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Access to awareness of direct gaze is related to autistic traits

Published online by Cambridge University Press:  27 June 2018

Apoorva Rajiv Madipakkam ,
Marcus Rothkirch ,
Isabel Dziobek  and
Philipp Sterzer
Apoorva Rajiv Madipakkam*
Affiliation:
Visual Perception Laboratory, Department of Psychiatry, Charité – Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117 Berlin, Germany International Graduate Program Medical Neurosciences, Charité – Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Luisenstr. 56, 10117 Berlin, Germany
Marcus Rothkirch
Affiliation:
Visual Perception Laboratory, Department of Psychiatry, Charité – Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117 Berlin, Germany
Isabel Dziobek
Affiliation:
Berlin School of Mind and Brain, Institute of Psychology, Humboldt Universität zu Berlin, Unter den Linden 6, 10099 Berlin, Germany
Philipp Sterzer
Affiliation:
Visual Perception Laboratory, Department of Psychiatry, Charité – Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, 10117 Berlin, Germany Berlin School of Mind and Brain, Institute of Psychology, Humboldt Universität zu Berlin, Unter den Linden 6, 10099 Berlin, Germany
*
Author for correspondence: Apoorva Rajiv Madipakkam, E-mail: [email protected]
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Abstract

Background

The atypical processing of eye contact is a characteristic hallmark of autism spectrum disorder (ASD). The severity of these symptoms, however, is thought to lie on a continuum that extends into the typical population. While behavioural evidence shows that differences in social cognitive tasks in typically developed (TD) adults are related to the levels of autistic-like traits, it remains unknown whether such a relation exists for the sensitivity to direct gaze.

Methods

In two experiments, we measured reaction times to detect the faces with direct and averted gaze, suppressed from awareness, i.e. the access to awareness. In experiment 1, we tested N = 19 clinically diagnosed adults with ASD and N = 22 TD matched controls, while in experiment 2, we tested an independent sample of N = 20 TD adults.

Results

In line with the literature, experiment 1 showed preferential processing of direct gaze in the TD group but not in the ASD group. Importantly, we found a linear relationship in both experiments between the levels of autistic traits within the groups of TD participants and their sensitivity to direct gaze: with increasing autistic characteristics, there was a decrease in sensitivity to direct gaze.

Conclusion

These results provide the first evidence that differences in gaze processing and the sensitivity to direct gaze are already present in individuals with subclinical levels of autistic traits. Furthermore, they lend support to the continuum view of the disorder and could potentially help in an earlier diagnosis of individuals at high risk for autism.

Keywords

Autism spectrum disorderbreaking continuous flash suppressioncontinuum vieweye gaze processing
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 6 , April 2019 , pp. 980 - 986
Copyright
Copyright © Cambridge University Press 2018 

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References

Akechi, H, Stein, T, Senju, A, Kikuchi, Y, Tojo, Y, Osanai, H and Hasegawa, T (2014) Absence of preferential unconscious processing of eye contact in adolescents with autism spectrum disorder. Autism Research 7, 590–597.Google Scholar
Baron-Cohen, S (1997) Mindblindness: an Essay on Autism and Theory of Mind. Cambridge, Massachusetts, UK: MIT Press.Google Scholar
Baron-Cohen, S, Wheelwright, S, Skinner, R, Martin, J and Clubley, E (2001) The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders 31, 5–17.Google Scholar
Bates, ME and Lemay, EP (2004) The d2 test of attention: construct validity and extensions in scoring techniques. Journal of the International Neuropsychological Society: JINS 10, 392–400.Google Scholar
Bayliss, AP and Tipper, SP (2005) Gaze and arrow cueing of attention reveals individual differences along the autism spectrum as a function of target context. British Journal of Psychology 96, 95–114.Google Scholar
Bayliss, AP and Tipper, SP (2006) Predictive gaze cues and personality judgments. Psychological Science 17, 514–520.Google Scholar
Chen, FS and Yoon, JMD (2011) Brief report: broader autism phenotype predicts spontaneous reciprocity of direct gaze. Journal of Autism and Developmental Disorders 41, 1131–1134.Google Scholar
Chen, Y-C and Yeh, S-L (2012) Look into my eyes and I will see you: unconscious processing of human gaze. Consciousness and Cognition 21, 1703–1710.Google Scholar
Constantino, JN and Todd, RD (2003) Autistic traits in the general population: a twin study. Archives of General Psychiatry 60, 524–530.Google Scholar
Cousineau, D (2005) Confidence intervals in within-subject designs: a simpler solution to Loftus and Masson's method. Tutorial Quantitative Methods for Psychology 1, 42–45.Google Scholar
Dalton, KM, Nacewicz, BM, Alexander, AL and Davidson, RJ (2007) Gaze-fixation, brain activation, and amygdala volume in unaffected siblings of individuals with autism. Biological Psychiatry 61, 512–520.Google Scholar
David, AS (2010) Why we need more debate on whether psychotic symptoms lie on a continuum with normality. Psychological Medicine 40, 1935–1942.Google Scholar
Elsabbagh, M, Mercure, E, Hudry, K, Chandler, S, Pasco, G, Charman, T, Pickles, A, Baron-Cohen, S, Bolton, P and Johnson, MH (2012) Infant neural sensitivity to dynamic eye gaze is associated with later emerging autism. Current Biology 22, 338–342.Google Scholar
Farroni, T, Csibra, G, Simion, F and Johnson, MH (2002) Eye contact detection in humans from birth. Proceedings of the National Academy of Sciences 99, 9602–9605.Google Scholar
Folstein, S and Rutter, M (1977) Genetic influences and infantile autism. Nature 265, 726–728.Google Scholar
Foulkes, L, Bird, G, Gökçen, E, McCrory, E and Viding, E (2015) Common and distinct impacts of autistic traits and alexithymia on social reward. PLoS ONE 10, e0121018.Google Scholar
Frith, CD and Frith, U (2006) The neural basis of mentalizing. Neuron 50, 531–534.Google Scholar
Gayet, S, Van der Stigchel, S and Paffen, CL (2014) Breaking continuous flash suppression: competing for consciousness on the pre-semantic battlefield. Frontiers in Psychology 5.Google Scholar
Hains, SMJ and Muir, DW (1996) Infant sensitivity to adult eye direction. Child Development 67, 1940–1951.Google Scholar
Horley, K, Williams, LM, Gonsalvez, C and Gordon, E (2003) Social phobics do not see eye to eye:: a visual scanpath study of emotional expression processing. Journal of Anxiety Disorders 17, 33–44.Google Scholar
Hudson, M, Nijboer, TCW and Jellema, T (2012) Implicit social learning in relation to autistic-like traits. Journal of Autism and Developmental Disorders 42, 2534–2545.Google Scholar
Jameel, L, Vyas, K, Bellesi, G, Roberts, V and Channon, S (2014) Going ‘above and beyond’: are those high in autistic traits less pro-social? Journal of Autism and Developmental Disorders 44, 1846–1858.Google Scholar
Kanner, L (1943) Autistic disturbances of affective contact. Nervous Child 2, 217–250.Google Scholar
Katarzyna, C, Fred, V and Ami, K (2010) Limited attentional bias for faces in toddlers with autism spectrum disorders. Archives of General Psychiatry 67, 178–185.Google Scholar
Kleinke, CL (1986) Gaze and eye contact: a research review. Psychological Bulletin 100, 78.Google Scholar
Kliemann, D, Dziobek, I, Hatri, A, Steimke, R and Heekeren, HR (2010) Atypical reflexive gaze patterns on emotional faces in autism spectrum disorders. Journal of Neuroscience 30, 12281–12287.Google Scholar
Lehrl, S, Triebig, G and Fischer, B (1995) Multiple choice vocabulary test MWT as a valid and short test to estimate premorbid intelligence. Acta Neurologica Scandinavica 91, 335–345.Google Scholar
Lord, C, Risi, S, Lambrecht, L, Cook, EH, Leventhal, BL, DiLavore, PC, Pickles, A and Rutter, M (2000) The autism diagnostic observation schedule – generic: a standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders 30, 205–223.Google Scholar
Madipakkam, AR, Rothkirch, M, Dziobek, I and Sterzer, P (2017) Unconscious avoidance of eye contact in autism spectrum disorder. Scientific Reports 7, 13378.Google Scholar
Madipakkam, AR, Rothkirch, M, Guggenmos, M, Heinz, A and Sterzer, P (2015) Gaze direction modulates the relation between neural responses to faces and visual awareness. The Journal of Neuroscience 35, 13287–13299.Google Scholar
Mareschal, I, Calder, AJ and Clifford, CWG (2013) Humans have an expectation that gaze is directed toward them. Current Biology 23, 717–721.Google Scholar
McPartland, J, Dawson, G, Webb, SJ, Panagiotides, H and Carver, LJ (2004) Event-related brain potentials reveal anomalies in temporal processing of faces in autism spectrum disorder. Journal of Child Psychology and Psychiatry, and Allied Disciplines 45, 1235–1245.Google Scholar
Nummenmaa, L, Engell, AD, von dem Hagen, E, Henson, RNA and Calder, AJ (2012) Autism spectrum traits predict the neural response to eye gaze in typical individuals. NeuroImage 59, 3356–3363.Google Scholar
Pierce, K, Conant, D, Hazin, R, Stoner, R and Desmond, J (2011) Preference for geometric patterns early in life as a risk factor for autism. Archives of General Psychiatry 68, 101–109.Google Scholar
Redcay, E (2008) The superior temporal sulcus performs a common function for social and speech perception: implications for the emergence of autism. Neuroscience and Biobehavioral Reviews 32, 123–142.Google Scholar
Rothkirch, M, Madipakkam, AR, Rehn, E and Sterzer, P (2015) Making eye contact without awareness. Cognition 143, 108–114.Google Scholar
Satzger, W, Fessmann, H and Engel, RR (2002) Liefern HAWIE-R, WST und MWT-B vergleichbare IQ-Werte? Zeitschrift für Differentielle und Diagnostische Psychologie 23, 159–170.Google Scholar
Schurger, A (2009) A very inexpensive MRI-compatible method for dichoptic visual stimulation. Journal of Neuroscience Methods 177, 199–202.Google Scholar
Senju, A and Johnson, MH (2009) The eye contact effect: mechanisms and development. Trends in Cognitive Sciences 13, 127–134.Google Scholar
Senju, A, Tojo, Y, Yaguchi, K and Hasegawa, T (2005) Deviant gaze processing in children with autism: an ERP study. Neuropsychologia 43, 1297–1306.Google Scholar
Stein, T, Senju, A, Peelen, MV and Sterzer, P (2011) Eye contact facilitates awareness of faces during interocular suppression. Cognition 119, 307–311.Google Scholar
Stein, T and Sterzer, P (2014) Unconscious processing under interocular suppression: getting the right measure. Frontiers in Psychology 5, 1–5.Google Scholar
Tong, F, Meng, M and Blake, R (2016) Neural bases of binocular rivalry. Trends in Cognitive Sciences 10, 502–511.Google Scholar
von dem Hagen, EAH, Nummenmaa, L, Yu, R, Engell, AD, Ewbank, MP and Calder, AJ (2011) Autism spectrum traits in the typical population predict structure and function in the posterior superior temporal sulcus. Cerebral Cortex (New York, NY) 21, 493–500.Google Scholar
Wing, L (1988) The continuum of autistic characteristics. In Schopler, E and Mesibov, GB (eds), Diagnosis and Assessment in Autism. Current Issues in Autism, USA. Boston, MA: Springer, pp. 91–110.Google Scholar
Wittorf, A, Wiedemann, G and Klingberg, S (2014) Multiple-choice vocabulary intelligence test MWT in schizophrenia: valid measure of premorbid intelligence? Psychiatrische Praxis 41, 95–100.Google Scholar
Woodbury-Smith, MR, Robinson, J, Wheelwright, S and Baron-Cohen, S (2005) Screening adults for Asperger syndrome using the AQ: a preliminary study of its diagnostic validity in clinical practice. Journal of Autism and Developmental Disorders 35, 331–335.Google Scholar
Zhao, S, Uono, S, Yoshimura, S and Toichi, M (2015) Is impaired joint attention present in non-clinical individuals with high autistic traits? Molecular Autism 6, 67.Google Scholar