Performance in a gaze-cueing task is associated with autistic traits

Mariana FP de Araújo; Wagner A de Castro; Hiroshi Nishimaru; Susumu Urakawa; Taketoshi Ono; Hisao Nishijo; Mariana FP de Araújo; Wagner A de Castro; Hiroshi Nishimaru; Susumu Urakawa; Taketoshi Ono; Hisao Nishijo

doi:10.3934/Neuroscience.2021007

AIMS Neuroscience

2021, Volume 8, Issue 1: 148-160. doi: 10.3934/Neuroscience.2021007

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Performance in a gaze-cueing task is associated with autistic traits

1.
System Emotional Science, Graduate School of Medicine, University of Toyama, Toyama, Japan
2.
Department of Physiological Sciences, Health Sciences Center, Federal University of Espirito Santo, Vitoria-ES, Brazil
3.
Department of Musculoskeletal Functional Research and Regeneration, Graduate School of Biomedical and Health Sciences, Hiroshima University, Hiroshima, Japan
† Co-first authors.

Received: 21 September 2020 Accepted: 16 December 2020 Published: 17 December 2020

Individuals with autism spectrum disorder (ASD) show impairments in processing social cues such as facial expressions and gaze direction. Several researchers have proposed that autistic traits form a continuum that may be distributed within the general, typically developed, population. Accordingly, several studies have indicated that typically developed individuals with high levels of self-reported autistic traits have autistic-like performance in a variety of paradigms. Here, we designed a gaze-cueing task to examine whether gaze-triggered orienting is related to the extent of typically developed (TD) individuals' autistic traits (determined by their AQ test scores) and whether it is modulated by previous eye contact and different facial expressions. At each trial, TD subjects observed faces with or without eye contact. This facial stimulus then gazed toward the left or right side. Finally, a target appeared on the left or right side of the display and reaction time (RT) to the target was measured. RTs were modulated by congruency between gazing directions and target locations, and by prior eye contact in the congruent trials. In addition, individuals with higher AQ scores were slower at detecting the target when the cue was a happy face. Furthermore, faster RTs in congruent trials were associated with one specific autistic trait (attention switching deficits). Together, these results indicate that autistic traits may influence performance in a gaze cueing task.
- autistic traits,
- autism-spectrum quotient,
- cueing tasks,
- gaze-triggered orienting,
- feature-based perception,
- attention switching deficits,
- over-focused attention
Citation: Mariana FP de Araújo, Wagner A de Castro, Hiroshi Nishimaru, Susumu Urakawa, Taketoshi Ono, Hisao Nishijo. Performance in a gaze-cueing task is associated with autistic traits[J]. AIMS Neuroscience, 2021, 8(1): 148-160. doi: 10.3934/Neuroscience.2021007

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Abstract

Individuals with autism spectrum disorder (ASD) show impairments in processing social cues such as facial expressions and gaze direction. Several researchers have proposed that autistic traits form a continuum that may be distributed within the general, typically developed, population. Accordingly, several studies have indicated that typically developed individuals with high levels of self-reported autistic traits have autistic-like performance in a variety of paradigms. Here, we designed a gaze-cueing task to examine whether gaze-triggered orienting is related to the extent of typically developed (TD) individuals' autistic traits (determined by their AQ test scores) and whether it is modulated by previous eye contact and different facial expressions. At each trial, TD subjects observed faces with or without eye contact. This facial stimulus then gazed toward the left or right side. Finally, a target appeared on the left or right side of the display and reaction time (RT) to the target was measured. RTs were modulated by congruency between gazing directions and target locations, and by prior eye contact in the congruent trials. In addition, individuals with higher AQ scores were slower at detecting the target when the cue was a happy face. Furthermore, faster RTs in congruent trials were associated with one specific autistic trait (attention switching deficits). Together, these results indicate that autistic traits may influence performance in a gaze cueing task.

Acknowledgments

This work was supported by University of Toyama.

Author contributions

W.A.C, M.F.P.A. and H.Nishij. designed the experiments. W.A.C. collected the data. W.A.C. and M.F.P.A. analyzed the data. W.A.C, M.F.P.A., H.Nishij., S.U., T.O. and H.Nishim. discussed the results. W.A.C, M.F.P.A and H.Nishij. wrote the paper. All authors revised the paper.

Conflict of interest

The authors declare no conflict of interest.

References

[1]	Nation K, Penny S (2008) Sensitivity to eye gaze in autism: Is it normal? Is it automatic? Is it social? Dev Psychopathol 20: 79-97. doi: 10.1017/S0954579408000047
[2]	Senju A, Johnson MH (2009) Atypical eye contact in autism: Models, mechanisms and development. Neurosci Biobehav Rev 33: 1204-1214. doi: 10.1016/j.neubiorev.2009.06.001
[3]	Akechi H, Senju A, Kikuchi Y, et al. (2010) The effect of gaze direction on the processing of facial expressions in children with autism spectrum disorder: An ERP study. Neuropsychologia 48: 2841-2851. doi: 10.1016/j.neuropsychologia.2010.05.026
[4]	Pelphrey K, Goldman BD, Pelphrey KA, et al. (2002) Visual Scanning of Faces in Autism. J Autism Dev Disord 32: 249-261. doi: 10.1023/A:1016374617369
[5]	Nakano T, Tanaka K, Endo Y, et al. (2010) Atypical gaze patterns in children and adults with autism spectrum disorders dissociated from developmental changes in gaze behaviour. Proc Biol Sci 277: 2935-2943.
[6]	Kliemann D, Dziobek I, Hatri A, et al. (2010) Atypical reflexive gaze patterns on emotional faces in autism spectrum disorders. J Neurosci 30: 12281-12287. doi: 10.1523/JNEUROSCI.0688-10.2010
[7]	Tanaka JW, Sung A (2016) The “Eye Avoidance” Hypothesis of Autism Face Processing. J Autism Dev Disord 46: 1538-1552. doi: 10.1007/s10803-013-1976-7
[8]	Pitskel NB, Bolling DZ, Hudac CM, et al. (2011) Brain mechanisms for processing direct and averted gaze in individuals with autism. J Autism Dev Disord 41: 1686-1693. doi: 10.1007/s10803-011-1197-x
[9]	Itier RJ, Batty M (2009) Neural bases of eye and gaze processing: the core of social cognition. Neurosci Biobehav Rev 33: 843-863. doi: 10.1016/j.neubiorev.2009.02.004
[10]	Hori E, Tazumi T, Umeno K, et al. (2005) Effects of facial expression on shared attention mechanisms. Physiol Behav 84: 397-405. doi: 10.1016/j.physbeh.2005.01.002
[11]	Kompatsiari K, Ciardo F, Tikhanoff V, et al. (2018) On the role of eye contact in gaze cueing. Sci Rep 8: 1-10. doi: 10.1038/s41598-018-36136-2
[12]	Baron-Cohen S, Wheelwright S, Skinner R, et al. (2001) The Autism-Spectrum Quotient (AQ): Evidence from asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord 31: 5-17. doi: 10.1023/A:1005653411471
[13]	Wheelwright S, Auyeung B, Allison C, et al. (2010) Defining the broader, medium and narrow autism phenotype among parents using the Autism Spectrum Quotient (AQ). Mol Autism 1: 1-9. doi: 10.1186/2040-2392-1-10
[14]	Chen FS, Yoon JMD (2010) Brief report: Broader autism phenotype predicts spontaneous reciprocity of direct gaze. J Autism Dev Disord 41: 1131-1134. doi: 10.1007/s10803-010-1136-2
[15]	Ingersoll B (2010) Broader autism phenotype and nonverbal sensitivity: evidence for an association in the general population. J Autism Dev Disord 40: 590-598. doi: 10.1007/s10803-009-0907-0
[16]	Valla JM, Maendel JW, Ganzel BL, et al. (2013) Autistic trait interactions underlie sex-dependent facial recognition abilities in the normal population. Front Psychol 4: 1-6. doi: 10.3389/fpsyg.2013.00286
[17]	Sevgi M, Diaconescu AO, Henco L, et al. (2020) Social Bayes: Using Bayesian Modeling to Study Autistic Trait–Related Differences in Social Cognition. Biol Psychiatry 87: 185-193. doi: 10.1016/j.biopsych.2019.09.032
[18]	Hudson M, Nijboer TCW, Jellema T (2012) Implicit social learning in relation to autistic-like traits. J Autism Dev Disord 42: 2534-2545. doi: 10.1007/s10803-012-1510-3
[19]	Bayliss AP, Pellegrino G Di, Tipper SP (2005) Sex differences in eye gaze and symbolic cueing of attention. Q J Exp Psychol Sect A Hum Exp Psychol 58: 631-650. doi: 10.1080/02724980443000124
[20]	Lassalle A, Itier RJ (2015) Autistic traits influence gaze-oriented attention to happy but not fearful faces. Soc Neurosci 10: 70-88. doi: 10.1080/17470919.2014.958616
[21]	Lin G, Cui Y, Zeng J, et al. (2020) The Effect of Autistic Traits on Social Orienting in Typically Developing Individuals. Front Psychol 11: 794. doi: 10.3389/fpsyg.2020.00794
[22]	Kamachi M, Bruce V, Mukaida S, et al. (2001) Dynamic properties influence the perception of facial expressions. Perception 30: 875-887. doi: 10.1068/p3131
[23]	Wakabayashi A, Tojo Y, Baron-Cohen S, et al. (2004) The autism-spectrum quotient (AQ) Japanese version: evidence from high-functioning clinical group and normal adults. Shinrigaku Kenkyu 75: 78-84. doi: 10.4992/jjpsy.75.78
[24]	Friesen CK, Kingstone A (1998) The eyes have it! Reflexive orienting is triggered by nonpredictive gaze. Psychon Bull Rev 5: 490-495. doi: 10.3758/BF03208827
[25]	Driver J, Davis G, Ricciardelli P, et al. (1999) Gaze perception triggers reflexive visuospatial orienting. Vis Cogn 6: 509-540. doi: 10.1080/135062899394920
[26]	Pruett JR, Lamacchia A, Hoertel S, et al. (2011) Social and non-social cueing of visuospatial attention in autism and typical development. J Autism Dev Disord 41: 715-731. doi: 10.1007/s10803-010-1090-z
[27]	Landry O, Parker A (2013) A meta-analysis of visual orienting in autism. Front Hum Neurosci 7: 1-12. doi: 10.3389/fnhum.2013.00833
[28]	Frischen A, Bayliss AP, Tipper SP (2007) Gaze cueing of attention: visual attention, socoial cognition and individual differences. Psychol Bull 133: 694-724. doi: 10.1037/0033-2909.133.4.694
[29]	Dalmaso M, Alessi G, Castelli L, et al. (2020) Eye contact boosts the reflexive component of overt gaze following. Sci Rep 10: 1-10. doi: 10.1038/s41598-020-61619-6
[30]	Elsabbagh M, Gliga T, Pickles A, et al. (2013) The development of face orienting mechanisms in infants at-risk for autism. Behav Brain Res 251: 147-154. doi: 10.1016/j.bbr.2012.07.030
[31]	Kaldy Z, Giserman I, Carter AS, et al. (2016) The Mechanisms Underlying the ASD Advantage in Visual Search. J Autism Dev Disord 46: 1513-1527. doi: 10.1007/s10803-013-1957-x

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