Color afterimages in autistic adults Article (Published Version) Maule, John, Stanworth, Kirstie, Pellicano, Elizabeth and Franklin, Anna (2018) Color afterimages in autistic adults. Journal of Autism and Developmental Disorders, 48 (4). pp. 1409-1421. ISSN 0162-3257 This version is available from Sussex Research Online: http://sro.sussex.ac.uk/id/eprint/61156/ This document is made available in accordance with publisher policies and may differ from the published version or from the version of record. If you wish to cite this item you are advised to consult the publisher’s version. Please see the URL above for details on accessing the published version. Copyright and reuse: Sussex Research Online is a digital repository of the research output of the University. Copyright and all moral rights to the version of the paper presented here belong to the individual author(s) and/or other copyright owners. To the extent reasonable and practicable, the material made available in SRO has been checked for eligibility before being made available. Copies of full text items generally can be reproduced, displayed or performed and given to third parties in any format or medium for personal research or study, educational, or not-for-profit purposes without prior permission or charge, provided that the authors, title and full bibliographic details are credited, a hyperlink and/or URL is given for the original metadata page and the content is not changed in any way. http://sro.sussex.ac.uk J Autism Dev Disord DOI 10.1007/s10803-016-2786-5 S.I. : LOCAL VS. GLOBAL PROCESSING IN AUTISM SPECTRUM DISORDERS Color Afterimages in Autistic Adults 1 1 2 1 John Maule • Kirstie Stanworth • Elizabeth Pellicano • Anna Franklin Ó The Author(s) 2016. This article is published with open access at Springerlink.com Abstract It has been suggested that attenuated adaptation Introduction to visual stimuli in autism is the result of atypical per- ceptual priors (e.g., Pellicano and Burr in Trends Cogn Sci Autism is characterized by difficulties in social communi- 16(10):504–510, 2012. doi:10.1016/j.tics.2012.08.009). cation and behavioral traits including rigid patterns of This study investigated adaptation to color in autistic behavior, preference for sameness, and intense and adults, measuring both strength of afterimage and the restricted interests (American Psychiatric Association influence of top-down knowledge. We found no difference 2013). Sensory symptoms, including both hyper-reactivity in color afterimage strength between autistic and typical and hypo-reactivity to external stimuli, atypicalities in adults. Effects of top-down knowledge on afterimage sensory processing and unusual sensory interests are now intensity shown by Lupyan (Acta Psychol 161:117–130, included in the most recent revision of the diagnostic cri- 2015. doi:10.1016/j.actpsy.2015.08.006) were not repli- teria for autism (Diagnostic and Statistical Manual of cated for either group. This study finds intact color adap- Mental Disorders, Fifth Edition (DSM-5) (American Psy- tation in autistic adults. This is in contrast to findings of chiatric Association 2013). This inclusion implies that they attenuated adaptation to faces and numerosity in autistic are part of the core of autism, with such atypical sensory children. Future research should investigate the possibility experiences potentially also being related to other key of developmental differences in adaptation and further features of the condition (Pellicano 2013). examine top-down effects on adaptation. There has been a recent influx of hypotheses attempting to account for these sensory and perceptual differences in Keywords Autism Á Afterimages Á Adaptation Á Color Á particular. Bayesian accounts of perception propose that Top-down knowledge information from sensory input is combined with prior knowledge or experience to facilitate the interpretation of the sensory information (e.g. Knill and Pouget 2004; & John Maule Kersten et al. 2004). Pellicano and Burr’s (2012) hypo- [email protected] priors account posits, within a Bayesian framework, that an Kirstie Stanworth under-weighting (relative to typical individuals) of the [email protected] strength of prior information when interpreting sensory Elizabeth Pellicano information may underlie autistic sensation and perception. [email protected] Building on this work, others have proposed accounts of Anna Franklin atypical (rather than simply reduced) priors in autism (e.g., [email protected] Hellendoorn et al. 2015), and predictive coding accounts of autistic perception (Friston et al. 2013; Lawson et al. 2014; 1 The Sussex Colour Group, School of Psychology, University of Sussex, Pevensey II 5B7, Brighton BN1 9QH, UK Sinha et al. 2014; Van de Cruys et al. 2013). One sensory process that could be affected by under- 2 Centre for Research in Autism and Education (CRAE), UCL Institute of Education, University College London, London, weighting of prior information is adaptation (Pellicano and UK Burr 2012). Adaptation is a fundamental property of neural 123 J Autism Dev Disord networks and describes changes in neural activity in questions—first, do claims for attenuated adaptation in response to a persistent stimulus (Kohn 2007). Adaptation autism generalize beyond face perception to other is thought to serve a crucial function for sensory systems, domains? And, second, do claims for attenuated adaptation tuning neural responses to maximize sensitivity to the in autism generalize from childhood to adulthood? We range of stimuli present in the immediate environment (e.g. investigate these issues with regards to adaptation to a low- Webster 2011). Adaptation to visual stimuli can result in level visual attribute, color. the experience of aftereffects—distortions in perception Adaptation to color can be demonstrated by the phe- which tend to bias perception in the opposite direction to nomenon of color afterimages—an observer who stares at a that adapted (e.g. adaptation to a grating tilted to the left, colored patch for a few seconds will experience an afterim- causes a vertical grating to appear tilted slightly to the right age of the patch in the opponent color (e.g. afterimage of (Clifford 2012). Since adaptation afterimages are directly lime-green following adaptation to magenta) if they look at a related to the recent sensory input of the beholder, whereby uniform white field (Wheatstone 1838). The locus of adap- prior sensory experiences are used to calibrate sensory tation which causes color afterimages has been the subject of systems and hence bias current perception, adaptation discussion, and the current evidence suggests that color afterimages should therefore be attenuated in autism (Pel- afterimages are instantiated by adaptation of photoreceptors licano and Burr 2012). in the retina and retinal ganglion cells, but may then be Several studies have found differences in adaptation subject to further modulation by cortical processes (Zaidi aftereffects in autism. Research on high-level face identity et al. 2012). For example, if an observer is alternately shown aftereffects has shown that they are weaker in autistic a vertical grating on a red background and a horizontal compared to typical children (Ewing et al. 2013a; Rhodes grating on a green background for around 2 min they will et al. 2014), and that the strength of the aftereffect corre- subsequently perceive a reddish tinge to a horizontal grating lates significantly with autistic features, such that those on a white background, and a greenish tinge on a vertical with greater degrees of autistic features have the smallest grating on a white background (McCollough 1965). This is aftereffects (Pellicano et al. 2007). Subsequent work has known as the McCollough effect, and is most likely mediated shown that adaptation is diminished in autistic children for by processes in early visual cortex (area V1; Vul and facial configuration (Ewing et al. 2013b), facial emotion MacLeod 2006), not just at the level of the retina. (Rutherford et al. 2012) and eye-gaze direction (Pellicano The primary aim of the current study was to investigate et al. 2013). There is also evidence for slightly reduced face whether color adaptation is reduced in autistic individuals, as identity aftereffects in parents (and siblings) of autistic has been shown previously for faces and numerosity. There children, suggesting that reduced adaptation may be a is already evidence that autistic children differ from their feature of the broad endophenotype of autism (Fiorentini typically developing peers in both color discrimination and et al. 2012). Two studies involving autistic adults, rather memory, at least under some conditions (Cranwell et al. than children, have failed to find evidence of reduced 2015; Franklin et al. 2008; Fujita et al. 2011; Heaton et al. adaptation to facial identity and emotion (Cook et al. 2014) 2008; but see also Koh et al. 2010). There is also anecdotal and figural contraction/expansion (Walsh et al. 2015), and case study evidence for enhanced color associations indicating that the differences apparent in childhood may (both phobias and intense interests) in autism (Ludlow et al. reflect a developmental delay rather than a deficit as such. 2014) and hyper-sensitivity to certain colors, ambient More recent work has attempted to determine the perva- lighting and colored patterns (Robertson and Simmons siveness of reduced adaptation in autism by examining the 2015). Together these studies suggest that various aspects of nature