Abstract
Purpose
The dorsal stream vulnerability hypothesis posits that the dorsal stream, responsible for visual motion and visuo-motor processing, may be particularly vulnerable during neurodevelopment. Consistent with this, autism spectrum disorder (ASD) has been associated with deficits in global motion integration, though deficits in ventral stream tasks, such as form identification, have also been reported. In the current study, we examined whether a similar pattern of results is found in a cohort of 381 children born with neurodevelopmental risk factors and exhibiting a wide spectrum of caregiver-reported autistic traits. Methods: We examined the associations between global motion perception, global form perception, fine motor function, visual-motor integration, and autistic traits (autism spectrum quotient, AQ) using linear regression, accounting for possible interactions with sex and other factors relevant to neurodevelopment. Results: All assessments of dorsal stream function were significantly associated with AQ such that worse performance predicted higher AQ scores. We also observed a significant sex interaction, with worse global form perception associated with higher AQ in boys (n = 202) but not girls (n = 179). Conclusion: We found widespread associations between dorsal stream functions and autistic traits. These associations were observed in a large group of children with a range of AQ scores, demonstrating a range of visual function across the full spectrum of autistic traits. In addition, ventral function was associated with AQ in boys but not girls. Sex differences in the associations between visual processing and neurodevelopment should be considered in the designs of future studies.
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References
Alnawmasi, M. M., Chakraborty, A., Dalton, K., Quaid, P., Dunkley, B. T., & Thompson, B. (2019). The effect of mild traumatic brain injury on the visual processing of global form and motion. Brain Injury, 33(10), 1354–1363. https://doi.org/10.1080/02699052.2019.1641842.
Armstrong, K., & Iarocci, G. (2013). The Autism Spectrum Quotient has convergent validity with the Social Responsiveness Scale in a high-functioning sample. Journal of Autism and Developmental Disorders, 43(9), 2228–2232. https://doi.org/10.1007/s10803-013-1769-z.
Atkinson, J. (2017). The davida teller award lecture, 2016 visual brain development: A review of ‘dorsal stream vulnerability’-motion, mathematics, amblyopia, actions, and attention. Journal of Vision, 17(3), 1–24. https://doi.org/10.1167/17.3.26.
Atkinson, J., & Braddick, O. (2005). Dorsal stream vulnerability and autistic disorders: The importance of comparative studies of form and motion coherence in typically developing children and children with developmental disorders. In Cahiers de Psychologie Cognitive (Vol. 23, Issues 1–2).
Atkinson, J., Salmond, C., & Crampton, P. (2014). NZDep2013 Index of Deprivation. In NZDep2013 Index of Deprivation. https://www.otago.ac.nz/wellington/otago069936.pdf
Auyeung, B., Baron-Cohen, S., Wheelwright, S., & Allison, C. (2008). The Autism Spectrum Quotient: Children’s version (AQ-Child). Journal of Autism and Developmental Disorders, 38(7), 1230–1240. https://doi.org/10.1007/s10803-007-0504-z.
Baron-Cohen, S., Wheelwright, S., Skinner, R., Martin, J., & 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(1).
Baron-Cohen, S., Hoekstra, R. A., Knickmeyer, R., & Wheelwright, S. (2006). The autism-spectrum quotient (AQ)—Adolescent version. Journal of Autism and Developmental Disorders, 36(3), 343–350. https://doi.org/10.1007/s10803-006-0073-6.
Beery, K., & Beery, N. (2010). The beery-buktenica developmental test of visual-motor integration (6th ed.). Pearson Education.
Bishop, D. V. M., Maybery, M., Maley, A., Wong, D., Hill, W., & Hallmayer, J. (2004). Using self-report to identify the broad phenotype in parents of children with autistic spectrum disorders: A study using the autism-spectrum quotient. Journal of Child Psychology and Psychiatry, 45(8), 1431–1436. https://doi.org/10.1111/J.1469-7610.2004.00325.X.
Braddick, O., Atkinson, J., & Wattam-Bell, J. (2003). Normal and anomalous development of visual motion processing: Motion coherence and ‘dorsal-stream vulnerability’. Neuropsychologia, 41(13), 1769–1784. https://doi.org/10.1016/S0028-3932(03)00178-7.
Chakraborty, A., Anstice, N. S., Jacobs, R. J., Paudel, N., LaGasse, L. L., Lester, B. M., McKinlay, C. J. D., Harding, J. E., Wouldes, T. A., & Thompson, B. (2017). Global motion perception is related to motor function in 4.5-year-old children born at risk of abnormal development. Vision Research, 135, 16–25. https://doi.org/10.1016/j.visres.2017.04.005.
Chen, N., Cai, P., Zhou, T., Thompson, B., & Fang, F. (2016). Perceptual learning modifies the functional specializations of visual cortical areas. Proceedings of the National Academy of Sciences, 113(20), 5724–5729. https://doi.org/10.1073/pnas.1524160113
Church, B. A., Rice, C. L., Dovgopoly, A., Lopata, C. J., Thomeer, M. L., Nelson, A., & Mercado, E. (2015). Learning, plasticity, and atypical generalization in children with autism. Psychonomic Bulletin and Review, 22(5), 1342–1348. https://doi.org/10.3758/S13423-014-0797-9/TABLES/2.
Dean, M., Harwood, R., & Kasari, C. (2017). The art of camouflage: Gender differences in the social behaviors of girls and boys with autism spectrum disorder. Autism, 21(6), 678–689. https://doi.org/10.1177/1362361316671845.
DiCriscio, A. S., Smith, J., & Troiani, V. (2021). Comprehensive Assessment of Visual Perceptual Skills in Autism Spectrum Disorder. Frontiers in Psychology, 12, 2591. https://doi.org/10.3389/FPSYG.2021.662808/BIBTEX.
Federici, A., Parma, V., Vicovaro, M., Radassao, L., Casartelli, L., & Ronconi, L. (2020). Anomalous perception of Biological Motion in Autism: A conceptual review and Meta-analysis. Scientific Reports, 10(1), 4576. https://doi.org/10.1038/s41598-020-61252-3.
Gallant, J. L., Shoup, R. E., & Mazer, J. A. (2000). A human Extrastriate Area functionally homologous to Macaque V4. Neuron, 27(2), 227–235. https://doi.org/10.1016/S0896-6273(00)00032-5.
Glass, L. (1969). Moiré Effect from Random Dots. Nature, 223(5206), 578–580. https://doi.org/10.1038/223578a0.
Glass, L., & Pérez, R. (1973). Perception of random dot interference patterns. Nature, 246(5432), 360–362. https://doi.org/10.1038/246360a0.
Goodale, M. A. (2011). Transforming vision into action. Vision Research, 51(13), 1567–1587. https://doi.org/10.1016/J.VISRES.2010.07.027.
Goodale, M. A., & Milner, A. D. (1992). Separate visual pathways for perception and action. Trends in Neurosciences, 15(1), 20–25. https://doi.org/10.1016/0166-2236(92)90344-8.
Green, R. R., Bigler, E. D., Froehlich, A., Prigge, M. B. D., Travers, B. G., Cariello, A. N., Anderson, J. S., Zielinski, B. A., Alexander, A., Lange, N., & Lainhart, J. E. (2016). Beery VMI performance in autism spectrum disorder. Child Neuropsychology, 22(7), 795–817. https://doi.org/10.1080/09297049.2015.1056131.
Greimel, E., Bartling, J., Dunkel, J., Brückl, M., Deimel, W., Remschmidt, H., Kamp-Becker, I., & Schulte-Körne, G. (2013). The temporal dynamics of coherent motion processing in autism spectrum disorder: Evidence for a deficit in the dorsal pathway. Behavioural Brain Research, 251, 168–175. https://doi.org/10.1016/j.bbr.2013.05.055.
Griffin, J. W., Bauer, R., & Scherf, K. S. (2021). A quantitative Meta-analysis of Face Recognition Deficits in Autism: 40 years of Research. 147(3), 268–292. https://doi.org/10.1037/bul0000310
Grinter, E. J., Maybery, M. T., & Badcock, D. R. (2010a). Vision in developmental disorders: Is there a dorsal stream deficit? Brain Research Bulletin, 82(3–4), 147–160. https://doi.org/10.1016/J.BRAINRESBULL.2010a.02.016.
Grinter, E. J., Maybery, M. T., Pellicano, E., Badcock, J. C., & Badcock, D. R. (2010b). Perception of shapes targeting local and global processes in autism spectrum disorders. Journal of Child Psychology and Psychiatry, 51(6), 717–724. https://doi.org/10.1111/J.1469-7610.2009.02203.X.
Harris, H., Israeli, D., Minshew, N., Bonneh, Y., Heeger, D. J., Behrmann, M., & Sagi, D. (2015). Perceptual learning in autism: Over-specificity and possible remedies. Nature Neuroscience (Vol, 18(11), 1574–1576. https://doi.org/10.1038/nn.4129. Nature Publishing Group.
Hattie, J. A. C., & Brown, G. T. L. (2007). Technology for School-Based Assessment and Assessment for Learning: Development Principles from New Zealand. Journal of Educational Technology Systems, 36(2), 189–201. https://doi.org/10.2190/ET.36.2.g.
Hay, I., Dutton, G. N., Biggar, S., Ibrahim, H., & Assheton, D. (2020). Exploratory study of dorsal visual stream dysfunction in autism; A case series. Research in Autism Spectrum Disorders, 69(October 2019), 101456. https://doi.org/10.1016/j.rasd.2019.101456
Henderson, S. E., Sugden, D. A., & Barnett, A. L. (2007). Movement assessment battery for children-2 second edition. Harcourt Assessment.
Hoel, P. G., Port, S. C., & Stone, C. J. (1971). Introduction to statistical theory. Houghton-Mifflin.
Jeffery, L., Crookes, K., Bothe, E., Thorburn, M., Kaiko, N., Giffard, C., & Palermo, R. (2018). Higher levels of autistic traits are linked to poorer face recognition performance but not reduced adaptive coding in 6–8 year-old children. Journal of Vision, 18(10), 921. https://doi.org/10.1167/18.10.921.
Joseph, R. M., Keehn, B., Connolly, C., Wolfe, J. M., & Horowitz, T. S. (2009). Why is visual search superior in autism spectrum disorder? Developmental Science, 12(6), 1083–1096. https://doi.org/10.1111/j.1467-7687.2009.00855.x.
Lange, J., & Lappe, M. (2006). A model of Biological Motion Perception from Configural Form Cues. Journal of Neuroscience, 26(11), 2894–2906. https://doi.org/10.1523/JNEUROSCI.4915-05.2006.
Levitt, H. (1971). Transformed Up-Down methods in Psychoacoustics. The Journal of the Acoustical Society of America, 49(2B), 467. https://doi.org/10.1121/1.1912375.
Lewis, T. L., Ellemberg, D., Maurer, D., Dirks, M., Wilkinson, F., & Wilson, H. R. (2004). A window on the normal development of sensitivity to global form in glass patterns. Perception, 33(4), 409–418. https://doi.org/10.1068/p5189.
Lockwood Estrin, G., Milner, V., Spain, D., Happé, F., & Colvert, E. (2021). Barriers to Autism Spectrum Disorder diagnosis for Young Women and Girls: A systematic review. Review Journal of Autism and Developmental Disorders, 8(4), 454–470. https://doi.org/10.1007/S40489-020-00225-8/FIGURES/2.
Manjaly, Z. M., Bruning, N., Neufang, S., Stephan, K. E., Brieber, S., Marshall, J. C., Kamp-Becker, I., Remschmidt, H., Herpertz-Dahlmann, B., Konrad, K., & Fink, G. R. (2007). Neurophysiological correlates of relatively enhanced local visual search in autistic adolescents. Neuroimage, 35(1), 283–291. https://doi.org/10.1016/j.neuroimage.2006.11.036.
Maunsell, J. H. R., & Van Essen, D. C. (1983). Functional Properties of neurons in middle temporal visual area of the Macaque Monkey. I. selectivity for stimulus direction, speed, and Orientation. Journal of Neurophysiology, 49(5).
McKinlay, C. J. D., Alsweiler, J. M., Ansell, J. M., Anstice, N. S., Chase, J. G., Gamble, G. D., Harris, D. L., Jacobs, R. J., Jiang, Y., Paudel, N., Signal, M., Thompson, B., Wouldes, T. A., Yu, T. Y., & Harding, J. E. (2015). Neonatal glycemia and neurodevelopmental outcomes at 2 years. New England Journal of Medicine, 373(16), 1507–1518. https://doi.org/10.1056/nejmoa1504909.
McKinlay, C. J. D., Alsweiler, J. M., Anstice, N. S., Burakevych, N., Chakraborty, A., Chase, J. G., Gamble, G. D., Harris, D. L., Jacobs, R. J., Jiang, Y., Paudel, N., Diego, S., Thompson, R. J., Wouldes, B., T. A., & Harding, J. E. (2017). Association of neonatal glycemia with neurodevelopmental outcomes at 4.5 years. JAMA Pediatrics, 171(10), 972. https://doi.org/10.1001/jamapediatrics.2017.1579.
Mercado, E., Chow, K., Church, B. A., & Lopata, C. (2020). Perceptual category learning in autism spectrum disorder: Truth and consequences. Neuroscience & Biobehavioral Reviews, 118, 689–703. https://doi.org/10.1016/j.neubiorev.2020.08.016.
Murray, A. L., Booth, T., McKenzie, K., & Kuenssberg, R. (2016). What range of trait levels can the autism-spectrum quotient (AQ) measure reliably? An item response theory analysis. Psychological Assessment, 28(6), 673–683. https://doi.org/10.1037/PAS0000215.
Nackaerts, E., Wagemans, J., Helsen, W., Swinnen, S. P., Wenderoth, N., & Alaerts, K. (2012). Recognizing Biological Motion and Emotions from Point-Light Displays in Autism Spectrum Disorders. Plos One, 7(9), e44473. https://doi.org/10.1371/journal.pone.0044473.
Nakamura, H., Kashii, S., Nagamine, T., Matsui, Y., Hashimoto, T., Honda, Y., & Shibasaki, H. (2003). Human V5 demonstrated by magnetoencephalography using random dot kinematograms of different coherence levels. Neuroscience Research, 46(4), 423–433. https://doi.org/10.1016/S0168-0102(03)00119-6.
Ohl, A., & Schelly, D. (2021). No evidence of a minimal clinically important difference for the Beery-Buktenica Developmental Test of Visual-Motor Integration in children with autism spectrum disorder. British Journal of Occupational Therapy, 0(0), 030802262110578. https://doi.org/10.1177/03080226211057834.
Osório, J. M. A., Rodríguez-Herreros, B., Richetin, S., Junod, V., Romascano, D., Pittet, V., Chabane, N., Gygax, J., M., & Maillard, A. M. (2021). Sex differences in sensory processing in children with autism spectrum disorder. Autism Research, 14(11), 2412–2423. https://doi.org/10.1002/AUR.2580.
Paudel, N., Thompson, B., Chakraborty, A., Harding, J., Jacobs, R. J., Wouldes, T. A., Yu, S. T. Y., & Anstice, N. S. (2022). Relationship between visual and neurodevelopmental measures at 2 years with visual acuity and stereopsis at 4.5 years in children born at risk of neonatal hypoglycaemia. Ophthalmic and Physiological Optics, 42(1), 195–204. https://doi.org/10.1111/opo.12910.
Robertson, C. E., Thomas, C., Kravitz, D. J., Wallace, G. L., Baron-Cohen, S., Martin, A., & Baker, C. I. (2014). Global motion perception deficits in autism are reflected as early as primary visual cortex. Brain, 137(9), 2588–2599. https://doi.org/10.1093/brain/awu189.
Rudolph, K., & Pasternak, T. (1999). Transient and permanent deficits in motion perception after lesions of cortical areas MT and MST in the macaque monkey. Cerebral Cortex, 9(1), 90–100. https://doi.org/10.1093/cercor/9.1.90.
Ruzich, E., Allison, C., Smith, P., Ring, H., Auyeung, B., & Baron-Cohen, S. (2017). The autism-spectrum quotient in siblings of people with autism. Autism Research, 10(2), 289–297. https://doi.org/10.1002/AUR.1651.
Sacrey, L. A. R., Zwaigenbaum, L., Bryson, S., Brian, J., & Smith, I. M. (2018). The reach-to-grasp movement in infants later diagnosed with autism spectrum disorder: A high-risk sibling cohort study. Journal of Neurodevelopmental Disorders, 10(1), 1–11. https://doi.org/10.1186/S11689-018-9259-4/TABLES/5.
Sapey-Triomphe, L. A., Timmermans, L., & Wagemans, J. (2021). Priors Bias Perceptual decisions in Autism, but are less flexibly adjusted to the Context. Autism Research, 14(6), 1134–1146. https://doi.org/10.1002/AUR.2452.
Sasson, N. J., & Bottema-Beutel, K. (2022). Studies of autistic traits in the general population are not studies of autism. Autism, 26(4), 1007–1008. https://doi.org/10.1177/13623613211058515.
Scase, M. O., Braddick, O. J., & Raymond, J. E. (1996). What is noise for the motion. System? Vision Research, 36(16), 2579–2586. https://doi.org/10.1016/0042-6989(95)00325-8.
Seabold, S., & Perktold, J. (2010). Statsmodels: Econometric and Statistical Modeling with Python. Proceedings of the 9th Python in Science Conference.
Shah, R., Dai, D. W. T., Alsweiler, J. M., Brown, G. T. L., Chase, J. G., Gamble, G. D., Harris, D. L., Keegan, P., Nivins, S., Wouldes, T. A., Thompson, B., Turuwhenua, J., Harding, J. E., McKinlay, C. J. D., Team, C. W. H., Feldman, T. L., Hay, H., Hess, W., Wilson, R., & Wilson, D. (2022). J. Association of Neonatal Hypoglycemia With Academic Performance in Mid-Childhood. JAMA, 327(12), 1158–1170. https://doi.org/10.1001/JAMA.2022.0992
Silva, A. E., & Liu, Z. (2018). Spatial proximity modulates the strength of motion opponent suppression elicited by locally paired dot displays. Vision Research, 144, 1–8. https://doi.org/10.1016/j.visres.2018.01.004.
Silva, A. E., Thompson, B., & Liu, Z. (2021). Motion opponency examined throughout visual cortex with multivariate pattern analysis of fMRI data. Human Brain Mapping, 42(1), 5–13. https://doi.org/10.1002/HBM.25198.
Spencer, J., OʼBrien, J., Riggs, K., Braddick, O., Atkinson, J., & Wattam-Bell, J. (2000). Motion processing in autism. Neuroreport, 11(12), 2765–2767. https://doi.org/10.1097/00001756-200008210-00031.
Thompson, B., McKinlay, C. J. D., Chakraborty, A., Anstice, N. S., Jacobs, R. J., Paudel, N., Yu, T. Y., Ansell, J. M., Wouldes, T. A., & Harding, J. E. (2017). Global motion perception is associated with motor function in 2-year-old children. Neuroscience Letters, 658, 177–181. https://doi.org/10.1016/j.neulet.2017.08.062.
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), 49. https://doi.org/10.1186/s13229-019-0299-8.
Van Der Hallen, R., Evers, K., Brewaeys, K., Van Den Noortgate, W., & Wagemans, J. (2015). Global processing takes time: A meta-analysis on local-global visual processing in ASD. Psychological Bulletin, 141(3), 549–573. https://doi.org/10.1037/bul0000004.
Van der Hallen, R., Manning, C., Evers, K., & Wagemans, J. (2019). Global motion perception in Autism Spectrum disorder: A Meta-analysis. Journal of Autism and Developmental Disorders, 49(12), 4901–4918. https://doi.org/10.1007/s10803-019-04194-8.
Watamaniuk, S. N. J., Sekuler, R., & Williams, D. W. (1989). Direction perception in complex dynamic displays: The integration of direction information. Vision Research, 29(1), 47–59. https://doi.org/10.1016/0042-6989(89)90173-9.
Williams, D. W., & Sekuler, R. (1984). Coherent global motion percepts from stochastic local motions. Vision Research, 24(1), 55–62. https://doi.org/10.1016/0042-6989(84)90144-5.
Wilson, H. R., Wilkinson, F., & Asaad, W. (1997). Concentric orientation summation in human form vision. Vision Research, 37(17), 2325–2330. https://doi.org/10.1016/S0042-6989(97)00104-1.
Zhang, M., Jiao, J., Hu, X., Yang, P., Huang, Y., Situ, M., Guo, K., Cai, J., & Huang, Y. (2020). Exploring the spatial working memory and visual perception in children with autism spectrum disorder and general population with high autism-like traits. PLOS ONE, 15(7), e0235552. https://doi.org/10.1371/journal.pone.0235552.
Zhao, J., Gao, Z., Lai, J., & Joshi, R. M. (2021). The relationship between autism traits and listening comprehension among chinese preschool children with autism spectrum disorder. Reading and Writing, 1–19. https://doi.org/10.1007/S11145-021-10216-8/TABLES/2.
Acknowledgements
This work was funded by the Health Research Council of New Zealand (17/240) and the Maurice and Phyllis Paykel Trust. AES is supported by a Transformative Quantum Technologies postdoctoral fellowship. BT is supported by the Hong Kong Special Administrative Region Government and InnoHK. We are grateful to the children and families who participated in this study. We would like to thank the CHYLD steering group for their input. [Members of the CHYLD Study Team: Steering group: Jane Harding, DPhil, Christopher McKinlay, PhD, Jane Alsweiler, PhD, Deborah Harris, PhD, Gavin Brown, PhD, J. Geoffrey Chase, PhD, Gregory Gamble, MSc, Trecia Wouldes, PhD, Peter Keegan, PhD, and Benjamin Thompson, DPhil; International advisory committee: Heidi Feldman, PhD, William Hay, MD, Robert Hess, PhD, and Darrell Wilson, MD; Other members of the CHYLD Mid-childhood Outcome Study team: Jason Turuwhenua, PhD, Jenny Rogers, MHSc, Steven Miller, MD, Eleanor Kennedy, PhD, Arijit Chakraborty, PhD, Jennifer Knopp, PhD, Rajesh Shah, PhD, Darren Dai, MSSc, Samson Nivins, MSc, Tony Zhou, PhD, Jocelyn Ledger, Stephanie Macdonald, BSc, Alecia McNeill BSc, Coila Bevan, BA, Nataliia Burakevych, PhD, Robin May, MPhil, Safayet Hossin, MSc, Grace McKnight, Rashedul Hasan, MSc, Jessica Wilson, MSc.]
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Silva, A.E., Harding, J.E., Chakraborty, A. et al. Associations Between Autism Spectrum Quotient and Integration of Visual Stimuli in 9-year-old Children: Preliminary Evidence of Sex Differences. J Autism Dev Disord (2023). https://doi.org/10.1007/s10803-023-06035-1
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DOI: https://doi.org/10.1007/s10803-023-06035-1