Spatial localisation in autism: evidence for differences in early cortical visual processing Keziah Latham1,2*, Susana TL Chung2,3, Peter M Allen1,2, Teresa Tavassoli4,5 and Simon Baron-Cohen4 Abstract Background: Vision in people with autism spectrum conditions (ASC) is reported to be different from people without ASC, but the neural level at which the differences begin to occur is not yet known. Here we examine two variants of a vernier acuity task to determine if differences are evident in early visual processing. Findings: Abutting and separated vernier acuity was assessed in 16 people with ASC and 14 matched controls. In controls, abutting and separated thresholds were unrelated (r = 0.13, p = 0.65), suggesting thresholds are determined by two separate mechanisms. In contrast, the abutting and separated thresholds of ASC observers were strongly correlated (r = 0.88, p < 0.0001), with separated thresholds tending towards being superior to those of controls [t(28) = −2.46, p = 0.02]. Conclusions: The findings suggest the mechanisms employed by ASC observers in separated vernier tasks are different to those of controls. This psychophysical evidence suggests that visual differences in ASC may begin at an early cortical stage of visual processing. Keywords: Autism spectrum conditions, Spatial vision, Vernier acuity, Hyperacuity, Psychophysics, Visual processing Findings Where in the visual processing system do differences in vision begin to arise for people with autistic spectrum conditions (ASC)? People with ASC appear to have normal responses to basic visual tasks [1], but difficulties with complex face recognition tasks and enhanced attention to local visual information over global in tasks such as visual search [2,3]. To understand the nature and location of differences in visual processing in ASC, Simmons et al. [3] state: “A really basic characterization of the visual processing capabilities of people with ASC would be extremely useful, even if all it could do was say with certainty ‘nothing is wrong here’”. Starting with basic visual processing, visual acuity (or the minimum recognisable acuity) is limited by foveal cone spacing [4] and is similar in people with ASC and controls [1]. Moving methodically up the visual pathway, the next logical visual function to examine is the spatial localisation of two features, or the minimum discriminable acuity. Localisation thresholds can be more precise than cone spacing and are limited in the primary visual cortex [5-8]. Here, we assess spatial localisation using a vernier acuity paradigm across two conditions that are thought to be mediated by different neural mechanisms: (1) abutting line vernier targets, processed by contrastdependent spatial filters encompassing both stimulus elements [5,6]; (2) line vernier targets separated by 10 arc min. For lines separated by more than 4 arc min [5,6], vernier thresholds are contrast-independent, the mechanism underlying performance involving position identification of each stimulus element using a local sign process [9], followed by a collator mechanism capable of comparing the responses to the two individual stimulus elements [6-8]. Our hypothesis, based on earlier evidence, is that spatial localisation in ASC and control observers will be similar, with differences arising at higher (attentional) levels of visual processing. Methods Procedure Two-line vernier thresholds were assessed using two long (30 arc min at 8 m), thin (18.9 arc sec at 8 m), bright * Correspondence: [email protected] 1 Department of Vision & Hearing Sciences, Anglia Ruskin University, Cambridge, UK 2 Vision and Eye Research Unit, Anglia Ruskin University, Cambridge, UK Full list of author information is available at the end of the article © 2013 Latham et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Latham et al. Molecular Autism 2013, 4:4 molecularautism/content/4/1/4(luminance 300 cdm-2) white lines presented vertically on a dark (luminance 26 and from one person with ASC as their WASI IQ was 0.05), but as expected did differ on Autism Spectrum Quotient (AQ) scores (p < 0.0001). Results There was no difference in response bias for abutting stimuli [ASC −2.5 ± 4.7, control −2.2 ± 5.7; t(28)-1.15, p = 0.88] or for separated stimuli [ASC −3.2 ± 8.8, control +3.4 ± 9.0; t(28)-2.01, p = 0.06]. Mean vernier thresholds for each group and condition are shown in Table 2. Thresholds for the control group were in accordance with previously published data for similar parameters [5]. There was no significant difference in thresholds between ASC and control observers for abutting vernier stimuli [t(28) = −0.63, p = 0.54; Cohen’s d −0.25]. There was a significant difference between groups for separated vernier thresholds [t(28) = −2.52, p = 0.018, Bonferroni corrected; Cohen’s d = −0.96, effect size r =−0.43], with ASC observers’ thresholds being better than controls’. However, of greater interest than the mean difference between the groups is the relationship between abutting and separated vernier thresholds for the two groups as shown in Figure 1. In controls (filled points), the abutting and separated thresholds are unrelated (Pearson r = 0.13, p = 0.65). In ASC (open points), the abutting and separated thresholds rise in proportion to one another (Pearson r = 0.88, p < 0.0001). It would be expected that abutting and separated vernier thresholds would be unrelated, since in typical controls they have been shown to be determined by two separate mechanisms. As previously outlined, abutting thresholds are determined by contrast-dependent spatial filters encompassing both elements [5,6], whilst separated thresholds are determined by a two-step process of local sign designation followed by comparison of features [6-8]. The results of the control observers are consistent with these findings. The finding of a strong correlation between abutting and separated vernier thresholds in the ASC observers suggests that their thresholds for the two conditions may be determined by the same mechanism. People with Table 1 Sample characteristics ASC (n = 16) Controls (n = 14) Two-tailed independent t-test (Levene > 0.05; equal variances assumed) Mean ± SD (range) Mean ± SD (range) Age 34.4±9.8 years (20–54 years) 38.1 ± 6.3 years (26–48 years) t = 1.19, df28, p = 0.24 Gender 9 female, 7 male 6 female, 8 male Pearson chi-square 0.54, p = 0.46 WASI 120.5 ± 10.9 (99–135) 115.5 ± 9.4 (100–130) t = 1.30, df26, p = 0.20 AQ 40.7 ± 4.6 (29–48) 12.4 ± 4.3 (4–21) t =16.6, df28, p < 0.0001 VA −0.15 ± 0.09 logMAR (0.00 - -0.28) −0.16 ± 0.10 logMAR (0.00 - -0.30) t = 0.27 df27 p = 0.79 Table 2 Group-mean vernier thresholds (± SD) in log sec arc, taken as the geometric mean of two blocks of responses for each participant ASC Control Abutting 1.16 ± 0.20 1.21 ± 0.20 Separated 1.35 ± 0.20 1.52 ± 0.15 Latham et al. Molecular Autism 2013, 4:4 Page 3 of 4 molecularautism/content/4/1/4ASC may have spatial filters that act over greater separations than in control observers, such that they do not need to switch to a comparison mechanism at a 10 arc min separation. However, it is not clear how such larger spatial filters would have the capacity to retain a high accuracy of vernier judgement. Future work to test this hypothesis might include an exploration of the influence of contrast [5], reverse polarity elements [6] or spatial frequency masks [13] on the separated vernier thresholds of observers with ASC. The finding of differences in ASC in the mechanisms used to determine vernier thresholds is not consistent with visual differences in autism being solely due to changes in higher level attention rather than early sensory processing [2,14], nor are the findings consistent with the suggestion that visual thresholds for tasks with two stages of processing, such as the separated vernier task, are poorer in ASC because of atypical cortical lateral connectivity [15]. Neuroanatomical studies suggest high local connectivity between smaller minicolumns in the autistic primary visual cortex [16] that might be implicated in differences in threshold mechanisms in people with ASC, and atypical lateral connectivity has also been suggested to explain psychophysical findings of better contrast detection in the presence of lateral masks in ASC [17]. Enhanced performance in ASC has been shown for visual simultaneity thresholds [18], a localisation task in the temporal domain, which is similar to the task reported here in the spatial domain. In conclusion, we show that vernier thresholds for abutting and separated vernier stimuli are not related in controls but are strongly correlated in ASC, suggesting that people with ASC employ different mechanisms than controls in processing separated vernier stimuli. These findings provide psychophysical evidence of a difference in visual processing in ASC at an early stage of cortical visual processing and demonstrate that visual changes in ASC are not restricted to higher level perceptual processes. Abbreviations ASC: Autism spectrum conditions; AQ: Autism Spectrum Quotient; IQ: Intelligence Quotient; WASI: Wechsler Abbreviated Scale of Intelligence. Competing interests The authors declare that they have no competing interests. Authors’ contributions KL conceived of the study, participated in the data collection, analysed the data and led preparation of the manuscript. SC conceived of the study, programmed the stimuli and analysed the data. PA and TT participated in the design of the study and data collection. SBC participated in the design of study. All authors helped to draft and revise the manuscript and have read and approved the final manuscript. Acknowledgements We thank the participants and Dennis Levi and Caroline Robertson for helpful comments. TT was supported by the Pinsent Darwin Trust and Autistica, and SBC by the MRC UK and the Wellcome Trust. The study was conducted in association with the NIHR CLAHRC for Cambridgeshire and Peterborough NHS Trust. Author details 1 Department of Vision & Hearing Sciences, Anglia Ruskin University, Cambridge, UK. 2 Vision and Eye Research Unit, Anglia Ruskin University, Cambridge, UK. 3 School of Optometry, University of California, Berkeley, CA, USA. 4 Department of Psychiatry, Autism Research Centre, Cambridge University, Cambridge, UK. 5 Department of Psychiatry, Seaver Autism Centre, Mount Sinai School of Medicine, New York, NY, USA. Received: 21 September 2012 Accepted: 31 January 2013 Published: 19 February 2013 References 1. Tavassoli T, Latham K, Bach M, Dakin SC, Baron-Cohen S: Psychophysical measures of visual acuity in Autism Spectrum Conditions. Vision Res 2011, 51:1778–1780. 2. Dakin SC, Frith U: Vagaries of visual perception in autism. Neuron 2005, 48:497–507. 3. Simmons DR, Robertson AE, McKay LS, Toal E, McAleer P, Pollick FE: Vision in autism spectrum disorders. Vision Res 2009, 49:2705–2739. 4. 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