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Spatial Sensitivity Differences between Adults of Good and Poor Reading Ability

Geoffrey R. Patching and Timothy R. Jordan

4–14 PURPOSE. To determine whether normal adults of good and sitivity to spatial . In particular, study results poor reading ability exhibit different patterns of sensitivity to indicate that dyslexic individuals have reduced sensitivity to spatial frequency, as previously found between dyslexic and certain spatial frequencies, and this reduction tends to be nondyslexic control subjects. greatest in the low- to midfrequency range (i.e., between 2 and 4–8,10,11,13–15 METHODS. The , spatial frequency sensitivity, and 8 cyc/deg). However, despite a wealth of re- reading ability of 96 normal, nondyslexic adults was assessed. search involving dyslexic individuals there is a dearth of studies Participants were ranked according to reading ability. The top examining spatial frequency sensitivity differences between 50% were classified as good readers and the bottom 50% as “normal,” nondyslexic adults of good or poor reading ability. poor readers. Surveys of reading ability reveal a considerable range of reading abilities in the normal adult population.16,17 For in- RESULTS. Despite no differences in visual acuity, good and poor stance, the International Adult Literacy Survey (IALS; 1994– readers showed different patterns of spatial frequency sensitiv- 1998, National Literacy Secretariat, Canada)17 indicates that up ity. In particular, compared with good readers, poor readers to 52% of the normal adult population, although able to read, showed reduced sensitivity to spatial frequencies between 2 have sufficiently low levels of reading ability to make it difficult and 6 cyc/deg, and no differences in sensitivity were found at for them to face novel demands, such as acquiring new work lower or higher spatial frequencies. skills. Accordingly, the purpose of the present study was to CONCLUSIONS. The findings indicate that spatial frequency sen- assess the reading ability of normal adults and determine sitivity differences found previously between dyslexic and non- whether good and poor readers exhibit different patterns of dyslexic controls can extend to the normal (nondyslexic) adult sensitivity to spatial frequencies. population. (Invest Ophthalmol Vis Sci. 2005;46:2219–2224) The present study drew on a sample of normal, nondyslexic DOI:10.1167/iovs.03-1247 adults recruited from the university population. Reading ability was assessed by measuring effective reading speed. Effective phthalmic clinicians have long used letter charts as the reading speed is a measure widely used to assess the reading Ostandard measure of vision necessary for fluent reading. ability of normal (nondyslexic) adults.18–28 It is defined as the However, letter charts measure a person’s ability to resolve time taken to read short passages or sentences in words per fine detail and, even when visual acuity is normal, other visual minute (wpm) multiplied by either the number of words read factors may also play an important role in reading. Spatial correctly26 or the number of questions answered correctly in a frequency sensitivity is one such factor of increasing interest. brief comprehension test.19 As a combined measure of reading Spatial frequency sensitivity provides an indication of a speed and comprehension, effective reading speed encapsu- person’s ability to perceive visual information across the full lates not only participants’ ability to comprehend what they visual spectrum, from fine to broad scale, and is measured with have read but also the efficiency with which they are able to repetitive patterns of black-and-white bars. The luminance pat- achieve understanding, and this combined measure of speed tern across these bars describes a , and the patterns and comprehension was selected as the index of reading ability are referred to as sine-wave . Spatial frequency is ex- in our study. pressed as the number of cycles (one black plus one white bar) Contrast sensitivity was measured with a spatial two-alter- per degree of visual angle. The amount of contrast required native, forced-choice (2AFC) task in which participants were (i.e., contrast threshold) for detection of sine-wave gratings is required to indicate on which side of a display screen a sinu- known to vary systematically as a function of their spatial soidal was presented. The QUEST staircase procedure frequency. The reciprocal of the threshold contrast (i.e., 1/con- was used to estimate each participant’s contrast threshold.29 trast threshold) is the contrast sensitivity, and the contrast This procedure has been effective in several investigations26,30 sensitivity function (CSF) describes the variation of the sensi- and enabled assessment of participants’ sensitivity to a range of tivity over a range of spatial frequencies.1–3 spatial frequencies from 0.5 to 12 cyc/deg. Comparison of A substantial body of evidence indicates that dyslexic and sensitivity to spatial frequencies between good and poor read- nondyslexic control subjects exhibit different patterns of sen- ers promised to reveal whether normal adults of good or poor reading ability differ in their sensitivity to certain spatial fre- quencies. From the Department of Psychology, Stockholm University, Stock- holm, Sweden; and the School of Psychology, University of Leicester, University Road, Leicester, United Kingdom. Supported by Wellcome Trust Grant 059727 (TRJ). METHOD Submitted for publication November 15, 2003; revised July 4, 2004; accepted August 5, 2004. Participants Disclosure: G.R. Patching, None; T.R. Jordan, None Ninety-six undergraduate students (38 men and 58 women) between The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked “advertise- the ages of 18 and 35 took part in the experiment. All participants were ment” in accordance with 18 U.S.C. §1734 solely to indicate this fact. native speakers of English, and none reported any history of epilepsy Corresponding author: Geoffrey R. Patching, Department of Psy- or dyslexia or demonstrated any reading problems when tested. Each chology, Stockholm University, S-106 91 Stockholm, Sweden; participant took part in one 75-minute session, in which each partici- [email protected]. pant was tested for visual acuity, contrast sensitivity, and reading

Investigative Ophthalmology & Visual Science, June 2005, Vol. 46, No. 6 Copyright © Association for Research in Vision and Ophthalmology 2219

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ability. Informed consent was obtained from each participant before Reading Speed the experiment, in accordance with the Declaration of Helsinki. Stimuli. Seven passages were selected from Notes From a Small Island by Bill Bryson,36 which provided an engaging text. On average, Visual Acuity each passage contained 527 words. After each passage, five multiple- choice questions were presented. The questions referred to different 31 Visual acuity was tested with the Bailey-Lovie eye chart. Participants detailed aspects of the preceding paragraph and were designed to were required to continue reading letters down the chart from a ensure that participants read each paragraph in full.37,38 distance of 3 m until they failed to identify any letters on one line. Visual Conditions. Viewing was binocular. Each passage was Performance was scored by the method recommended by Kitchin and presented on the same ␥-corrected video monitor as that used to test 32 Bailey. The total number of letters read incorrectly was recorded, and contrast sensitivity. The text was presented in black on a light gray an “error” score of 0.02 assigned to each. These scores were added to background, and a complete passage of text filled an area approxi- the last line on which any letters were read. To continue participating mately 18° (horizontal) ϫ 27° (vertical) and had proportions similar to in the study, participants were required to have a minimum binocular those of an A4 page of text (which is familiar in the British reading acuity of 10/10 (3/3), indicative of normal visual acuity. environment). Background illumination of the monitor screen was 46 cd/m2, and the luminance of text was 0.15 cd/m2. Contrast Sensitivity Design. Each participant was presented with all seven passages. One passage (the first shown) was always used as practice, and the Stimuli. Contrast sensitivity was tested with gray-scale vertical remaining six as test passages, shown in a random order. sine-wave gratings of 0.5, 1, 2, 4, 6, 8, 10, and 12 cyc/deg. These spatial Procedure. Participants were told that the experiment would frequencies were chosen to conform to previous psychophysical examine the time taken to read different passages of text, and that they 1–3 studies of spatial frequency sensitivity and to cover the range of should read through each passage once, from start to finish, as rapidly spatial frequencies used in previous studies involving dyslexic indi- as if they were reading a page of a book. As soon as a button was 4–13,15 viduals. A Gaussian patch modulated each sine wave grating, to pressed, a passage was presented (shown in its entirety on the screen) create eight Gabor stimuli, each with a different spatial frequency. and the timer started. Participants pressed the button again when they Visual Conditions. Viewing was binocular. The Gabor stimuli had read the final word of each passage, and this stopped the timer. were presented on a ␥-corrected video monitor with a resolution of The passage was immediately replaced with five multiple-choice ques- 980 ϫ 1024 pixels. Viewed from a distance of 57 cm, the viewable area tions and participants were required to select one of three answers of the monitor measured 23° horizontally and 29° vertically. Back- from each of the five questions before continuing. ground illumination of the monitor screen and space-averaged lumi- nance of each Gabor was kept constant at 35 cd/m2. Each Gabor subtended 12° vertically and 12° horizontally (the radial size of each RESULTS standard deviation of Gaussian patch was 3°) and were presented so that the center of each Gabor always fell 6° to the left or right of the To identify good and poor readers, an effective reading speed center of the video monitor on the horizontal midline. was calculated for each participant by multiplying the reading Apparatus. The Gabor stimuli were presented on a 40.4 ϫ speed in words per minute by the proportion of questions they 30.2-cm monitor (Trinitron GDM-F520; Sony, Tokyo, Japan). A Cam- answered correctly. Effective reading speed ranged from 99 bridge Research Systems (Rochester, UK) visual stimulus generator (reading speed, 156 wpm; proportion of questions answered (VSG2/5) card controlled stimulus presentations and timing. Re- correctly, 0.63) to 365 (reading speed, 421 wpm; proportion of sponses were collected with a button box (CT3; Cambridge Research questions answered correctly, 0.87). For poor readers (bottom Systems). Luminance was measured with an optical photometer. The 50%, comprising 20 men and 28 women), effective reading Ϯ experiment was conducted in a quiet, darkened room. A viewing hood speeds ranged from 99 to 185 (mean, 53 21 wpm; SD) and, for good readers (top 50%, comprising 18 men and 30 women), fixed to the monitor ensured a constant viewing distance and elimi- Ϯ nated any extraneous light sources. from 186 to 365 (mean, 228 37 wpm). Visual acuities for all participants ranged from Ϫ0.5 to Ϫ0.3 Design. Each different Gabor stimulus was presented 80 times, logMAR (mean, Ϫ0.35 Ϯ 0.05; SD). The visual acuity data were randomly interleaved, giving a total of 640 trials. Contrast sensitivity analyzed with an analysis of variance with two between-sub- was measured with a spatial 2AFC task in which participants had to jects factors (reading ability, sex). No statistically reliable dif- decide on which side of the video monitor the Gabor patch was ferences in visual acuity were found between good and poor presented. During each trial, the contrast of each Gabor was deter- ϭ Ͼ readers (F(1,92) 0.07; P 0.70), between men and women mined by using the QUEST algorithm29,30,33 in the Psychophysics ϭ Ͼ F(1,92) 1.75; P 0.10), and no interaction was found be- Toolbox.34,35 The threshold was set at 0.82, and the initial contrast of ϭ Ͼ tween reading ability and sex (F(1,92) 0.15; P 0.70). each Gabor was set at the average obtained from pilot studies. The final Nevertheless, good and poor readers exhibited different pat- estimate was taken as the mean of the posterior probability distribution 30 terns of spatial frequency sensitivity. The results of the spatial function. frequency sensitivity test for good and poor readers are shown Procedure. Each participant was given written instructions in- in Figure 1. The sensitivity data were analyzed with a Green- forming him or her of the task and of the importance of responding as house-Geisser corrected analysis of variance with two be- accurately as possible. At the start of each trial, a clearly audible “beep” tween-subjects factors (reading ability, sex) and one within- was emitted from the button box to inform participants that a Gabor subject factor (spatial frequency). This analysis revealed main patch was about to be presented. A Gabor patch was then presented ϭ Ͻ effects of reading ability (F(1,92) 6.00; P 0.05) and spatial ϭ Ͻ on either the left or right side of the video monitor. To avoid onset frequency (F(3.97,365.60) 310.06; P 0.001) and an interac- transients, each Gabor was ramped on (exponentially) over the first tion between reading ability and spatial frequency (F(3.97,365.60) 100 ms. Each Gabor then remained on the video monitor at the ϭ 3.05, P Ͻ 0.01). No differences were found between men contrast level determined by the QUEST algorithm, until a choice and women and no interactions were obtained with this factor. response was made. To make a choice, participants were required to The Tukey honest significant difference (HSD) tests showed press one of two buttons to indicate on which side of the video that poor readers were less sensitive than good readers to monitor the Gabor patch was presented. spatial frequencies of 2, 4, and 6 cyc/deg (all P Ͻ 0.05). In good

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DISCUSSION The results of the present study indicate that sensitivity to certain spatial frequencies affects reading ability in the normal (nondyslexic) adult population. In particular, despite having normal visual acuity, poor readers showed reduced sensitivity to spatial frequencies of 2, 4, and 6 cyc/deg, relative to good readers. This finding resonates with those found previously be- tween dyslexic and nondyslexic control subjects,4–8,10,11,13–15 indicating that differences in spatial frequency sensitivity between dyslexic and nondyslexic control subjects can extend to the normal (nondyslexic) adult population. Further examination of the relationship between spatial frequency sensitivity and reading ability revealed moderate correlations between effective reading speed and spatial fre- quency sensitivity for spatial frequencies of 2, 4, 6, and 8 cyc/deg. Similarly, prereaders’ sensitivity to spatial frequencies of 2 and 4 cyc/deg has been found to be related to their reading ability 2 years later.39 The implication of the results in that study is that spatial frequency sensitivity differences found between children do not result from a failure to learn to read, but that differences in sensitivity to certain spatial frequencies produce different reading abilities and, in light of the present study, that relations between spatial frequency sensitivity and reading ability found previously with young children can ex- tend into adulthood. FIGURE 1. Log sensitivity (1/contrast threshold) for good and poor readers. However, results of previous studies that have tested per- formance with a small range of spatial frequencies (typically, no more than four) and have shown a decline in sensitivity to all spatial frequencies tested may reflect merely an overall lack readers, sensitivity was lower at spatial frequencies of 1 and 4 40 cyc/deg than for 2 cyc/deg (P Ͻ 0.01); lower for 0.5 and 6 of attention to the task or, in the case of normal, nondyslexic cyc/deg than for 1, 2, and 4 cyc/deg (P Ͻ 0.01); lower for 8 children, overall differences in intellectual ability. In contrast, cyc/deg than for 0.5, 1, 2, 4, and 6 cyc/deg (P Ͻ 0.01); and the present study tested sensitivity over a wider range of spatial lower for 10 and 12 cyc/deg than for 0.5, 1, 2, 4, 6, and 8 frequencies (eight, from 0.5 to 12 cyc/deg), and revealed no cyc/deg (P Ͻ 0.05). However, for poor readers, sensitivity was overall deficits for poor readers but, instead, deficits only at lower at spatial frequencies of 1 cyc/deg than of 2 cyc/deg specific spatial frequencies. Consequently, it seems unlikely (P Ͻ 0.01); lower at 4 cyc/deg than at 1 and 2 cyc/deg (P Ͻ that problems concerning overall differences in intellectual ability between good and poor readers, or overall differences 0.01); lower at 0.5 cyc/deg than at 1, 2, and 4 cyc/deg (P Ͻ in attention to the task, can account for the selective reduction 0.01); lower at 6 cyc/deg than at 1, 2, and 4 cyc/deg (P Ͻ 0.01); in spatial-frequency sensitivity displayed by adults of poor lower at 8 cyc/deg than for 0.5, 1, 2, 4, and 6 cyc/deg (P Ͻ reading ability. 0.01); and lower at 10 and 12 cyc/deg than at 0.5, 1, 2, 4, 6, and The deficits displayed by poor readers in sensitivity to some, 8 cyc/deg (P Ͻ 0.01). No other comparisons were significant. but not all, spatial frequencies provide a strong indication that Statistically, a similar pattern of results emerged when read- differences in sensitivity to certain spatial frequencies affect ing ability was considered in terms of raw reading speed alone. the ability to read. However, the precise nature of the causal However, effective reading speed registers differences in raw relationship between spatial frequency sensitivity and reading reading speed and comprehension combined. Indeed, this ability has yet to be fully determined. Indeed, although it point is further supported by the high correlation between currently seems highly unlikely that differences in reading ϭ Ͻ effective and raw reading speeds (r 0.90; P 0.001) and ability cause selective differences in spatial frequency sensitiv- ϭ between effective reading speed and comprehension (r ity, further rigorous experimental research is needed, to deter- Ͻ 0.34; P 0.001). Therefore, as in previous studies, effective mine fully the precise link between spatial frequency sensitiv- reading speed is considered the most appropriate measure of ity and reading ability. 19 reading ability (see Jackson and McClelland for further dis- One explanation of the present findings is that poor readers cussion). Further analysis revealed no speed accuracy tradeoff, have reduced sensitivity to a midrange of spatial frequencies, as evidenced by the low correlation between raw reading and this reduction in sensitivity to these spatial frequencies speed and comprehension (r ϭϪ0.08; P Ͼ 0.40). affects their ability to perceive words. Psychophysically, words Further correlation analysis was conducted to examine re- are complex images comprising a broad range of spatial fre- lations between effective reading speed and spatial frequency quency information, from coarse to fine scale, and there is a sensitivity. Figure 2 shows the scatter plots relating effective growing body of research that suggests an important role for reading speed and sensitivity to each spatial frequency sepa- coarse-scale (low-frequency) and fine-scale (high-frequency) rately for each spatial frequency. Statistically significant corre- visual information in word perception20,22,41–45 (Boden C, et lations were found between effective reading speed and sen- al. IOVS 2000;41:ARVO Abstract 2298; Dakin SC, et al. IOVS sitivity to spatial frequencies of 2 (r ϭ 0.20; P Ͻ 0.05), 4 (r ϭ 1999;40:ARVO Abstract 184). Indeed, several investigators 0.30; P Ͻ 0.01), 6 (r ϭ 0.30; P Ͻ 0.01), and 8 (r ϭ 0.27; P Ͻ posit a system of word recognition in which both coarse-scale 0.01) cyc/deg. No other correlations were significant. No sta- visual information about word shape and more fine-scale infor- tistically reliable relationship was found between visual acuity mation about letter features play an important role in visual and effective reading speed (r ϭϪ0.04; P Ͼ 0.70). word perception.46–49 Consequently, individual differences in

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FIGURE 2. The relationship between effective reading speed and spatial frequency sensitivity separately for each spatial frequency. The correlation coefficient, Pearson’s r, is specified in each scatterplot. IOVS, June 2005, Vol. 46, No. 6 Spatial Frequency Sensitivity and Reading Ability 2223

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