J Autism Dev Disord DOI 10.1007/s10803-014-2086-x

BRIEF REPORT

Brief Report: Visual Acuity in Children with Autism Spectrum Disorders Matthew A. Albrecht • Geoffrey W. Stuart • Marita Falkmer • Anna Ordqvist • Denise Leung Jonathan K. Foster • Torbjorn Falkmer



 Springer Science+Business Media New York 2014

Abstract Recently, there has been heightened interest in suggestions of enhanced visual acuity in autism spectrum disorders (ASD) which was sparked by evidence that was later accepted to be methodologically flawed. However, a recent study that claimed children with ASD have enhanced visual acuity (Brosnan et al. in J Autism Dev Disord 42:2491–2497, 2012) repeated a critical methodological flaw by using an inappropriate viewing distance for a computerised acuity test, placing the findings in doubt. We examined visual acuity in 31 children with ASD and 33 controls using the 2 m 2000 Series Revised Early Treatment Diabetic Retinopathy Study chart placed at twice the conventional distance to better evaluate possible enhanced acuity. Children with ASD did not demonstrate superior acuity. The current findings strengthen the argument that reports of enhanced acuity in ASD are due to methodological flaws and challenges the reported association between visual acuity and systemising type behaviours.

Keywords Asperger syndrome  Case control study  ETDRS  High functioning autism  Perception  Vision

M. A. Albrecht  J. K. Foster School of Psychology and Speech Pathology, Curtin Health Innovation Research Institute, Curtin University, Perth, WA, Australia

A. Ordqvist  T. Falkmer Faculty of Health Sciences, Department of Medicine and Health Sciences (IMH), Rehabilitation Medicine, Linko¨ping University and Pain and Rehabilitation Centre, UHL, County Council, Linkoping, Sweden

G. W. Stuart Olga Tennison Autism Research Centre, School of Psychological Science, La Trobe University, Melbourne, VIC, Australia M. Falkmer  D. Leung  T. Falkmer (&) Faculty of Health Sciences, School of Occupational Therapy and Social Work, Curtin Health Innovation Research Institute, Curtin University, GPO Box U1987, Perth, WA 6845, Australia e-mail: [email protected]

Introduction Neurological differences in people with ASD can result in a variety of perceptual processing alterations. In particular, many studies have found an enhancement in ‘local processing’ in ASD (Dakin and Frith 2005; Happe´ and Frith 2006). This enhancement has subsequently been hypothesised to account for part of the observed behavioural profile in ASD (Happe´ 1999; Mottron et al. 2006). Ashwin et al. (2009) reported a considerable enhancement in visual acuity in male adults with high functioning autism or Asperger syndrome. They suggested that their findings may offer an alternative explanation for the enhanced local processing seen in people with ASD.

J. K. Foster Neurosciences Unit, Health Department of WA, Perth, WA, Australia T. Falkmer School of Occupational Therapy, La Trobe University, Melbourne, VIC, Australia

M. Falkmer CHILD Programme, School of Education and Communication, Institute of Disability Research, Jo¨nko¨ping University, Jonkoping, Sweden

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Surprisingly, the claimed mean Snellen acuity of the group with ASD in the Ashwin et al. study was 20/7, and the maximum reported score was 20/5.7. These visual acuity scores are outside the physical receptor limits of the human eye (Applegate 2000). Subsequently, two commentaries by Bach and Dakin (2009) and Crewther and Sutherland (2009) identified several methodologically flaws within the study of Ashwin et al. (2009), including sitting participants at 60 cm from the screen, which is much closer than the recommended distance of 2 m meaning that none of the stimuli were able to provide a test for the claimed acuities. Several follow-up studies found no evidence for superior visual acuity in individuals with ASD (Falkmer et al. 2011; Tavassoli et al. 2011; Bo¨lte et al. 2012). Indeed, even prior to the initial Ashwin et al. (2009) study, there was no evidence for superior acuity in people with ASD (Scharre et al. 1992). Most recently, Brosnan et al. (2012) have again claimed that people with ASD, in this case children, have superior visual acuity compared to non-ASD controls. However, this study, like that of Ashwin et al. used the computerised Freiburg visual acuity and contrast test (FrACT) (Bach 1996). Most notably, the participants in the Brosnan et al. (2012) study, again like those of Ashwin et al. were seated 60 cm from the test screen, compared to the recommended minimum distance of 2 m (Bach and Dakin 2009). Critically, although Brosnan et al. (2012) reported the viewing distance used (60 cm) and the resolution of their monitor (1,280 9 1,024), they did not specify the pixel size of their monitor or its physical dimensions. The physical dimension of the monitor, along with resolution (given as 1,280 9 1,024) will determine angular pixel size. At normal acuity (20/20, or 0 in logMAR) the minimum angular resolution is 1 min of arc, while to present stimuli at 20/10 (logMAR = -0.3) would require a gap of 0.5 min of arc. FrACT will not generate a Landolt C optotype with a gap less than one pixel (Bach and Dakin 2009). Therefore, in order to generate a stimulus representing an acuity of 20/10 (equivalent to the smallest line on a standard acuity chart) the monitor would need to be 11.7 by 8.9 cm or smaller to present a Landolt C optotype with the indicated resolution and the required pixel size. There was no indication that specialised display hardware of this size was used. If not, this meant that the smallest test stimuli were above accepted acuity thresholds, which would lead to spurious results calculated by the threshold finding algorithm within FrACT (Bach and Dakin 2009; Crewther and Sutherland 2009). Hence, it seems unlikely that the results of Brosnan et al. (2012) are valid with respect to their claim of superior visual acuity in children with ASD. Again, it appears as though inappropriate recording conditions during the use of

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the FrACT has given the result that individuals with ASD, in this instance children, have superior visual acuity compared with control children. The aim of the present study was to investigate this most recent claim of enhanced visual acuity specifically in children with ASD. We used the 2 m 2000 Series Revised Early Treatment Diabetic Retinopathy Study (ETDRS) Chart (Precision Vision 2011), a ‘‘gold-standard’’ assessment tool in acuity research, as superior visual acuity should not depend on the instrument used. We hypothesised that there would not be superior visual acuity in children with ASD compared with controls, consistent with adolescent-adult research conducted by Falkmer et al. (2011) and Tavassoli et al. (2011) who also used an ETDRS chart, and Tavassoli et al. (2011) and Bo¨lte et al. (2012) who used the FrACT.

Methods Participants Thirty-one (26 male) children with Asperger’s Syndrome or with High Functioning Autism (ASD group) and 33 (26 male) typically developing children participated in the study. The children with ASD were recruited through the Telethon Institute of Child Health Research and through The Autism Association of Western Australia. The children in the control group were recruited through local primary schools, local sports clubs, personal contacts and through local radio and newspaper advertisements in the Perth metropolitan area in Western Australia. Medical records were sighted to confirm that each child with ASD had been diagnosed by a multi-disciplinary team assessment (Le Couteur et al. 2008; Woolfenden et al. 2012; Falkmer et al. 2013). No child with ASD was taking a medication that was relevant for assessment of visual acuity and none had a comorbid disorder. All children were attending mainstream schools, were able to read and comprehend both written and verbal instructions in English, and did not have a comorbid cognitive impairment. The mean age for the two groups was similar, 10.6 years (SD = 1.3 years) in children with ASD and 10.6 years (SD = 1.2 years) in children without ASD (controls); all children in the study were aged between 8 and 13 years. According to the accompanying parents, all children were reported to have normal or corrected vision and children who needed optometric corrections wore their usual glasses/lenses. However, several children had visual acuity scores substantially \20/20, therefore a supplementary analysis excluding those children who had a logMAR score larger than 0.02, or 20/21 on the Snellen scale (see Fig. 1 for cut off) was performed. The study was approved by the Human Research Ethical

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chart background was consistent with the standards of the ETDRS protocol (170 cd/m2). Procedures

Fig. 1 Raw logMAR and corresponding Snellen acuity scores for the control (N = 33) and ASD (N = 28) children with posterior means ±95 % HDIs for the full sample (Open Circles) and for the reduced sample with logMAR B 0.02 (Filled Circles). For the full sample (individuals both above and below the dashed line; controls N = 33, ASD N = 31), the mean contrast between children with ASD and the control children was credibly non-zero (ASD—controls contrast = 0.085, 95 % HDI = 0.018, 0.15). However, there was little difference between the groups for the reduced sample (individuals below the dashed line; controls N = 31, ASD N = 21; ASD— controls contrast = 0.022, 95 % HDI = - 0.020, 0.064)

Committee of Curtin University, Perth, Western Australia (approval numbers OTSW-03-2011 and OTSW-10-2011).

Before testing began, the visual acuity procedure was verbally explained to the children. In addition, relevant pictures were used to explain the procedures. All children were asked to name ten letters that would appear in the visual acuity test, to ensure that they possessed the necessary reading ability to successfully complete the test. The chart was read from top to bottom (i.e., lowest acuity to highest acuity) first with one eye covered, then the other eye covered, and finally with both eyes. However, only the data obtained from reading with both eyes are presented in this paper, in order to give the most appropriate comparison with previous results. The test was terminated when participants reached a line on the chart where they could not read any of letters on that line. Scoring was performed as per the ETDRS instructions: the log of the minimum angular resolution (logMAR) score for the row where the participant correctly identified all five letters was identified. From this score, 0.02 logMAR units were subtracted for every letter that was correctly identified beyond this last fully correct row. A Snellen acuity of 20/20 corresponds to a logMAR of zero (lower acuity corresponds to higher logMAR numbers). Statistical Analyses

Visual Acuity Measurement In order to give the best chance of detecting potential superior visual acuity, and to use the current ‘‘gold standard’’ in visual acuity research, a 2 m 2000 Series Revised ETDRS Chart (Precision Vision 2011) was presented at a distance of 4 m (this allowed for testing of visual acuities up to 20/5 on the Snellen scale). The ETDRS Charts are standardised for assessing visual acuity and, compared to Snellen type acuity charts, they have better accuracy in determining the level of visual acuity (regardless of whether the individual has high or low acuity) and are less influenced by crowding effects because they have consistent letter and row spacing (Kaiser 2009). In addition, compared to the FrACT, ETDRS charts are not dependent on computer pixel size or screen resolutions only the distance from the chart to calculate acuity. However, it should be mentioned that the FrACT is perfectly capable of providing an accurate assessment of visual acuity when used according to specifications. Each line of the chart contains five letters with spacing proportional to the font size. The chart was placed in an ETDRS Illuminator cabinet (Precision Vision 2011). The surface luminance of the white

Bayesian estimation was used (as per Kruschke 2013) to provide more detailed information for testing hypotheses, since it can accommodate outliers easily (as might reasonably be expected from clinical samples), differences in variances between groups, and gives a range of possible effect sizes. Due to the respective shapes of the data of the two groups, and to reduce the influence of outliers and render the analysis ‘robust’, the Bayesian analysis used a tdistribution to model the data. The t-distribution is described by three parameters: the mean, the SD, and the normality parameter (m). As m approaches infinity, the distribution more closely resembles a normal distribution. At lower values of m, the distribution has a smaller central peak but larger tails. When this distribution is fitted to sample data that is contaminated by outliers, it results in a down weighting of the influence that outlying data points have on the estimated mean (dependent on the estimate of m, which is derived from the data). This down weighting, or redescending principle, is similar to that used in other methods of robust statistical estimators (Lange et al. 1989). This statistical approach therefore reduced the influence of poor acuities on estimates of central tendency.

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Both participant groups were modelled with a separate mean and SD parameter, but shared a common m parameter (Kruschke 2013). The log10 posterior mean for the common m parameter was equal to 0.76 (95 % HDI = 0.32, 1.6) for the full sample, and 1.48 (95 % HDI = 0.82, 2.10) for the reduced sample. The priors used in the analysis were non-informative priors so as not to bias the results towards, or away from, any particular hypothesis. The prior on each of the means was described using a normal distribution with the mean equal to the overall mean (both controls and children with ASD combined) and precision (inverse of the squared SD) equal to 10-6 multiplied by the precision of the overall group. The prior on each of the SDs was described by a uniform distribution bounded by 0.001 multiplied by the overall group SD and 1,000 multiplied by the overall group standard deviation, i.e., each value between 0.001 and 1,000 times the SD is equally likely. The prior on the normality parameter was described by a shifted exponential distribution centred on 30, representing a satisfactory compromise between detecting high and low normality parameters. In total, 1,000 steps were used to tune the samplers, 5,000 steps were used burn in the chains, and a total of 1,000,000 Markov Chain Monte Carlo (MCMC) samples were obtained for the final parameter estimates. The 95 % highest density intervals (HDI) of the posterior distribution were used to describe the credibility interval for each of the estimates and contrasts. All statistical analysis was performed in R version 2.15.1 (R Development Core Team, 2012) using the ‘‘rjags’’ package to interface with the Gibbs sampler, JAGS version 3.3.0 (Plummer, 2003, 2011). The Bayesian data analysis scripts were modified from Kruschke (2013).

Results Figure 1 presents the raw data for both controls and children with ASD along with the means (±95 % HDIs) of the posterior parameter estimates for the full sample (open circles) and for the sample with all individuals obtaining a logMAR score less than or equal to 0.02 (closed circles). The difference in visual acuity estimates from the Bayesian analysis for the full sample indicated that the children with ASD had poorer overall acuity compared to the control children (ASD—controls contrast = 0.085, 95 % HDI = 0.018, 0.15; Effect size = 0.70, 95 % HDI = 0.154, 1.29). However, our study is more concerned with the claim of superior visual acuity in children with ASD. When the children with visual acuities poorer than 0.02 logMAR, that is with higher logMAR values, were excluded (2 controls, 10 children with ASD), there was no difference in acuity between children with ASD and controls (contrast = 0.022, 95 % HDI =

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-0.020, 0.064; Effect size = 0.30, 95 % HDI = -0.27, 0.88). We tested for differential practice effects between the ASD children and controls as all results present scores for binocular viewing which was carried out after monocular viewing. Eighteen out of 33 control participants and 16 out of 31 children with ASD improved their score beyond 0.02 logMAR units (i.e., more than one scoring increment) when using both eyes (X2[1] = 0, p = 1), while the remaining participants’ score for both eyes was equivalent to the score for the best performing single eye.

Discussion The present findings are consistent with the many studies that have failed to find superior visual acuity in individuals with ASD (Scharre et al. 1992; Milne et al. 2009; Koh et al. 2010; Ke´¨ıta et al. 2010; Falkmer et al. 2011; Tavassoli et al. 2011; Bo¨lte et al. 2012). Only one participant with ASD in the present study demonstrated a visual acuity superior to that of the control group, and this was only 0.02 logMAR units superior to the best of the controls (20/11.5 vs. 20/12 on the Snellen scale). This evidence, together with the previously cited studies, does not support the notion of superior visual acuity in children with ASD. The failure to find superior visual acuity in children with ASD is not surprising considering the methodological limitations of the studies that have reported positive effects in people with ASD (Bach and Dakin 2009; Crewther and Sutherland 2009). Interestingly, Brosnan et al. (2012) included in the introduction these arguments (reinforced by Falkmer et al. 2011; Tavassoli et al. 2011; and Bo¨lte et al. 2012, who are also quoted), but did not address them in their design using the same viewing distance as Ashwin et al. (2009). This was against the advice of the developer of the test who emphasises the criticality of an appropriate viewing distance in the first two items of a user ‘‘checklist’’ on the FrACT website (http://michaelbach.de/fract/checklist. html). Their justification for using a short viewing distance was that they wished to test acuity at the same distance as their other tests. Unfortunately, the use of a short viewing distance limits the upper range of acuities that can be tested. There was some acknowledgement of this problem in the discussion of the paper: ‘‘…those with ASD can demonstrate a higher index of visual acuity using the FrACT methodology at short viewing distances rather than those with ASD having a higher visual acuity per se.’’ (p. 2496). Yet they claimed in the abstract that children with ASD ‘‘…have significantly greater visual acuity.’’ (Brosnan et al. 2012). They also argued that because the measured acuities in the control group were in the normal range indicated, the test was valid even though this has no bearing on the

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geometry of the viewing conditions. Given that there is no reputable evidence for superior acuity in children with ASD, the suggested association between actual visual acuity and systemising behaviours found in Brosnan et al. (2012) is highly unlikely. Moreover, the elements in the embedded figures test are fully visible without superior acuity, further questioning the likelihood of a meaningful association between systemising behaviours and visual acuity. The most plausible explanation for the findings presented in Brosnan et al. (2012) is that there is a relationship between systemising type behaviour on the embedded figures test and systemising type behaviour that emerges in individuals with ASD given certain testing conditions (e.g., stereotypical response strategies on the FrACT at short distances and increased tolerance for repetitive tasks, Bach and Dakin 2009; Crewther and Sutherland 2009). For there to be a significant increase in visual acuity in ASD, there would need to be a number of fundamental anatomical changes in individuals with ASD compared with controls, specifically increases in either or both of the size of the eye and the density of photoreceptors in the fovea (Falkmer et al. 2011). It is these anatomical differences that have been linked with the superior acuity seen in eagles (Reymond 1985; Jones et al. 2007), the animals that Ashwin et al. (2009) originally compared their ASD participants with superior visual acuity to. However, evidence to suggest that individuals with ASD show the necessary anatomical alterations that would lead to superior acuity does not exist in the literature. A few children in our study exhibited acuity less than the accepted 20/20 Snellen standard. This does not compromise our findings because Brosnan et al. (2012), consistent with the previous report by Ashwin et al. (2009), claimed that enhanced acuity was a significant feature of ASD with a very large effect size (see their Fig. 2). We found that the ceiling of visual acuity was the same in both groups. In a sample of our age distribution, it is likely that most individuals would be able to focus their eyes at the viewing distance used, with or without optical correction. The ultimate limit of visual acuity is not due to inadequate focus of the eye. Rather, it is due to the optical quality of the eye, which is limited by higher order aberrations—in essence the ‘‘roughness’’ of the cornea and lens (see Falkmer et al. 2011 for further details). There is no known mechanism by which this fundamental optical limit can be overcome, and not a single previous credible example of ‘‘superacuity’’ in a human being. We are therefore confident that such an ability was not being masked in the case of the minority of participants where our acuity screening test indicated optometric correction might be required. Our findings indicate that there is no enhanced visual acuity in children with ASD compared to typically developing children. This is the fifth study to date that we are

aware of (alongside Scharre et al. 1992; Falkmer et al. 2011; Tavassoli et al. 2011; Bo¨lte et al. 2012) to find no enhancement of visual acuity in individuals with ASD. The only studies to have made such claims (Ashwin et al. 2009; Brosnan et al. 2012) have been based on assessments of acuity that were rendered meaningless by the use of viewing distances that invalidated the test. Future attempts to explain altered visual perception in ASD should explore other factors. Acknowledgments We want to express our gratitude to the participating children and their parents. We are also grateful for the help provided by the Telethon Institute of Child Health Research and The Autism Association Western Australia for their help in the recruitment process.

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Brief report: visual acuity in children with autism spectrum disorders.

Recently, there has been heightened interest in suggestions of enhanced visual acuity in autism spectrum disorders (ASD) which was sparked by evidence...
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