Basic oculomotor function is similar in young children with ASD and typically developing controls.

eye position eye tracking gaze kinematic characteristics movies oculomotor control saccade

Journal

Autism research : official journal of the International Society for Autism Research
ISSN: 1939-3806
Titre abrégé: Autism Res
Pays: United States
ID NLM: 101461858

Informations de publication

Date de publication:
12 2021
Historique:
revised: 29 06 2021
received: 21 10 2020
accepted: 28 07 2021
pubmed: 19 8 2021
medline: 15 12 2021
entrez: 18 8 2021
Statut: ppublish

Résumé

A variety of eye tracking studies have demonstrated that young children with ASD gaze at images and movies of social interactions differently than typically developing children. These findings have supported the hypothesis that gaze behavior differences are generated by a weaker preference for social stimuli in ASD children. The hypothesis assumes that gaze differences are not caused by abnormalities in oculomotor function including saccade frequency and kinematics. Previous studies of oculomotor function have mostly been performed with school-age children, adolescents, and adults using visual search, anti-saccade, and gap saccade tasks that are less suitable for young pre-school children. Here, we examined oculomotor function in 144 children (90 with ASD and 54 controls), 1-10-years-old, as they watched two animated movies interleaved with the presentation of multiple salient stimuli that elicited saccades-to-targets. The results revealed that the number of fixations, fixation duration, number of saccades, saccade duration, saccade accuracy, and saccade latency did not differ significantly across groups. Minor initial differences in saccade peak velocity were not supported by analysis with a linear mixed model. These findings suggest that most children with ASD exhibit similar oculomotor function to that of controls, when performing saccades-to-targets or freely viewing child-friendly movies. This suggests that previously reported gaze abnormalities in children with ASD are not due to underlying oculomotor deficiencies. LAY SUMMARY: This study demonstrates that children with ASD perform similar eye movements to those of controls when freely observing movies or making eye movements to targets. Similar results were apparent across groups in the number of eye movements, their accuracy, duration, and other measures that assess eye movement control. These findings are important for interpreting previously reported differences in gaze behavior of children with ASD, which are likely due to atypical social preferences rather than impaired control of eye movements.

Identifiants

pubmed: 34405961
doi: 10.1002/aur.2592
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2580-2591

Subventions

Organisme : Israel Science Foundation
ID : 1150/20
Organisme : Israel Science Foundation
ID : 961/14

Informations de copyright

© 2021 International Society for Autism Research and Wiley Periodicals LLC.

Références

Albers, C. A., & Grieve, A. J. (2007). Bayley scales of infant and toddler development-Third edition. San Antonio, TX: Harcourt assessment. Journal of Psychoeducational Assessment, 25(2), 180-190. https://doi.org/10.1177/0734282906297199
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (DSM-5®). American Psychiatric Pub. https://doi.org/10.1176/appi.books.9780890425596.744053
Anton-Erxleben, K., & Carrasco, M. (2013). Attentional enhancement of spatial resolution: Linking behavioural and neurophysiological evidence. Nature Reviews Neuroscience, 14(3), 188-200. https://doi.org/10.1038/nrn3443
Avni, I., Meiri, G., Bar-Sinai, A., Reboh, D., Manelis, L., Flusser, H., Michaelovski, A., Menashe, I., & Dinstein, I. (2019). Children with autism observe social interactions in an idiosyncratic manner. Autism Research, 13(6), 935-946. https://doi.org/10.1002/aur.2234
Bahill, A., Brockenbrough, A., & Troost, B. (1981). Variability and development of a normative data base for saccadic eye movements. Investigative Ophthalmology & Visual Science, 21(1), 116-125.
Bast, N., Mason, L., Freitag, C. M., Smith, T., Portugal, A. M., Poustka, L., Banaschewski, T., Johnson, M., & EU-AIMS LEAP Group. (2021). Saccade dysmetria indicates attenuated visual exploration in autism spectrum disorder. Journal of Child Psychology and Psychiatry, 62(2), 149-159. https://doi.org/10.1111/jcpp.13267
Batki, A., Baron-Cohen, S., Wheelwright, S., Connellan, J., & Ahluwalia, J. (2000). Is there an innate gaze module? Evidence from human neonates. Infant Behavior and Development, 23(2), 223-229. https://doi.org/10.1016/S0163-6383(01)00037-6
Boghen, D., Troost, B. T., Daroff, R. B., Dell'Osso, L. F., & Birkett, J. E. (1974). Velocity characteristics of normal human saccades. Investigative Ophthalmology, 13(8), 619-623.
Canice McGivern, R., & Mark Gibson, J. (2006). Characterisation of ocular fixation in humans by analysis of saccadic intrusions and fixation periods: A pragmatic approach. Vision Research, 46(21), 3741-3747. https://doi.org/10.1016/j.visres.2006.05.016
Chawarska, K., MacAri, S., & Shic, F. (2012). Context modulates attention to social scenes in toddlers with autism. Journal of Child Psychology and Psychiatry and Allied Disciplines, 53(8), 903-913. https://doi.org/10.1111/j.1469-7610.2012.02538.x
Chita-Tegmark, M. (2016). Attention allocation in ASD: A review and meta-analysis of eye-tracking studies. Review Journal of Autism and Developmental Disorders, 3(3), 209-223. https://doi.org/10.1007/s40489-016-0077-x
Constantino, J. N., & Gruber, C. P. (2012). Social responsiveness scale: SRS-2. Western Psychological Services.
Dinstein, I., Arazi, A., Golan, H. M., Koller, J., Elliott, E., Gozes, I., Shulman, C., Shifman, S., Raz, R., Davidovitch, N., Gev, T., Aran, A., Stolar, O., Ben-Itzchak, E., Snir, I. M., Israel-Yaacov, S., Bauminger-Zviely, N., Bonneh, Y. S., Gal, E., … Meiri, G. (2020). The national autism database of Israel: A resource for studying autism risk factors, biomarkers, outcome measures, and treatment efficacy. Journal of Molecular Neuroscience, 70(9), 1303-1312. https://doi.org/10.1007/s12031-020-01671-z
Farroni, T., Csibra, G., Simion, F., & Johnson, M. H. (2002). Eye contact detection in humans from birth. Proceedings of the National Academy of Sciences of the United States of America, 99(14), 9602-9605. https://doi.org/10.1073/pnas.152159999
Faul, F., Erdfelder, E., Lang, A. G., & Buchner, A. (2007). G*power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39(2), 175-191. https://doi.org/10.3758/BF03193146
Frank, M. C., Vul, E., & Johnson, S. P. (2009). Development of infants' attention to faces during the first year. Cognition, 110(2), 160-170. https://doi.org/10.1016/j.cognition.2008.11.010
Frazier, T. W., Strauss, M., Klingemier, E. W., Zetzer, E. E., Hardan, A. Y., Eng, C., & Youngstrom, E. A. (2017). A meta-analysis of gaze differences to social and nonsocial information between individuals with and without autism. Journal of the American Academy of Child and Adolescent Psychiatry, 56(7), 546-555. https://doi.org/10.1016/j.jaac.2017.05.005
Fukushima, J., Hatta, T., & Fukushima, K. (2000). Development of voluntary control of saccadic eye movements: I. Age-related changes in normal children. Brain and Development, 22(3), 173-180. https://doi.org/10.1016/S0387-7604(00)00101-7
Goldberg, M. C., Lasker, A. G., Zee, D. S., Garth, E., Tien, A., & Landa, R. J. (2002). Deficits in the initiation of eye movements in the absence of a visual target in adolescents with high functioning autism. Neuropsychologia, 40(12), 2039-2049. https://doi.org/10.1016/S0028-3932(02)00059-3
Haith, M. M., Bergman, T., & Moore, M. J. (1977). Eye contact and face scanning in early infancy. Science, 198(4319), 853-855. https://doi.org/10.1126/science.918670
Harris, C. M., Hainline, L., Abramov, I., Lemerise, E., & Camenzuli, C. (1988). The distribution of fixation durations in infants and naive adults. Vision Research, 28(3), 419-432. https://doi.org/10.1016/0042-6989(88)90184-8
Henderson, C. R. (1973). Sire evaluation and genetic trends. Journal of Animal Science, 1973, 10-41. https://doi.org/10.1093/ansci/1973.Symposium.10
Johnson, B., Rinehart, N., Papadopoulos, N., Tonge, B., Millist, L., White, O., & Fielding, J. (2012). A closer look at visually guided saccades in autism and asperger's disorder. Frontiers in Integrative Neuroscience, 6, 1-17. https://doi.org/10.3389/fnint.2012.00099
Johnson, B. P., Lum, J. A. G., Rinehart, N. J., & Fielding, J. (2016). Ocular motor disturbances in autism spectrum disorders: Systematic review and comprehensive meta-analysis. Neuroscience and Biobehavioral Reviews, 69, 260-279. https://doi.org/10.1016/j.neubiorev.2016.08.007
Johnson, M. H., Dziurawiec, S., Ellis, H., & Morton, J. (1991). Newborns' preferential tracking of face-like stimuli and its subsequent decline. Cognition, 40(1-2), 1-19. https://doi.org/10.1016/0010-0277(91)90045-6
Jones, W., Carr, K., & Klin, A. (2008). Absence of preferential looking to the eyes of approaching adults predicts level of social disability in 2-year-old toddlers with autism spectrum disorder. Archives of General Psychiatry, 65(8), 946-954. https://doi.org/10.1001/archpsyc.65.8.946
Jones, W., & Klin, A. (2013). Attention to eyes is present but in decline in 2-6-month-old infants later diagnosed with autism. Nature, 504(7480), 427-431. https://doi.org/10.1038/nature12715
Kliemann, D., Dziobek, I., Hatri, A., Steimke, R., & Heekeren, H. R. (2010). Atypical reflexive gaze patterns on emotional faces in autism spectrum disorders. Journal of Neuroscience, 30(37), 12281-12287. https://doi.org/10.1523/JNEUROSCI.0688-10.2010
Klin, A., Lin, D. J., Gorrindo, P., Ramsay, G., & Jones, W. (2009). Two-year-olds with autism orient to non-social contingencies rather than biological motion. Nature, 459(7244), 257-261. https://doi.org/10.1038/nature07868
Kovarski, K., Siwiaszczyk, M., Malvy, J., Batty, M., & Latinus, M. (2019). Faster eye movements in children with autism spectrum disorder. Autism Research, 12(2), 212-224. https://doi.org/10.1002/aur.2054
Lee, M. D., & Wagenmakers, E. J. (2014). Bayesian cognitive modeling: A practical course. Cambridge University Press.
Lord, C., Risi, S., Lambrecht, L., Cook, E. H. J., Leventhal, B. L., DiLavore, P. C., Pickles, A., & Rutter, M. (2000). The autism diagnostic schedule - Generic: A standard measures of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205-223. https://doi.org/10.1023/A:1005592401947
Lord, C., Rutter, M., Di Lavore, P., Risi, S., Gotham, K., & Bishop, S. (2012). Autism diagnostic observation schedule, second edition (ADOS-2) manual (part I): Modules 1-4. Western Psychological Services.
Luna, B., Doll, S. K., Hegedus, S. J., Minshew, N. J., & Sweeney, J. A. (2007). Maturation of executive function in autism. Biological Psychiatry, 61(4), 474-481. https://doi.org/10.1016/j.biopsych.2006.02.030
Meiri, G., Dinstein, I., Michaelowski, A., Flusser, H., Ilan, M., Faroy, M., Bar-Sinai, A., Manelis, L., Stolowicz, D., Yosef, L. L., Davidovitch, N., Golan, H., Arbelle, S., & Menashe, I. (2017). Brief report: The negev hospital-university-based (HUB) autism database. Journal of Autism and Developmental Disorders, 47(9), 2918-2926. https://doi.org/10.1007/s10803-017-3207-0
Minshew, N. J., Luna, B., & Sweeney, J. A. (1999). Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism. Neurology, 52(5), 917-922. https://doi.org/10.1212/wnl.52.5.917
Moody, E. J., Reyes, N., Ledbetter, C., Wiggins, L., DiGuiseppi, C., Alexander, A., Jackson, S., Lee, L. C., Levy, S. E., & Rosenberg, S. A. (2017). Screening for autism with the SRS and SCQ: Variations across demographic, developmental and behavioral factors in preschool children. Journal of Autism and Developmental Disorders, 47(11), 3550-3561. https://doi.org/10.1007/s10803-017-3255-5
Moore, A., Wozniak, M., Yousef, A., Barnes, C. C., Cha, D., Courchesne, E., & Pierce, K. (2018). The geometric preference subtype in ASD: Identifying a consistent, early-emerging phenomenon through eye tracking. Molecular Autism, 9(1), 19. https://doi.org/10.1186/s13229-018-0202-z
Moriuchi, J. M., Klin, A., & Jones, W. (2017). Mechanisms of diminished attention to eyes in autism. American Journal of Psychiatry, 174(1), 26-35. https://doi.org/10.1176/appi.ajp.2016.15091222
Müller, H. J., & Rabbitt, P. M. (1989). Reflexive and voluntary orienting of visual attention: Time course of activation and resistance to interruption. Journal of Experimental Psychology: Human Perception and Performance, 15(2), 315-330. https://doi.org/10.1037//0096-1523.15.2.315
Nakano, T., Tanaka, K., Endo, Y., Yamane, Y., Yamamoto, T., Nakano, Y., Ohta, H., Kato, N., & Kitazawa, S. (2010). Atypical gaze patterns in children and adults with autism spectrum disorders dissociated from developmental changes in gaze behaviour. Proceedings of the Royal Society B: Biological Sciences, 277(1696), 2935-2943. https://doi.org/10.1098/rspb.2010.0587
Osterling, J., & Dawson, G. (1994). Early recognition of children with autism: A study of first birthday home videotapes. Journal of Autism and Developmental Disorders, 24(3), 247-257. https://doi.org/10.1007/BF02172225
Papagiannopoulou, E. A., Chitty, K. M., Hermens, D. F., Hickie, I. B., & Lagopoulos, J. (2014). A systematic review and meta-analysis of eye-tracking studies in children with autism spectrum disorders. Social Neuroscience, 9(6), 610-632. https://doi.org/10.1080/17470919.2014.934966
Pierce, K., Marinero, S., Hazin, R., McKenna, B., Barnes, C. C., & Malige, A. (2016). Eye tracking reveals abnormal visual preference for geometric images as an early biomarker of an autism spectrum disorder subtype associated with increased symptom severity. Biological Psychiatry, 79(8), 657-666. https://doi.org/10.1016/j.biopsych.2015.03.032
Riby, D. M., & Hancock, P. J. B. (2009). Do faces capture the attention of individuals with Williams syndrome or autism? Evidence from tracking eye movements. Journal of Autism and Developmental Disorders, 39(3), 421-431. https://doi.org/10.1007/s10803-008-0641-z
Rice, K., Moriuchi, J. M., Jones, W., & Klin, A. (2012). Parsing heterogeneity in autism spectrum disorders: Visual scanning of dynamic social scenes in school-aged children. Journal of the American Academy of Child and Adolescent Psychiatry, 51(3), 238-248. https://doi.org/10.1016/j.jaac.2011.12.017
Robinson, D. A. (1964). The mechanics of human saccadic eye movement. The Journal of Physiology, 174(2), 245-264. https://doi.org/10.1113/jphysiol.1964.sp007485
Senju, A., & Johnson, M. H. (2009). Atypical eye contact in autism: Models, mechanisms and development. Neuroscience and Biobehavioral Reviews, 33(8), 1204-1214. https://doi.org/10.1016/j.neubiorev.2009.06.001
Shic, F., Bradshaw, J., Klin, A., Scassellati, B., & Chawarska, K. (2011). Limited activity monitoring in toddlers with autism spectrum disorder. Brain Research, 1380, 246-254. https://doi.org/10.1016/j.brainres.2010.11.074
Shultz, S., Klin, A., & Jones, W. (2018). Neonatal transitions in social behavior and their implications for autism. Trends in Cognitive Sciences, 22(5), 452-469. https://doi.org/10.1016/j.tics.2018.02.012
Simion, F., Regolin, L., & Bulf, H. (2008). A predisposition for biological motion in the newborn baby. Proceedings of the National Academy of Sciences of the United States of America, 105(2), 809-813. https://doi.org/10.1073/pnas.0707021105
Stefan, A. M., Gronau, Q. F., Schönbrodt, F. D., & Wagenmakers, E. J. (2019). A tutorial on Bayes factor design analysis using an informed prior. Behavior Research Methods, 51(3), 1042-1058. https://doi.org/10.3758/s13428-018-01189-8
Todorova, G. K., Hatton, R. E. M. B., & Pollick, F. E. (2019). Biological motion perception in autism spectrum disorder: A meta-analysis. Molecular Autism, 10(1), 1-28. https://doi.org/10.1186/s13229-019-0299-8
Van der Geest, J. N., Kemner, C., Camfferman, G., Verbaten, M. N., & Van Engeland, H. (2001). Eye movements, visual attention, and autism: A saccadic reaction time study using the gap and overlap paradigm. Biological Psychiatry, 50(8), 614-619. https://doi.org/10.1016/S0006-3223(01)01070-8
Van Loon, E. M., Hooge, I. T. C., & Van den Berg, A. V. (2002). The timing of sequences of saccades in visual search. Proceedings of the Royal Society B: Biological Sciences, 269(1500), 1571-1579. https://doi.org/10.1098/rspb.2002.2062
Van Opstal, A. J., & Van Gisbergen, J. A. M. (1989). Scatter in the metrics of saccades and properties of the collicular motor map. Vision Research, 29(9), 1183-1196. https://doi.org/10.1016/0042-6989(89)90064-3
Viviani, P., & McCollum, G. (1983). The relation between linear extent and velocity in drawing movements. Neuroscience, 10(1), 211-218. https://doi.org/10.1016/0306-4522(83)90094-5
Wang, S., Jiang, M., Duchesne, X. M., Laugeson, E. A., Kennedy, D. P., Adolphs, R., & Zhao, Q. (2015). Atypical visual saliency in autism spectrum disorder quantified through model-based eye tracking. Neuron, 88(3), 604-616. https://doi.org/10.1016/j.neuron.2015.09.042
Wechsler, D. (2002). Wechsler preschool and primary scale of intelligence (pp. 120-130). Wechsler Preschool and Primary Scale of Intelligence. https://doi.org/10.1007/978-1-4419-1698-3_866
Wilkes, B. J., Carson, T. B., Patel, K. P., Lewis, M. H., & White, K. D. (2015). Oculomotor performance in children with high-functioning autism spectrum disorders. Research in Developmental Disabilities, 38, 338-344. https://doi.org/10.1016/j.ridd.2014.12.022

Auteurs

Inbar Avni (I)

Cognitive and Brain Sciences Department, Ben Gurion University, Beer Sheva, Israel.
National Autism Research Center of Israel, Ben Gurion University, Beer Sheva, Israel.

Gal Meiri (G)

National Autism Research Center of Israel, Ben Gurion University, Beer Sheva, Israel.
Pre-school Psychiatry Unit, Soroka University Medical Center, Beer Sheba, Israel.

Analya Michaelovski (A)

National Autism Research Center of Israel, Ben Gurion University, Beer Sheva, Israel.
Zusman Child Development Center, Soroka University Medical Center, Beer Sheva, Israel.

Idan Menashe (I)

National Autism Research Center of Israel, Ben Gurion University, Beer Sheva, Israel.
Public Health Department, Ben-Gurion University, Beer Sheva, Israel.

Lior Shmuelof (L)

Cognitive and Brain Sciences Department, Ben Gurion University, Beer Sheva, Israel.

Ilan Dinstein (I)

Cognitive and Brain Sciences Department, Ben Gurion University, Beer Sheva, Israel.
National Autism Research Center of Israel, Ben Gurion University, Beer Sheva, Israel.
Psychology Department, Ben Gurion University, Beer Sheva, Israel.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH