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PUPILLOMETRY reflected in the eyes People with higher autistic traits display stronger fluctuations in size when presented with an optical .

WOON JU PARK, KIMBERLY B SCHAUDER AND DUJE TADIN

example, it enables us to communicate with Related research article Turi M, Burr DC, patients suffering from ‘locked-in’ syndrome – a Binda P. 2018. Pupillometry reveals percep- condition characterized by the paralysis of every tual differences that are tightly linked to muscle except the eye (Stoll et al., 2013). autistic traits in typical adults. eLife 7: Now, in eLife, Marco Turi, David Burr and e32399. DOI: 10.7554/eLife.32399 Paola Binda – who are based at research insti- tutes in Pisa, Florence and Sydney – report that fluctuations in pupil size may provide insight into clinical disorders (Turi et al., 2018). The researchers used a well-known optical cylinder ost of the tasks that our brain orches- illusion that consists of two overlapping sets of trates in our body are performed out- black and white dots moving in opposite direc- M side of our conscious awareness. In tions on a 2D plane (Figure 1A). Due to the dif- addition to breathing, maintaining our balance ferent speeds of the dots, anyone looking at the and keeping our heart beating, these tasks dots usually sees a rotating 3D cylinder include increasing or decreasing the size of our (Andersen and Bradley, 1998; Video 1 in as our environment becomes darker or Turi et al., 2018). However, since the resulting lighter. This allows us to see in both darkened illusion makes it difficult to detect which color is rooms and on bright sunny days. Although the at the front (and, thus, the direction of rotation), area of a pupil can change by as much as a fac- our selects one interpretation at tor of ten (Winn et al., 1994), we are not aware any given time. As a result, the perceived rota- of the small movements in the ocular muscles tion switches direction every few seconds that open and close our pupils. (Figure 1B). Such approaches, where the physi- Recent studies have painted a complex and cal stimulus remains constant but our subjective fascinating picture of what drives these changes changes, have been widely used to in pupil size. Despite representing the lowest study the mechanisms underlying visual aware- level of visual function, these pupil dynamics can ness (Kim and Blake, 2005). reflect sophisticated processes that are closely To track any subjective change in perception, linked to our everyday experience (including the participants reported how they experienced attention, decision making, and even aesthetic the rotation of the cylinder, while the research- experiences; Binda and Murray, 2015; ers measured the pupil size. Although the overall Copyright Park et al. This article is Hartmann and Fischer, 2014). Therefore, meas- intensity of light (the primary factor influencing distributed under the terms of the urements of the pupils, also known as pupillome- pupil size) remained constant, the size of the Creative Commons Attribution try, may be used as an indicator for cognitive pupils changed: the pupils became larger when License, which permits unrestricted and perceptual states. This method is also objec- the black dots seemed to be in the front, but use and redistribution provided that the original author and source are tive and non-invasive, and can, therefore be became smaller, when the white dots appeared credited. applied in a wide range of clinical contexts. For to be in front (Figure 1C).

Park et al. eLife 2018;7:e35374. DOI: https://doi.org/10.7554/eLife.35374 1 of 3 Insight Pupillometry Consciousness reflected in the eyes

Figure 1. Changes in pupil size depend on subjective . (A) Turi et al. used a visual stimulus in which two sets of dots (white and black) moved in opposite directions (thin arrows). (B) To an observer this stimulus appears as a 3D cylinder that rotates in a clockwise direction with the black dots at the front (top), or in a counter-clockwise direction with the white dots at the front (bottom). This perceived direction of rotation switches every few seconds. (C) Turi et al. found that pupil size increased when the black dots appeared to be at the front, and decreased when the white dots appeared to be at the front. The size of this change was correlated with Autism-Spectrum Quotient score.

In some participants, the size of the pupils size, because their focus alternates between changed substantially between the black and black and white dots. This observation is tightly white phases, while in others the changes were linked with the long-standing hypothesis that only minimal. Turi et al. revealed that these dif- individuals with autism spectrum disorders tend ferences strongly correlated with the Autism- to focus more on the detail rather than the big- Spectrum Quotient (AQ) scores of the partici- ger picture (Happe´ and Frith, 2006). pants (Baron-Cohen et al., 2001). The higher The findings of Turi et al. provide compelling the number of autistic traits reported by an indi- evidence that the size of a pupil reflects subjec- vidual in the AQ questionnaire, the stronger the tive differences in a way that is highly correlated changes in pupil size became. This effect to the reported autistic traits of the participants. accounted for about half of the variance in AQ The study provides numerous possibilities to scores, which is considerably higher than the investigate higher-level cognitive processes. This sizes of the effects reported for other sensory can be particularly valuable when studying indi- measures (e.g., Ujiie et al., 2015). viduals who may find it difficult to engage in Turi et al. argue that the changes in pupil size complex behavioral tasks, such as individuals reflect how individuals process visual information with minimal language skills or deficits in other differently. Some people tend to focus on small, cognitive abilities. Pupillometry is clearly a pow- defined areas such as the surface at the front, erful tool for characterizing the individual differ- while others concentrate on the entire cylinder. ences in processing visual information and, Consequently, people with a more detailed potentially, for advancing our understanding of focus should have more fluctuations in pupil autism spectrum disorders.

Park et al. eLife 2018;7:e35374. DOI: https://doi.org/10.7554/eLife.35374 2 of 3 Insight Pupillometry Consciousness reflected in the eyes

Woon Ju Park is in the Center for Visual Science and Disorders 31:5–17. DOI: https://doi.org/10.1023/A: the Department of Brain and Cognitive Sciences, 1005653411471, PMID: 11439754 University of Rochester, Rochester, United States. Binda P, Murray SO. 2015. Keeping a large-pupilled [email protected] eye on high-level . Trends in Cognitive Sciences 19:1–3. DOI: https://doi.org/10. http://orcid.org/0000-0003-1473-4876 1016/j.tics.2014.11.002, PMID: 25467128 Kimberly B Schauder is in the Center for Visual Happe´ F, Frith U. 2006. The weak coherence account: Science and the Department of Clinical and Social detail-focused cognitive style in autism spectrum Sciences in Psychology, University of Rochester, disorders. Journal of Autism and Developmental Rochester, United States. Disorders 36:5–25. DOI: https://doi.org/10.1007/ [email protected] s10803-005-0039-0, PMID: 16450045 http://orcid.org/0000-0001-6832-1044 Hartmann M, Fischer MH. 2014. Pupillometry: the eyes shed fresh light on the mind. Current Biology 24: Duje Tadin is in the Center for Visual Science and the R281–R282. DOI: https://doi.org/10.1016/j.cub.2014. Department of Brain and Cognitive Sciences, 02.028, PMID: 24698378 University of Rochester, Rochester, United States, and Kim CY, Blake R. 2005. Psychophysical magic: the Departments of Ophthalmology and Neuroscience, rendering the visible ’invisible’. Trends in Cognitive University of Rochester School of Medicine, Rochester, Sciences 9:381–388. DOI: https://doi.org/10.1016/j. United States. tics.2005.06.012, PMID: 16006172 Stoll J, Chatelle C, Carter O, Koch C, Laureys S, [email protected] Einha¨ user W. 2013. Pupil responses allow https://orcid.org/0000-0003-1571-5589 communication in locked-in syndrome patients. Current Biology 23:R647–R648. DOI: https://doi.org/ Competing interests: The authors declare that no 10.1016/j.cub.2013.06.011, PMID: 23928079 competing interests exist. Turi M, Burr DC, Binda P. 2018. Pupillometry reveals Published 06 March 2018 perceptual differences that are tightly linked to autistic traits in typical adults. eLife 7:e32399. DOI: https://doi. org/10.7554/eLife.32399 References Ujiie Y, Asai T, Wakabayashi A. 2015. The relationship Andersen RA, Bradley DC. 1998. Perception of three- between level of autistic traits and local bias in the dimensional structure from motion. Trends in context of the McGurk effect. Frontiers in Psychology Cognitive Sciences 2:222–228. DOI: https://doi.org/10. 6:891. DOI: https://doi.org/10.3389/fpsyg.2015.00891, 1016/S1364-6613(98)01181-4, PMID: 21227176 PMID: 26175705 Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Winn B, Whitaker D, Elliott DB, Phillips NJ. 1994. Clubley E. 2001. The autism-spectrum quotient (AQ): Factors affecting light-adapted pupil size in normal evidence from Asperger syndrome/high-functioning human subjects. Investigative Ophthalmology & Visual autism, males and females, scientists and Science 35:1132–1137. PMID: 8125724 mathematicians. Journal of Autism and Developmental

Park et al. eLife 2018;7:e35374. DOI: https://doi.org/10.7554/eLife.35374 3 of 3