismic amblyopia, reading is impaired, not only during monocular viewing with the amblyopic eye, but also with the nonamblyopic eye and binocularly, even though normal visual acuity pertains to the latter two conditions. The impaired reading performance is associated with differences in both the saccadic and fixational patterns, most likely as adaptation strategies to abnormal sensory experiences such as crowding and suppression.
Amblyopia is the single most common visual deficit affecting visual acuity (VA) in childhood, with a prevalence estimated between 1.0% and 4.0%.
1 It consists of reduced VA in the absence of organic disease, caused by unequal visual stimulation between the eyes, most commonly due to strabismus or refractive error. Amblyopia is also one of the most common causes of persistent unilateral visual loss in adults. The impact of amblyopia is significant on visual acuity, as well as on other visual dysfunctions associated with this visual disorder.
2
Reading is a key visual task related to daily living, but surprisingly the impact of amblyopia on reading ability has been poorly investigated. Eye movement recording techniques have contributed greatly to our understanding of the processes underlying reading.
3 Although eye movement recordings have also been used to investigate reading after disease that affects the visual system
4,5 as well as in aging,
6 these techniques have never been applied in the investigation of reading in amblyopia.
Reading is frequently included in assessments of visual function. In many visual disorders, including amblyopia, reading speed measurements provide more information about visual impairment than recording visual acuity alone. In fact, Zürcher and Lang
7 recommend that patching treatment continue until reading ability recovers, rather than just using visual acuity to determine a successful outcome. By recording the time taken to read a fixed amount of text, Stifter et al.
8 showed that in children with microstrabismic amblyopia, the maximum reading speed with the amblyopic eye (139.4 ± 42.1 words per minute [wpm]) was significantly impaired compared with that of either eye of normally sighted children (189 ± 15.6 wpm for the right eye, 191.1 ± 18.8 wpm for the left eye). During binocular reading, Stifter et al. also found that amblyopic children had reduced maximum reading speed (172.9 ± 43.9 wpm) compared with that of normal children (200.4 ± 11 wpm). Also, in amblyopes, maximum reading speed was significantly impaired in the amblyopic eyes compared with the nonamblyopic eyes (172.4 ± 46.7 wpm). Anisometropes have been reported to show similar deficits (Osarovsky-Sasin E, et al.
IOVS 2002;43:ARVO E-Abstract 4691). To our knowledge, however, no study has yet been performed in which eye movement patterns associated with reduced reading ability were investigated in amblyopia.
In our study, we sought to evaluate for the first time the oculomotor characteristics associated with impaired reading performance in adult strabismic amblyopia and to corroborate previous findings in which reading deficits resulting from amblyopia have been described.
A full ophthalmic examination including assessment of distance VA (logMAR crowded acuity tests), binocular function (Bagolini striated glasses test), stereopsis/stereoacuity (TNO test), ocular motility examination, cover/uncover and alternate cover test, slit lamp examination, and direct ophthalmoscopy was performed on all subjects. None of the amblyopic subjects demonstrated stereo vision. Twelve of the amblyopic volunteers showed total suppression with the Bagolini test, and eight showed central suppression only. The control (normal) subjects showed no suppression, with mean stereo acuity of 60 min arc. Each subject wore optimal correction for all clinical vision tests and reading trials.
All the participants were native English speakers and naïve to eye movement experiments. The study fulfilled the tenets of the Declaration of Helsinki and was approved by the local ethics committee. Written, informed consent was obtained from all the subjects.
The subjects were required to read nine paragraphs of continuous text in an excerpt from the English translation of the Brothers Grimm fairy tale, “Tom Thumb.”
10 Each paragraph had on average a width of 775 mm and height of 466 mm, and subtended a visual angle of 35.8° width and 22.0° height. Each paragraph had approximately the same layout, consisting of 13.11 ± 0.39 lines, 178.6 ± 8.72 words, and 900.6 ± 28.7 characters with spaces with 1.5 interline spacing resulting in 13.62 ± 0.37 words per line and 68.75 ± 0.83 characters with spaces per line. The text was presented on a rear projection screen (1.75 m width and 1.17 m height) as black letters (luminance = 0.88 cd/m
2) on a white background (luminance = 14.3 cd/m
2) with a letter contrast of 93.84%. Only the left-hand side of each line was justified. The text was displayed in Courier New fixed-width font (monospaced), nine-point size, with no hyphenated words and was centered on the screen horizontally and vertically. The print size, measured as the height of the lowercase x, corresponded to visual acuity of 0.735 in logMAR optotype (calculated from the equation log
10 [(angle subtended by
x − height)/(5 arc min)] see Ref.
11). Patients were included if they had a visual acuity 1 logMAR line better than the font size (i.e., visual acuity better than 0.635 logMAR). They were tested as to whether they could read this font size before the investigation commenced.
The subjects were seated at a viewing distance of 1.20 m in front of the stimulus display screen with the head stabilized with a chin rest. The primary position of gaze corresponded to the screen's center. The participants were instructed to read at the rate necessary to understand the text and to read silently, as jaw movements introduce artifacts in eye movement data by causing vibration of the head-mounted eye tracker. After the participants reported reading each paragraph, comprehension was checked by having them answering two multiple-choice questions relevant to the text with 18 questions in total. All subjects answered the questions correctly, demonstrating a good level of understanding of the content.
All investigations were performed in random order, both binocularly and during monocular reading. During monocular reading, the contralateral eye was occluded with a black opaque occluder. The test duration was approximately 1 hour.
Differences between amblyopes and control subjects were assessed by using univariate ANOVA (SPSS ver. 14.0; SPSS, Chicago, IL), including age, sex, and NART score as factors. The following comparisons were made: monocular reading with the amblyopic eye of the amblyopes and the nondominant eye of the control subjects, monocular reading with the nonamblyopic eye of the amblyopes and the dominant eye of the control subjects, and binocular reading in both the amblyopes and the control subjects. During binocular viewing, eye movement from the dominant/nonamblyopic eye was used. Repeated-measures ANOVAs were conducted to evaluate the intrasubject differences in the amblyopes during monocular and binocular viewing conditions.
Our findings indicate that in strabismic amblyopia reading is impaired, not only during monocular viewing with the amblyopic eye, but also with the nonamblyopic eye and during binocular viewing, even though visual acuity is usually normal in the latter two conditions. We also show for the first time that these reading deficits are associated with distinct differences in oculomotor patterns, in particular, an increased number of regressive saccades and prolonged fixation durations.
Our findings describe for the first time the oculomotor patterns associated with the reduced reading speed in amblyopia compared with that of control subjects—namely, the increased number of regressions and the prolonged fixation duration. To some degree, the oculomotor patterns in the amblyopes resemble those observed during reading in normal individuals with simulated central scotomas and in patients with central field loss.
Reading performance is determined by the size of the visual
30 and the perceptual span.
15 When the center of the visual field is obscured, reading speed declines, and the eye movement pattern changes.
18 In simulations of central scotomas in which the eye-contingent display change technique was used to create foveal masks, Rayner et al.
15 found that increasing the mask size resulted in an increase in the number of progressive and regressive saccades and the fixation duration in normally sighted observers. Fine and Rubin
16 also found an increased number of saccades and extended fixation durations. In addition, McMahon et al.
31 concluded that higher saccadic frequencies were significantly associated with reduced reading rates in patients with age-related macular degeneration. They suggested that the reduced visual span results in poor saccadic accuracy and a subsequent increase in the number of saccades to reach the visually presented stimulus.
The visual information necessary for reading in normal reading conditions can be perceived within the first 50 ms during a fixation.
3 Since a fixation lasts on average 200 to 250 ms, it appears that the remaining time is used to program the next eye movement and to integrate characteristics of the text using high-level cortical processes. Failure to perform these tasks leads to extended fixation durations. This assumption is consistent with the oculomotor adaptations observed in patients with central field loss.
5 Regressive saccades are associated with problems with linguistic processing as well as oculomotor errors. In our investigation, any potential difficulty with linguistic processing was minimized by using reading material below the reading ability of the participants. Furthermore, NART scores were matched between the amblyopes and the control subjects indicating an equivalent intellectual level in the two groups. It is possible therefore, that the higher number of regressions in amblyopes is associated with difficulties in programming the subsequent saccade.
As far as we are aware, this is the first systematic study of eye movements in adult amblyopes during reading. Future exploration may include investigation of oculomotor deficits in amblyopic children during reading and whether improvements in visual acuity during patching (monitored with occlusion dose monitors for example) lead to changes in oculomotor reading strategies. Care would need to be taken to control for natural changes in reading speed that occur at this period of development. The present findings are limited to strabismic and mixed amblyopes and consequently do not distinguish the effects of amblyopia on reading per se from the effects of strabismus. It would be interesting to look at the effect of reading on anisometropic amblyopes, to further explore this question. We have taken persons with mild to moderate amblyopia who could read the fixed font size used in this experimental design. There is merit to using a range of font sizes to examine more severely amblyopic patients, to compare reading strategies relative to impairment in visual acuity.
The use of matched NART groups in this study controlled for differences in cognitive ability between the amblyopic and nonamblyopic volunteers. The result is that any differences in reading in our study are due to the reading deficits imposed by visual and oculomotor deficits caused by (strabismic) amblyopia rather than by any associated cognitive impairments. However, several studies indicate that strabismic amblyopia can be associated with cognitive impairments for example in children who are born prematurely (or very preterm).
32,33 The combination of cognitive and visuomotor deficits is likely to lead to reduced scholastic performance in amblyopes. The effect of cognitive impairments on reading ability could be investigated by more extensive testing of cognitive ability than the NART which includes nonverbal measures of cognitive function.