Abstract
Although most researchers agree that individuals with Autism Spectrum Disorder (ASD) exhibit atypical attention, there is little consensus on the exact nature of their deficits. We explored whether attentional control in ASD varies as a function of motor proficiency. Nineteen children with ASD and 26 typically-developing controls completed the Movement Assessment Battery for Children and two ocular motor tasks requiring them to generate a saccade toward, and fixate, a visual target in the presence or absence of a distractor. The ASD group demonstrated poorer accuracy than typically-developing controls when distractors were present. Importantly, however, ASD symptomology was only related to poorer accuracy in individuals with motor difficulties. These findings suggest that distractor inhibition may be selectively impaired in this subgroup.
Similar content being viewed by others
References
Adams, N., & Jarrold, C. (2012). Inhibition in autism: Children with autism have difficulty inhibiting irrelevant distractors but not prepotent responses. Journal of Autism and Developmental Disorders, 42, 1052–1063.
Akshoomoff, N. A., & Courchesne, E. (1994). ERP evidence for a shifting attention deficit in patients with damage to the cerebellum. Journal of Cognitive Neuroscience, 6(4), 388–399.
Allen, G., & Courchesne, E. (2003). Differential effects of developmental cerebellar abnormality on cognitive and motor functions in the cerebellum: An fMRI study of autism. American Journal of Psychiatry, 160, 262–273.
Ames, C., & Fletcher-Watson, S. (2010). A review of methods in the study of attention in autism. Developmental Review, 30(1), 52–73.
Anzulewicz, A., Sobota, K., & Delafield-Butt, J. T. (2016). Toward the autism motor signature: Gesture patterns during smart tablet gameplay identify children with autism. Scientific Reports, 6, 1–13.
APA. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Washington, DC: American Psychiatric Publishing.
Blaser, E., Eglington, L., Carter, A. S., & Kaldy, Z. (2014). Pupillometry reveals a mechanism for the autism spectrum disorder (ASD) advantage in visual tasks. Scientific Reports, 4, 1–5.
Bottcher, L. (2010). Children with spastic cerebral palsy, their cognitive functioning, and social participation: A review. Child Neuropsychology, 16(3), 209–228.
Buckner, R. L. (2013). The cerebellum and cognitive function: 25 years of insight from anatomy and neuroimaging. Neuron, 80(3), 807–815.
Burack, J. A. (1994). Selective attention deficits in persons with autism: Preliminary evidence of an inefficient attentional lens. Journal of Abnormal Psychology, 103(3), 535–543.
Christ, S. E., Holt, D. D., White, D. A., & Green, L. (2007). Inhibitory control in children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 37(6), 1155–1165.
Christ, S. E., Kester, L. E., Bodner, K. E., & Miles, J. H. (2011). Evidence for selective inhibitory impairment in individuals with autism spectrum disorder. Neuropsychology, 25(6), 690–701.
Conners, K. C. (2008). Conners (3rd ed.). Toronto: Multi-Health Systems.
Constantino, J. N., & Gruber, C. P. (2012). Social responsiveness scale-second edition (SRS-2). Torrance: Western Psychological Services.
Courchesne, E., Townsend, J., Akshoomoff, N. A., Saitoh, O., Yeung-Courchesne, R., Lincoln, A. J., et al. (1994). Impairment in shifting attention in autistic and cerebellar patients. Behavioral Neuroscience, 108(5), 848–865.
Dichter, G. S., & Belger, A. (2007). Social stimuli interfere with cognitive control in autism. Neuroimage, 35(3), 1219–1230.
Donovan, A. P., & Basson, M. A. (2017). The neuroanatomy of autism: A developmental perspective. Journal of Anatomy, 230(1), 4–15.
Downey, R., & Rapport, M. J. (2012). Motor activity in children with autism: A review of current literature. Pediatric Physical Therapy, 24(1), 2–20.
Dunn, S. A., Freeth, M., & Milne, E. (2016). Electrophysiological evidence of atypical spatial attention in those with a high level of self-reported autistic traits. Journal of Autism and Developmental Disorders, 46(6), 2199–2210.
Enderle, J. D. (2010). Models of horizontal eye movements, part 1: Early models of saccades and smooth pursuit. Synthesis Lectures on Biomedical Engineering, 5(1), 1–163.
Enticott, P. G., Bradshaw, J. L., Iansek, R., Tonge, B. J., & Rinehart, N. (2009). Electrophysiological signs of supplementary-motor-area deficits in high-functioning autism but not Asperger’s syndrome: An examination of internally cued movement-related potentials. Developmental Medicine and Child Neurology, 51(10), 787–791.
Eriksen, B. A., & Eriksen, C. W. (1974). Effects of noise letters upon the identification of a target letter in a nonsearch task. Perception and Psychophysics, 16(1), 143–149.
Fielding, J., Corben, L., Cremer, P., Millist, L., White, O., & Delatycki, M. (2010). Disruption to higher order processes in Friedreich ataxia. Neuropsychologia, 48(1), 235–242.
Findlay, J. M., & Blythe, H. I. (2009). Saccade target selection: Do distractors affect saccade accuracy? Vision Research, 49, 1267–1274.
Findlay, J. M., & Brown, V. (2006). Eye scanning of multi-element displays: II. Saccade planning. Vision Research, 46(1–2), 216–227.
Fournier, K. A., Hass, C. J., Naik, S. K., Lodha, N., & Cauraugh, J. H. (2010). Motor coordination in autism spectrum disorders: A synthesis and meta-analysis. Journal of Autism and Developmental Disorders, 40, 1227–1240.
Geurts, H. M., Luman, M., & van Meel, C. S. (2008). What’s in a game: The effect of social motivation on interference control in boys with ADHD and autism spectrum disorders. Journal of Child Psychology and Psychiatry, 49(8), 848–857.
Geurts, H. M., van den Bergh, S. F., & Ruzzano, L. (2014). Prepotent response inhibition and interference control in autism spectrum disorders: Two meta-analyses. Autism Research, 7(4), 407–420.
Gowen, E., & Hamilton, A. (2013). Motor abilities in autism: A review using a computational context. Journal of Autism and Developmental Disorders, 43(2), 323–344.
Green, D., Charman, T., Pickles, A., Chandler, S., Loucas, T., Simonoff, E., et al. (2009). Impairment in movement skills of children with autistic spectrum disorders. Developmental Medicine and Child Neurology, 51(4), 311–316.
Hampson, D. R., & Blatt, G. J. (2015). Autism spectrum disorders and neuropathology of the cerebellum. Frontiers in Neuroscience, 9, 1–16.
Harris, N. S., Courchesne, E., Townsend, J., Carper, R. A., & Lord, C. (1999). Neuroanatomic contributions to slowed orienting of attention in children with autism. Cognitive Brain Research, 8, 61–71.
Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: The Guildford Press.
Henderson, H., Schwartz, C., Mundy, P., Burnette, C., Sutton, S., Zahka, N., et al. (2006). Response monitoring, the error-related negativity, and differences in social behavior in autism. Brain and Cognition, 61(1), 96–109.
Henderson, S. E., Sugden, D. A., & Barnett, A. L. (2007). Movement assessment battery for children-2: Movement ABC-2: Examiner’s manual. London: Pearson.
Hocking, D. R., Corben, L. A., Fielding, J., Cremer, P. D., Millist, L., White, O. B., et al. (2014). Saccade reprogramming in Friedreich ataxia reveals impairments in the cognitive control of saccadic eye movement. Brain and Cognition, 87, 161–167.
Hocking, D. R., Fielding, J., Corben, L. A., Cremer, P. D., Millist, L., White, O. B., et al. (2010). Ocular motor fixation deficits in Friedreich ataxia. Cerebellum, 9(3), 411–418.
Houghton, G., & Tipper, S. P. (1994). A model of inhibitory mechanisms in selective attention. In D. Dagenbach & T. Carr (Eds.), Inhibitory processes in attention, memory, and language (pp. 53–112). Orlando: Academic Press.
Iarocci, G., & Burack, J. A. (2004). Intact covert orienting to peripheral cues among children with autism. Journal of Autism and Developmental Disorders, 34(3), 257–264.
Johnson, B. P., Lum, J. A., 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.
Johnson, B. P., Rinehart, N. J., Papadopoulos, N., Tonge, B., Millist, L., White, O., et al. (2012). A closer look at visually guided saccades in autism and Asperger’s disorder. Frontiers in Integrative Neuroscience, 6, 99.
Johnson, B. P., Rinehart, N. J., White, O., Millist, L., & Fielding, J. (2013). Saccade adaptation in autism and Asperger’s disorder. Neuroscience, 243, 76–87.
Kaldy, Z., Giserman, I., Carter, A. S., & Blaser, E. (2016). The mechanisms underlying the ASD advantage in visual search. Journal of Autism and Developmental Disorders. 46, 1513–1527
Keehn, B., Lincoln, A. J., Muller, R. A., & Townsend, J. (2010). Attentional networks in children and adolescents with autism spectrum disorder. Journal of Child Psychology and Psychiatry, 51(11), 1251–1259.
Keehn, B., Muller, R. A., & Townsend, J. (2013). Atypical attentional networks and the emergence of autism. Neuroscience and Biobehavioral Reviews, 37(2), 164–183.
Laidi, C., Boisgontier, J., Chakravarty, M. M., Hotier, S., d’Albis, M. A., Mangin, J. O., et al. (2017). Cerebellar anatomical alterations and attention to eyes in autism. Scientific Reports, 7(1), 1–11.
Levy, S. E., Giarelli, E., Lee, L.-C., Schieve, L. A., Kirby, R. S., Cunniff, C., et al. (2010). Autism spectrum disorder and co-occurring developmental, psychiatric, and medical conditions among children in multiple populations of the United States. Journal of Developmental and Behavioral Pediatrics, 31, 267–275.
Murphy, C. M., Christakou, A., Daly, E. M., Ecker, C., Giampietro, V., Brammer, M., et al. (2014). Abnormal functional activation and maturation of fronto-striato-temporal and cerebellar regions during sustained attention in autism spectrum disorder. American Journal of Psychiatry, 171, 1107–1116.
Mutreja, R., Craig, C., & O’Boyle, M. W. (2016). Attentional network deficits in children with autism spectrum disorder. Developmental Neurorehabilitation, 19(6), 389–397.
O’Halloran, C. J., Kinsella, G. J., & Storey, E. (2012). The cerebellum and neuropsychological functioning: A critical review. Journal of Clinical and Experimental Neuropsychology, 34(1), 35–56.
Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9(1), 97–113.
Papadopoulos, N., McGinley, J., Tonge, B., Bradshaw, J., Saunders, K., Murphy, A., et al. (2012). Motor proficiency and emotional/behavioural disturbance in autism and Asperger’s disorder: Another piece of the neurological puzzle? Autism, 16(6), 627–640.
Parsons, T. D., & Carlew, A. R. (2016). Bimodal virtual reality stroop for assessing distractor inhibition in autism spectrum disorders. Journal of Autism and Developmental Disorders, 46(4), 1255–1267.
Ramnani, N. (2012). Frontal lobe and posterior parietal contributions to the cortico-cerebellar system. Cerebellum, 11(2), 366–383.
Rinehart, N. J., Bellgrove, M. A., Tonge, B. J., Brereton, A. V., Howells-Rankin, D., & Bradshaw, J. L. (2006a). An examination of movement kinematics in young people with high-functioning autism and Asperger’s disorder: Further evidence for a motor planning deficit. Journal of Autism and Developmental Disorders, 36(6), 757–767.
Rinehart, N. J., Bradshaw, J. L., Brereton, A. V., & Tonge, B. (2001). Movement preparation in high-functioning autism and asperger disorder, a serial choice reaction time task involving motor reprogramming. Journal of Autism and Developmental Disorders, 31(1), 79–88.
Rinehart, N. J., Tonge, B., Bradshaw, J. L., Iansek, R., Enticott, P. G., & McGinley, J. (2006b). Gait function in high-functioning autism and Asperger’s disorder: Evidence for basal-ganglia and cerebellar involvement? European Child and Adolescent Psychiatry, 15(5), 256–264.
Rinehart, N. J., Tonge, B. J., Bradshaw, J. L., Iansek, R., Enticott, P. G., & Johnson, K. A. (2006c). Movement-related potentials in high-functioning autism and Asperger’s disorder. Developmental Medicine and Child Neurology, 48(4), 272–277.
Sanderson, C., & Allen, M. L. (2013). The specificity of inhibitory impairments in autism and their relation to ADHD-type symptoms. Journal of Autism and Developmental Disorders, 43(5), 1065–1079.
Sattler, J. M., & Dumont, R. (2004). Assessment of children: WISC-IV and WPPSI-III supplement. San Diego: Sattler.
Sokolov, A. A., Miall, R. C., & Ivry, R. B. (2017). The cerebellum: Adaptive prediction for movement and cognition. Trends in Cognitive Sciences, 21(5), 313–332.
Stanley-Cary, C., Rinehart, N. J., Tonge, B., White, O., & Fielding, J. (2011). Greater disruption to control of voluntary saccades in autistic disorder than Asperger’s disorder: Evidence for greater cerebellar involvement in autism? Cerebellum, 10(1), 70–80.
Tomlinson, S. P., Davis, N. J., & Bracewell, R. M. (2013). Brain stimulation studies of non-motor cerebellar function: A systematic review. Neuroscience and Biobehavioral Reviews, 37(5), 766–789.
Townsend, J., Courchesne, E., Covington, J., Westerfield, M., Harris, N. S., Lyden, P., et al. (1999). Spatial attention deficits in patients with acquired or developmental cerebellar abnormality. The Journal of Neuroscience, 19(13), 5632–5643.
Walker, R., Deubel, H., Schneider, W. X., & Findlay, J. M. (1997). Effect of remote distractors on saccade programming: Evidence for an extended fixation zone. Journal of Neurophysiology, 78, 1108–1119.
Acknowledgments
We would like to thank the paediatricians at Melbourne Children’s Clinic for supporting the study and assisting with recruitment. We are also especially grateful to our participants and their families for generously offering to take part in this study. This paper has been prepared as part of a doctoral thesis.
Funding
The work was supported by doctoral research funding from the School of Psychological Sciences and Monash Institute of Cognitive and Clinical Neurosciences, Monash University, Clayton, VIC, 3800, Australia.
Author information
Authors and Affiliations
Contributions
EL and JF designed the study. NR advised on participant-related processes and assisted EL with recruitment. EL collected the data and performed data analysis. All authors were involved in manuscript drafting and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
NR has received funding from the Ferrero Group Australia, Moose Toys and the Australian Football League. Ferrero Group Australia, Moose Toys and the Australian Football League had no role in this research including the collection, analysis, and interpretation of data, writing of the manuscript, and decision to submit the article for publication. NR has received speaker honorarium from Novartis (2002), Pfzier (2006) and Nutricia (2007). JF has also received research grants for Novartis (2015) and Sanofi-Genzyme (2017). NR is a Director of the Amaze Board (Autism Victoria). EL, NR and JF each declares that she has no conflict of interest.
Ethical Approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed Consent
Informed consent was obtained from all individual participants included in the study.
Rights and permissions
About this article
Cite this article
Lindor, E., Rinehart, N. & Fielding, J. Distractor Inhibition in Autism Spectrum Disorder: Evidence of a Selective Impairment for Individuals with Co-occurring Motor Difficulties. J Autism Dev Disord 49, 669–682 (2019). https://doi.org/10.1007/s10803-018-3744-1
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10803-018-3744-1