July 2010
Volume 51, Issue 7
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Eye Movements, Strabismus, Amblyopia and Neuro-ophthalmology  |   July 2010
Reading Strategies in Mild to Moderate Strabismic Amblyopia: An Eye Movement Investigation
Author Affiliations & Notes
  • Evgenia Kanonidou
    From the Ophthalmology Group, University of Leicester, Faculty of Medicine & Biological Sciences, Leicester Royal Infirmary, Leicester, United Kingdom.
  • Frank A. Proudlock
    From the Ophthalmology Group, University of Leicester, Faculty of Medicine & Biological Sciences, Leicester Royal Infirmary, Leicester, United Kingdom.
  • Irene Gottlob
    From the Ophthalmology Group, University of Leicester, Faculty of Medicine & Biological Sciences, Leicester Royal Infirmary, Leicester, United Kingdom.
  • Corresponding author: Irene Gottlob, Ophthalmology Group, University of Leicester, Faculty of Medicine & Biological Sciences, Robert Kilpatrick Clinical Sciences Building, Leicester Royal Infirmary, PO Box 65, Leicester, LE2 7LX, UK; ig15@le.ac.uk
Investigative Ophthalmology & Visual Science July 2010, Vol.51, 3502-3508. doi:10.1167/iovs.09-4236
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      Evgenia Kanonidou, Frank A. Proudlock, Irene Gottlob; Reading Strategies in Mild to Moderate Strabismic Amblyopia: An Eye Movement Investigation. Invest. Ophthalmol. Vis. Sci. 2010;51(7):3502-3508. doi: 10.1167/iovs.09-4236.

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      © ARVO (1962-2015); The Authors (2016-present)

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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. 
Methods
Subjects
Twenty patients (mean age, 44.9 ± 10.7 years) were recruited from ocular motility clinics in the Department of Ophthalmology, Leicester Royal Infirmary. All had a diagnosis of unilateral amblyopia caused by strabismus, defined as a minimum two-line interocular difference in distance visual acuity (logMAR). Mean VA in the amblyopic eye was 0.332 ± 0.153 logMAR and in the fellow eye −0.061 ± 0.053 logMAR. A control group of 20 volunteers also participated in the study. All had normal visual acuity and did not have any neurologic or psychiatric disease or other ocular comorbidity. 
The two study groups were comparable in age (P = 0.545), sex, and educational–intelligence level, matched by using the National Adult Reading Test (NART) (P = 0.312). 9 The NART involves correctly pronouncing a series of single words that are all irregular, with respect to the common rules of pronunciation. There is no time limit. 
The clinical details of the tested amblyopes and control subjects are summarized in Tables 1A and 1B. 
Table 1.
 
Clinical Details of the Participants
Table 1.
 
Clinical Details of the Participants
A. Amblyopes
ID Age Sex NART Deviation Visual Acuity (Viewing Eye) Fixation Bagolini Suppression Treatment
Amblyopic Nonamblyopic Binocular
1 47 M 105 R exotropia 0.475 0.000 0.000 Parafoveal Total Surgery
2 43 F 105 R esotropia 0.325 0.000 0.000 Foveal Total Surgery
3 48 F 106 L esotropia 0.475 0.000 0.000 Foveal Central Patching/surgery
4 38 M 114 R esotropia 0.125 −0.150 −0.150 Foveal Central Patching
5 64 F 106 L exotropia 0.200 −0.075 −0.075 Foveal Total Patching/surgery
6 58 F 109 R esotropia 0.250 0.000 0.000 Foveal Total Surgery
7 45 F 105 L esotropia 0.575 0.000 0.000 Parafoveal Total Patching
8 24 F 103 L esotropia 0.175 −0.075 −0.075 Foveal Central Patching/surgery
9 49 F 112 L exotropia 0.175 −0.075 −0.075 Foveal Total Patching/surgery
10 30 F 109 R exotropia 0.175 −0.075 −0.075 Foveal Central Surgery
11 51 M 114 L exotropia 0.200 −0.050 −0.050 Foveal Total Surgery
12 51 M 117 R exotropia 0.475 −0.175 −0.175 Foveal Central Patching
13 58 F 104 R esotropia 0.300 0.000 0.000 Foveal Total Patching/surgery
14 48 F 122 L exotropia 0.475 −0.075 −0.075 Foveal Total Patching/surgery
15 54 M 103 L exotropia 0.500 −0.100 −0.100 Foveal Central Patching/surgery
16 36 F 102 L exotropia 0.325 −0.100 −0.100 Foveal Total Patching/surgery
17 25 F 105 L exotropia 0.575 −0.100 −0.100 Foveal Central Patching/surgery
18 40 M 107 R exotropia 0.175 0.000 0.000 Foveal Central Surgery
19 38 M 106 R exotropia 0.200 −0.100 −0.100 Foveal Total Patching/surgery
20 51 M 124 R exotropia 0.475 −0.075 −0.075 Parafoveal Total Patching/surgery
Mean 44.9 108.9 0.333 −0.061 −0.061
SD 10.8 6.3 0.154 0.053 0.053
B. Controls
ID Age Sex NART Deviation Visual Acuity (Viewing Eye)
Nondominant Dominant Binocular
21 47 F 113 orthophoria −0.025 0.000 0.000
22 32 M 107 orthophoria −0.100 −0.100 −0.100
23 24 F 105 orthophoria 0.000 0.025 0.000
24 27 M 103 orthophoria −0.050 −0.050 −0.050
25 50 F 105 orthophoria −0.025 −0.050 −0.050
26 47 M 117 orthophoria −0.025 −0.025 −0.050
27 50 F 114 orthophoria −0.050 −0.025 −0.025
28 46 M 117 orthophoria 0.000 −0.025 −0.025
29 26 M 106 orthophoria −0.050 −0.050 −0.050
30 40 M 121 orthophoria 0.000 −0.025 −0.025
31 60 F 119 orthophoria −0.025 0.000 −0.025
32 50 M 118 orthophoria 0.000 −0.050 −0.050
33 33 M 115 orthophoria 0.000 0.000 0.000
34 30 M 105 orthophoria −0.050 −0.250 −0.050
35 54 F 108 orthophoria −0.075 −0.100 −0.100
36 58 F 107 orthophoria 0.000 −0.050 −0.050
37 52 F 110 orthophoria −0.050 −0.025 −0.050
38 36 F 111 orthophoria −0.025 −0.025 −0.025
39 45 F 113 orthophoria −0.075 −0.025 −0.050
40 49 F 103 orthophoria −0.050 −0.050 −0.075
Mean 42.8 110.9 −0.034 −0.045 −0.043
SD 11.0 5.7 0.030 0.057 0.028
Vision Assessment
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. 
Reading Assessment
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/m2) on a white background (luminance = 14.3 cd/m2) 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 log10 [(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. 
Eye Movement Recordings
Gaze position was measured with an infrared, video-based pupil-tracking system (EyeLink Eye Tracker; SensoMotoric Instruments GmbH, Berlin, Germany). 12 The eye-tracker has a sample rate of 250 Hz, a spatial resolution of 0.005°, and a spatial accuracy of 0.5°, with a noise level of less than 0.01° RMS (root mean square). Calibration was performed monocularly with a series of nine fixation points (3 × 3 grid, 40° wide and 35° high) projected individually on the screen (VisLab projection system; SensoMotoric Instruments GmbH) and a video projector (resolution, 1024 × 768; CP-X958 LCD; Hitachi Ltd., Tokyo, Japan). Saccades were detected with an automatic saccade detection algorithm based on a velocity threshold of 35°/s and an acceleration threshold of 9500°/s2
Data Analysis
Eye movements were analyzed with semiautomated custom-written scripts (Spike2 software; Cambridge Electronic Design, Ltd., Cambridge, UK). Reading speed was calculated from the characters, with spaces for each paragraph of text divided by the time taken to read the paragraph. For other parameters, cursors were selected corresponding to each of the reading lines (from the middle of the first and last fixations of each line) during which the following parameters were measured (Fig. 1, inset): total number of saccades per line, number of progressive (forward) saccades per line, amplitude of progressive saccades (in degrees), number of regressive (backward) saccades per line, and fixation duration (seconds). Means were calculated for all parameters in each subject. 
Figure 1.
 
Original recordings of an amblyopic subject and a normal control subject during monocular viewing with either eye and binocular reading. In the selected period, fewer lines of text were read during monocular viewing with either eye and binocular viewing by the amblyopic subjects compared with the normal control subjects. Inset: the parameters measured from the eye movement recording for each line: the number of progressive saccades (open arrows), the amplitude of progressive saccades (APS), the number of regressive saccades (filled arrows), the total number of saccades per line (open and filled arrows) and fixation duration (FD).
Figure 1.
 
Original recordings of an amblyopic subject and a normal control subject during monocular viewing with either eye and binocular reading. In the selected period, fewer lines of text were read during monocular viewing with either eye and binocular viewing by the amblyopic subjects compared with the normal control subjects. Inset: the parameters measured from the eye movement recording for each line: the number of progressive saccades (open arrows), the amplitude of progressive saccades (APS), the number of regressive saccades (filled arrows), the total number of saccades per line (open and filled arrows) and fixation duration (FD).
Statistical Analysis
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. 
Results
Original recordings of the eye movement patterns recorded from an amblyope and a control for each of the viewing conditions are illustrated in Figure 1. A clear difference in reading speed between the two subjects is evident from the number of lines read in the time interval. Three to four lines were read by the amblyopes in each viewing condition, whereas five to six lines were read by the control subjects in the same period (16 seconds). 
Means of the reading speed and other oculomotor parameters (with standard deviations) are illustrated in Figure 2 for the amblyopes and the control subjects and data describing statistical comparisons are shown in Table 2. Mean reading speeds were significantly slower in the amblyopes than in the control subjects for all three viewing conditions (Table 2B, first column). Mean reading speed in the amblyopes was 55%, 72%, and 67% of that in the control subjects for amblyopic/nondominant eye viewing, nonamblyopic/dominant eye viewing, and binocular viewing, respectively (all highly significant, P < 0.0001). Paired comparisons of the data in amblyopes for each viewing condition (Table 2C) also demonstrated a clear difference in mean reading speed between amblyopic eye viewing and either nonamblyopic eye or binocular viewing. Reading speed with the amblyopic eye viewing was 81% of that with the nonamblyopic eye viewing (P < 0.0001) and 83% of that with binocular viewing (P = 0.01). There was no difference in binocular reading speed in relation to whether the amblyopic volunteers showed central or total suppression with the Bagolini test (t = −1.390, P = 0.181). 
Figure 2.
 
Mean and standard deviation (error bars) of the oculomotor parameters in the amblyopic subjects and the normal control subjects measured in each condition. Left: reading speed (characters with spaces/second), amplitudes of progressive/forward saccades, and fixation duration (seconds). Right: column shows number of progressive saccades per line, number of regressive saccades per line, and total number of saccades per line. *Significant differences (P < 0.05).
Figure 2.
 
Mean and standard deviation (error bars) of the oculomotor parameters in the amblyopic subjects and the normal control subjects measured in each condition. Left: reading speed (characters with spaces/second), amplitudes of progressive/forward saccades, and fixation duration (seconds). Right: column shows number of progressive saccades per line, number of regressive saccades per line, and total number of saccades per line. *Significant differences (P < 0.05).
Table 2.
 
Descriptive and Inferential Statistical Results for Each of the Oculomotor Parameters
Table 2.
 
Descriptive and Inferential Statistical Results for Each of the Oculomotor Parameters
A. Mean (±SD)
Group/Viewing Eve Reading Speed Saccades per Line (n) Amplitude of Prog. Saccades (deg) Fixation Duration (ms)
Char/s Words/min Progressive Regressive Total
Amblyopes
    Amblyopic 13.1 (±4.1) 156 (±49) 9.19 (±4.17) 2.78 (±1.50) 12.0 (±4.01) 3.82 (±1.35) 247 (±28)
    Nonamblyopic 16.2 (±3.3) 193 (±39) 9.59 (±2.29) 1.96 (±0.79) 11.5 (±2.52) 3.75 (±1.10) 234 (±26)
    Binocular 15.7 (±4.0) 187 (±48) 9.27 (±2.67) 2.43 (±1.02) 11.7 (±2.85) 3.64 (±1.07) 224 (±28)
Controls
    Nondominant 22.2 (±5.1) 264 (±60) 8.43 (±1.96) 1.57 (±0.75) 10.0 (±2.51) 4.17 (±0.83) 217 (±30)
    Dominant 22.3 (±5.7) 266 (±68) 8.20 (±2.15) 1.52 (±0.84) 9.7 (±2.68) 4.28 (±0.99) 217 (±29)
    Binocular 23.4 (±5.8) 279 (±70) 8.35 (±2.11) 1.60 (±0.82) 10.0 (±2.56) 4.31 (±0.85) 206 (±25)
B. Between-Subject Comparisons: P-value (F-statistic)
Viewing Eye (Group) Reading Speed Saccades per Line (n) Amplitude of Prog. Saccades (deg) Fixation Duration (ms)
Progressive Regressive Total
Amblyopic (amblyope) vs. nondominant (control) F = 38.9 F = 0.55 F = 10.4 F = 3.47 F = 0.94 F = 10.1
P < 0.0001* P = 0.47 P = 0.003* P = 0.070 P = 0.34 P = 0.003*
Nonamblyopic (amblyope) vs. dominant (control) F = 17.3 F = 3.89 F = 2.98 F = 4.93 F = 2.63 F = 2.23
P < 0.0001* P = 0.056 P = 0.092 P = 0.032* P = 0.11 P = 0.14
Binocular (amblyope) vs. binocular (control) F = 23.7 F = 1.44 F = 8.01 F = 4.12 F = 4.89 F = 4.33
P < 0.0001* P = 0.24 P = 0.007* P = 0.049* P = 0.053 P = 0.044*
C. Within-Subject Comparisons: P-value (F-statistic)
Viewing Eye (Group) Reading Speed Saccades per Line (n) Amplitude of Prog. Saccades (deg) Fixation Duration (ms)
Progressive Regressive Total
Amblyopic (amblyope) vs. nonamblyopic (amblyope) t = −4.26 t = −0.67 t = 2.86 t = 0.78 t = 0.27 t = 3.20
P < 0.0001* P = 0.51 P = 0.010* P = 0.45 P = 0.79 P = 0.005*
Amblyopic (amblyope) vs. binocular (amblyope) t = −2.80 t = −0.16 t = 1.378 t = 0.567 t = 0.585 t = 4.203
P = 0.011* P = 0.89 P = 0.18 P = 0.58 P = 0.57 P < 0.0001*
Nonamblyopic (amblyope) vs. binocular (amblyope) t = 1.16 t = 1.13 t = −3.177 t = −0.634 t = 1.052 t = 1.528
P = 0.259 P = 0.27 P = 0.005* P = 0.53 P = 0.31 P = 0.14
On examination of the probabilities in Table 2 across all comparisons the two most consistent oculomotor parameters that show significant differences associated with these changes in reading speed are the fixation duration (column 5, four of five comparisons that are significantly different for reading speed are also significantly different for fixation duration) and the number of regressive saccades per line (column 3, three of five comparisons that are significantly different for reading speed are also significantly different for number of regressions). In contrast, no significant differences were apparent for number of progressive saccades per line or amplitude of progressive saccades (although one comparison in each case was near significance). The total number of saccades per line was at or near significance (P < 0.05) for all three comparisons between amblyopes and control subjects but not for within-subject comparisons in amblyopes. 
For reading speed, the difference between means of amblyopes and control subjects was approximately double the standard deviation of the data for the amblyopes. However, for the oculomotor parameters the differences were more subtle, with the difference between means equivalent to one standard deviation or less of the amblyopic patients' distribution of values. The results indicate that the reduction in reading speed is due to the multifactorial influences of various oculomotor deficits with the combined effect leading to the reduced reading speed in amblyopia. 
Discussion
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. 
Reading Deficits in Amblyopes
Stifter et al. 8 also described reading speed impairments in children with microstrabismic amblyopia during monocular reading with the amblyopic eye and binocularly. During reading with the amblyopic eye, these children achieved 73% and 72% of the reading rates exhibited in normally sighted children with either eye viewing. During binocular reading, amblyopic children achieved a reading speed equivalent to 80% of the reading speed of normally sighted children. In our reading task, reading speed with the amblyopic eye viewing was lower, equivalent to 55% of the reading speed of the nondominant eye and 56% of the dominant eye of the normal subjects. Binocular reading speed in our amblyopes was also lower, representing 67% of the normal binocularly reading rate. However, Stifter et al. found no significant differences in monocular reading with the nonamblyopic eye, with the amblyopic children achieving approximately 90% of the reading speed of the normally sighted children. By contrast, in our reading experiment, reading speed with the nonamblyopic eye was significantly impaired, equivalent to 72% of the reading speed achieved with the dominant eye. These discrepancies may be related to differences in the type of strabismic patients included in the study (Stifter et al. included only microstrabismic volunteers). Another difference was in the experimental designs used to evaluate reading performance. Stifter et al. used the Radner reading chart, comprising short sentences read aloud as quickly as possible by the children. In comparison, our reading material consisted of longer paragraphs of text, which the adults read silently at their own pace but with the intention of comprehending the passage. These differences are likely to explain the higher reading speeds recorded in amblyopes and control subjects observed in this study design (mean reading speed was 179 words per minute in amblyopes and 270 words per minute in control subjects) compared to using the Radner reading chart (mean reading speed for equivalent font size was approximately 125 words per minute in amblyopes and 155 words per minute in control subjects). 8 The differences in reading speed may be due to our use of adult subjects compared to the use of children by Stifter et al. 
We found that reading speed was significantly impaired with the amblyopic eye viewing, compared with the nonamblyopic eye and binocular viewing. Stifter et al. have also reported a significant mean interocular difference of 33 ± 19 wpm in children with microstrabismic amblyopia. 13 It was interesting to note that 8 of the 22 children included in their study showed no significant interocular difference in the best-corrected VA. This result indicates that effective improvement of visual acuity after treatment for amblyopia does not necessarily imply that other deficits, such as reading ability have been adequately treated. 
The reading deficit associated with binocular viewing in amblyopes may be related to the presence of suppression scotomas. 14 In several studies, researchers have investigated the effects of simulated central scotomas in normal individuals 15,16 and of pathologic scotomas caused by central field loss 4,5 on changes in reading speed. For example, Rayner et al. 15 showed that an artificial scotoma of even a one-letter-sized foveal mask caused a reduction in reading speed to one-half its normal value. These observations do not compare directly with our findings, since these experiments were performed during monocular viewing, whereas suppression scotomas are present only during binocular viewing. 
The crowding effect 17 may further contribute to the reduced reading rates observed in the amblyopes. It has been suggested that crowding underlies reduced reading speeds in normal peripheral vision compared with central vision. 18 Recently, Levi et al., 19 using the rapid serial visual presentation technique, suggested that reading rates in amblyopic vision are dependent on letter spacing. However, Chung 20,21 argued that vertical word spacing is a more important factor. An interesting future research project would be to investigate reading speeds and oculomotor patterns associated with changes in letter or word spacing. 
Surprisingly, our results indicated that monocular reading with the nonamblyopic eye of the amblyopes was significantly impaired compared with reading with the dominant eye of the control subjects, even though distance VA was comparable between the two groups. In strabismic amblyopia, sensory and oculomotor defects, similar to those that characterize the amblyopic eye, have been found to occur in the fellow, nondeviated eye. 1 These include unsteady and eccentric fixation, 22 smooth pursuit, 23 and optokinetic nystagmus asymmetry, 24,25 and small deficits in contrast sensitivity 26,27 and Vernier acuity. 28 Recently, Levi 17 also suggested an increased crowding effect in the nonamblyopic eye that might significantly affect reading rates. The impaired reading performance of the nonamblyopic eye may be related to previous occlusion of the good eye, leading to visual deficits not detected by changes in visual acuity. 29  
Oculomotor Patterns Observed during Reading
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. 
Clinical Implications of the Study
In terms of the clinical significance of the results during monocular viewing, amblyopic subjects have been found to be at an increased risk of visual impairment when trauma or disease affect the normal eye, leaving them to cope by relying on the amblyopic eye alone. 2 There is also a greater chance of severe bilateral vision loss in amblyopes (because of injury or trauma to the nonaffected eye) than in the general population. 34  
In clinical practice, the visual impairments and improvements in visual function in amblyopes are usually tracked with high-contrast visual acuity charts. Amblyopes may exhibit significant deficits in visual function after treatment for parameters such as contour integration, stability of fixation, low contrast perception, and motion detection, despite minor or absent deficits in high-contrast visual acuity. 35 Our findings support previous suggestions 7,8 that there may be some benefit in including standardized reading charts in the assessment of visual function in patients with strabismic amblyopia. 
Footnotes
 Supported by the Ulverscroft Foundation.
Footnotes
 Disclosure: E. Kanonidou, None; F.A. Proudlock, None; I. Gottlob, None
The authors thank Samira Anwar for a critical reading of the manuscript. 
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Figure 1.
 
Original recordings of an amblyopic subject and a normal control subject during monocular viewing with either eye and binocular reading. In the selected period, fewer lines of text were read during monocular viewing with either eye and binocular viewing by the amblyopic subjects compared with the normal control subjects. Inset: the parameters measured from the eye movement recording for each line: the number of progressive saccades (open arrows), the amplitude of progressive saccades (APS), the number of regressive saccades (filled arrows), the total number of saccades per line (open and filled arrows) and fixation duration (FD).
Figure 1.
 
Original recordings of an amblyopic subject and a normal control subject during monocular viewing with either eye and binocular reading. In the selected period, fewer lines of text were read during monocular viewing with either eye and binocular viewing by the amblyopic subjects compared with the normal control subjects. Inset: the parameters measured from the eye movement recording for each line: the number of progressive saccades (open arrows), the amplitude of progressive saccades (APS), the number of regressive saccades (filled arrows), the total number of saccades per line (open and filled arrows) and fixation duration (FD).
Figure 2.
 
Mean and standard deviation (error bars) of the oculomotor parameters in the amblyopic subjects and the normal control subjects measured in each condition. Left: reading speed (characters with spaces/second), amplitudes of progressive/forward saccades, and fixation duration (seconds). Right: column shows number of progressive saccades per line, number of regressive saccades per line, and total number of saccades per line. *Significant differences (P < 0.05).
Figure 2.
 
Mean and standard deviation (error bars) of the oculomotor parameters in the amblyopic subjects and the normal control subjects measured in each condition. Left: reading speed (characters with spaces/second), amplitudes of progressive/forward saccades, and fixation duration (seconds). Right: column shows number of progressive saccades per line, number of regressive saccades per line, and total number of saccades per line. *Significant differences (P < 0.05).
Table 1.
 
Clinical Details of the Participants
Table 1.
 
Clinical Details of the Participants
A. Amblyopes
ID Age Sex NART Deviation Visual Acuity (Viewing Eye) Fixation Bagolini Suppression Treatment
Amblyopic Nonamblyopic Binocular
1 47 M 105 R exotropia 0.475 0.000 0.000 Parafoveal Total Surgery
2 43 F 105 R esotropia 0.325 0.000 0.000 Foveal Total Surgery
3 48 F 106 L esotropia 0.475 0.000 0.000 Foveal Central Patching/surgery
4 38 M 114 R esotropia 0.125 −0.150 −0.150 Foveal Central Patching
5 64 F 106 L exotropia 0.200 −0.075 −0.075 Foveal Total Patching/surgery
6 58 F 109 R esotropia 0.250 0.000 0.000 Foveal Total Surgery
7 45 F 105 L esotropia 0.575 0.000 0.000 Parafoveal Total Patching
8 24 F 103 L esotropia 0.175 −0.075 −0.075 Foveal Central Patching/surgery
9 49 F 112 L exotropia 0.175 −0.075 −0.075 Foveal Total Patching/surgery
10 30 F 109 R exotropia 0.175 −0.075 −0.075 Foveal Central Surgery
11 51 M 114 L exotropia 0.200 −0.050 −0.050 Foveal Total Surgery
12 51 M 117 R exotropia 0.475 −0.175 −0.175 Foveal Central Patching
13 58 F 104 R esotropia 0.300 0.000 0.000 Foveal Total Patching/surgery
14 48 F 122 L exotropia 0.475 −0.075 −0.075 Foveal Total Patching/surgery
15 54 M 103 L exotropia 0.500 −0.100 −0.100 Foveal Central Patching/surgery
16 36 F 102 L exotropia 0.325 −0.100 −0.100 Foveal Total Patching/surgery
17 25 F 105 L exotropia 0.575 −0.100 −0.100 Foveal Central Patching/surgery
18 40 M 107 R exotropia 0.175 0.000 0.000 Foveal Central Surgery
19 38 M 106 R exotropia 0.200 −0.100 −0.100 Foveal Total Patching/surgery
20 51 M 124 R exotropia 0.475 −0.075 −0.075 Parafoveal Total Patching/surgery
Mean 44.9 108.9 0.333 −0.061 −0.061
SD 10.8 6.3 0.154 0.053 0.053
B. Controls
ID Age Sex NART Deviation Visual Acuity (Viewing Eye)
Nondominant Dominant Binocular
21 47 F 113 orthophoria −0.025 0.000 0.000
22 32 M 107 orthophoria −0.100 −0.100 −0.100
23 24 F 105 orthophoria 0.000 0.025 0.000
24 27 M 103 orthophoria −0.050 −0.050 −0.050
25 50 F 105 orthophoria −0.025 −0.050 −0.050
26 47 M 117 orthophoria −0.025 −0.025 −0.050
27 50 F 114 orthophoria −0.050 −0.025 −0.025
28 46 M 117 orthophoria 0.000 −0.025 −0.025
29 26 M 106 orthophoria −0.050 −0.050 −0.050
30 40 M 121 orthophoria 0.000 −0.025 −0.025
31 60 F 119 orthophoria −0.025 0.000 −0.025
32 50 M 118 orthophoria 0.000 −0.050 −0.050
33 33 M 115 orthophoria 0.000 0.000 0.000
34 30 M 105 orthophoria −0.050 −0.250 −0.050
35 54 F 108 orthophoria −0.075 −0.100 −0.100
36 58 F 107 orthophoria 0.000 −0.050 −0.050
37 52 F 110 orthophoria −0.050 −0.025 −0.050
38 36 F 111 orthophoria −0.025 −0.025 −0.025
39 45 F 113 orthophoria −0.075 −0.025 −0.050
40 49 F 103 orthophoria −0.050 −0.050 −0.075
Mean 42.8 110.9 −0.034 −0.045 −0.043
SD 11.0 5.7 0.030 0.057 0.028
Table 2.
 
Descriptive and Inferential Statistical Results for Each of the Oculomotor Parameters
Table 2.
 
Descriptive and Inferential Statistical Results for Each of the Oculomotor Parameters
A. Mean (±SD)
Group/Viewing Eve Reading Speed Saccades per Line (n) Amplitude of Prog. Saccades (deg) Fixation Duration (ms)
Char/s Words/min Progressive Regressive Total
Amblyopes
    Amblyopic 13.1 (±4.1) 156 (±49) 9.19 (±4.17) 2.78 (±1.50) 12.0 (±4.01) 3.82 (±1.35) 247 (±28)
    Nonamblyopic 16.2 (±3.3) 193 (±39) 9.59 (±2.29) 1.96 (±0.79) 11.5 (±2.52) 3.75 (±1.10) 234 (±26)
    Binocular 15.7 (±4.0) 187 (±48) 9.27 (±2.67) 2.43 (±1.02) 11.7 (±2.85) 3.64 (±1.07) 224 (±28)
Controls
    Nondominant 22.2 (±5.1) 264 (±60) 8.43 (±1.96) 1.57 (±0.75) 10.0 (±2.51) 4.17 (±0.83) 217 (±30)
    Dominant 22.3 (±5.7) 266 (±68) 8.20 (±2.15) 1.52 (±0.84) 9.7 (±2.68) 4.28 (±0.99) 217 (±29)
    Binocular 23.4 (±5.8) 279 (±70) 8.35 (±2.11) 1.60 (±0.82) 10.0 (±2.56) 4.31 (±0.85) 206 (±25)
B. Between-Subject Comparisons: P-value (F-statistic)
Viewing Eye (Group) Reading Speed Saccades per Line (n) Amplitude of Prog. Saccades (deg) Fixation Duration (ms)
Progressive Regressive Total
Amblyopic (amblyope) vs. nondominant (control) F = 38.9 F = 0.55 F = 10.4 F = 3.47 F = 0.94 F = 10.1
P < 0.0001* P = 0.47 P = 0.003* P = 0.070 P = 0.34 P = 0.003*
Nonamblyopic (amblyope) vs. dominant (control) F = 17.3 F = 3.89 F = 2.98 F = 4.93 F = 2.63 F = 2.23
P < 0.0001* P = 0.056 P = 0.092 P = 0.032* P = 0.11 P = 0.14
Binocular (amblyope) vs. binocular (control) F = 23.7 F = 1.44 F = 8.01 F = 4.12 F = 4.89 F = 4.33
P < 0.0001* P = 0.24 P = 0.007* P = 0.049* P = 0.053 P = 0.044*
C. Within-Subject Comparisons: P-value (F-statistic)
Viewing Eye (Group) Reading Speed Saccades per Line (n) Amplitude of Prog. Saccades (deg) Fixation Duration (ms)
Progressive Regressive Total
Amblyopic (amblyope) vs. nonamblyopic (amblyope) t = −4.26 t = −0.67 t = 2.86 t = 0.78 t = 0.27 t = 3.20
P < 0.0001* P = 0.51 P = 0.010* P = 0.45 P = 0.79 P = 0.005*
Amblyopic (amblyope) vs. binocular (amblyope) t = −2.80 t = −0.16 t = 1.378 t = 0.567 t = 0.585 t = 4.203
P = 0.011* P = 0.89 P = 0.18 P = 0.58 P = 0.57 P < 0.0001*
Nonamblyopic (amblyope) vs. binocular (amblyope) t = 1.16 t = 1.13 t = −3.177 t = −0.634 t = 1.052 t = 1.528
P = 0.259 P = 0.27 P = 0.005* P = 0.53 P = 0.31 P = 0.14
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