Skip to main content
SpringerLink
Log in

Neural Basis of Visual Attentional Orienting in Childhood Autism Spectrum Disorders

  • Original Paper
  • Published:
Journal of Autism and Developmental Disorders Aims and scope Submit manuscript

Abstract

We examined spontaneous attention orienting to visual salience in stimuli without social significance using a modified Dot-Probe task during functional magnetic resonance imaging in high-functioning preadolescent children with Autism Spectrum Disorder (ASD) and age- and IQ-matched control children. While the magnitude of attentional bias (faster response to probes in the location of solid color patch) to visually salient stimuli was similar in the groups, activation differences in frontal and temporoparietal regions suggested hyper-sensitivity to visual salience or to sameness in ASD children. Further, activation in a subset of those regions was associated with symptoms of restricted and repetitive behavior. Thus, atypicalities in response to visual properties of stimuli may drive attentional orienting problems associated with ASD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders V (Fifth). Arlington, VA: American Psychiatric Publishing.

    Book  Google Scholar 

  • Amso, D., Haas, S., Tenenbaum, E., Markant, J., & Sheinkopf, S. J. (2014). Bottom-up attention orienting in young children with autism. Journal of Autism and Developmental Disorders, 44(3), 664–673. doi:10.1007/s10803-013-1925-5.

  • Awh, E., Belopolsky, A. V., & Theeuwes, J. (2012). Top-down versus bottom-up attentional control: A failed theoretical dichotomy. Trends in Cognitive Sciences, 16(8), 437–443. doi:10.1016/j.tics.2012.06.010.

  • 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. doi:10.1038/srep04301.

  • Cavanna, A. E., & Trimble, M. R. (2006). The precuneus: A review of its functional anatomy and behavioural correlates. Brain: A Journal of Neurology, 129(3), 564–583. doi:10.1093/brain/awl004.

  • Corbetta, M., Patel, G., & Shulman, G. L. (2008). The reorienting system of the human brain: From environment to theory of mind. Neuron, 58(3), 306–324. doi:10.1016/j.neuron.2008.04.017.

  • Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3(3), 201–215. doi:10.1038/nrn755.

  • Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., … Davidson, R. J.. (2005). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8(4), 519–526. doi:10.1038/nn1421.

  • Dawson, G., Meltzoff, A. N., Osterling, J., Rinaldi, J., & Brown, E. (1998). Children with autism fail to orient to naturally occurring social stimuli. Journal of Autism and Developmental Disorders, 28(6), 479–485.

    Article  PubMed  Google Scholar 

  • Desimone, R., & Duncan, J. (1995). Neural mechanisms of selective visual attention. Annual Review of Neuroscience, 18(1), 193–222. doi:10.1146/annurev.ne.18.030195.001205.

  • Fischer-Terworth, C., & Probst, P. (2009). Obsessive–compulsive phenomena and symptoms in Asperger’s disorder and high-functioning autism: An evaluative literature review. Life Span and Disability, 12(1), 5–27.

    Google Scholar 

  • Forman, S. D., Cohen, J. D., Fitzgerald, M., Eddy, W. F., Mintun, M. A., & Noll, D. C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fmri): Use of a cluster-size threshold. Magnetic Resonance in Medicine, 33(5), 636–647. doi:10.1002/mrm.1910330508.

  • Freeth, M., Foulsham, T., & Chapman, P. (2011). The influence of visual saliency on fixation patterns in individuals with Autism Spectrum Disorders. Neuropsychologia, 49(1), 156–160. doi:10.1016/j.neuropsychologia.2010.11.012.

  • Hus, V., Gotham, K., & Lord, C. (2014). Standardizing ADOS domain scores: Separating severity of social affect and restricted and repetitive behaviors. Journal of Autism and Developmental Disorders, 44(10), 2400–2412. doi:10.1007/s10803-012-1719-1.

  • Indovina, I., & Macaluso, E. (2007). Dissociation of stimulus relevance and saliency factors during shifts of visuospatial attention. Cerebral Cortex, 17(7), 1701–1711. doi:10.1093/cercor/bhl081.

  • Itti, L., & Koch, C. (2001). Computational modelling of visual attention. Nature Reviews Neuroscience, 2(3), 194–203. doi:10.1038/35058500.

  • 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. doi:10.1111/j.1467-7687.2009.00855.x.

  • Keehn, B., Lincoln, A. J., Müller, 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. doi:10.1111/j.1469-7610.2010.02257.x.

  • Kéïta, L., Mottron, L., Dawson, M., & Bertone, A. (2011). Atypical lateral connectivity: A Neural basis for altered visuospatial processing in autism. Biological Psychiatry, 70(9), 806–811. doi:10.1016/j.biopsych.2011.07.031.

  • Kliemann, D., Dziobek, I., Hatri, A., Baudewig, J., & Heekeren, H. R. (2012). The role of the amygdala in atypical gaze on emotional faces in autism spectrum disorders. The Journal of Neuroscience, 32(28), 9469–9476. doi:10.1523/JNEUROSCI.5294-11.2012.

  • Klin, A., Jones, W., Schultz, R., & Volkmar, F. (2003). The enactive mind, or from actions to cognition: Lessons from autism. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 358(1430), 345–360. doi:10.1098/rstb.2002.1202.

  • Klin, A., Jones, W., Schultz, R., Volkmar, F., & Cohen, D. (2002). Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry, 59(9), 809–816. doi:10.1001/archpsyc.59.9.809.

  • Lainhart, J. E., Bigler, E. D., Bocian, M., Coon, H., Dinh, E., Dawson, G., … Volkmar, F. (2006). Head circumference and height in autism: A study by the collaborative program of excellence in autism. American Journal of Medical Genetics Part A, 140 A(21), 2257–2274. doi:10.1002/ajmg.a.31465.

  • Lavigne, J. V., Cromley, T., Sprafkin, J., & Gadow, K. D. (2009). The child and adolescent symptom inventory-progress monitor: A brief diagnostic and statistical manual of mental disorders, 4th edition-referenced parent-report scale for children and adolescents. Journal of Child and Adolescent Psychopharmacology, 19(3), 241–252. doi:10.1089/cap.2008.052.

  • Lord, C., Risi, S., Lambrecht, L., Cook, E. H. Jr., Leventhal, B. L., DiLavore, P. C., … 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(3), 205–223.

    Article  PubMed  Google Scholar 

  • Lord, C., Rutter, M., & Couteur, A. (1994). Autism diagnostic interview-revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24(5), 659–685. doi:10.1007/BF02172145.

  • Mogg, K., & Bradley, B. P. (1999). Orienting of attention to threatening facial expressions presented under conditions of restricted awareness. Cognition & Emotion, 13(6), 713–740. doi:10.1080/026999399379050.

  • Monk, C. S., Nelson, E. E., McClure, E. B., Mogg, K., Bradley, B. P., Leibenluft, E., … Pine, D. S. (2006). Ventrolateral prefrontal cortex activation and attentional bias in response to angry faces in adolescents with generalized anxiety disorder. The American Journal of Psychiatry, 163(6), 1091–1097. doi:10.1176/appi.ajp.163.6.1091.

  • Monk, C. S., Weng, S.-J., Wiggins, J. L., Kurapati, N., Louro, H. M. C., Carrasco, M., … Lord, C. (2010). Neural circuitry of emotional face processing in autism spectrum disorders. Journal of Psychiatry and Neuroscience, 35(2), 105–114. doi:10.1503/jpn.090085.

  • Perreault, A., Gurnsey, R., Dawson, M., Mottron, L., & Bertone, A. (2011). Increased sensitivity to mirror symmetry in autism. PLOS ONE, 6(4), e19519. doi:10.1371/journal.pone.0019519.

  • Pierce, K., Conant, D., Hazin, R., Stoner, R., & Desmond, J. (2011). Preference for geometric patterns early in life as a risk factor for autism. Archives of General Psychiatry, 68(1), 101–109. doi:10.1001/archgenpsychiatry.2010.113.

  • Posner, M. I., & Petersen, S. E. (1990). The attention system of the human brain. Annual Review of Neuroscience, 13, 25–42. doi:10.1146/annurev.ne.13.030190.000325.

  • Schwarzkopf, D. S., Anderson, E. J., de Haas, B., White, S. J., & Rees, G. (2014). Larger extrastriate population receptive fields in autism spectrum disorders. The Journal of Neuroscience, 34(7), 2713–2724. doi:10.1523/JNEUROSCI.4416-13.2014.

  • Taylor, P. C. J., Muggleton, N. G., Kalla, R., Walsh, V., & Eimer, M. (2011). TMS of the right angular gyrus modulates priming of pop-out in visual search: Combined TMS-ERP evidence. Journal of Neurophysiology, 106(6), 3001–3009. doi:10.1152/jn.00121.2011.

  • Tellegen, A., & Briggs, P. (1967). Old wine in new skins: grouping wechsler subtests into new scaLES. Journal of Consulting Psychology, 31(5), 499–506. doi:10.1037/h0024963.

  • Vogt, B. A., Finch, D. M., & Olson, C. R. (1992). Functional heterogeneity in cingulate cortex: The anterior executive and posterior evaluative regions. Cerebral Cortex, 2(6), 435–443. doi:10.1093/cercor/2.6.435-a.

  • Walther, D., & Koch, C. (2006). Modeling attention to salient proto-objects. Neural Networks, 19(9), 1395–1407. doi:10.1016/j.neunet.2006.10.001.

  • Wechsler, D. (1999). Manual for the Wechsler abbreviated intelligence scale (WASI). San Antonio, TX: The Psychological Corporation.

  • Weiss, L. G., Saklofske, D. H., Prifitera, A., Chen, H.-Y., & Hildebrand, D. (1999). The calculation of the WISC-Ill general ability index using Canadian Norms. Canadian Journal of School Psychology, 14(2), 1–10. doi:10.1177/082957359901400202.

Download references

Author Contributions

EM, LK, and CV designed the study and wrote the manuscript. EM and MN collected data. LK and JS clinically characterized children with ASD. WG designed the study and recruited participants. All authors read and approved the final manuscript.

Funding

Funding for this study came from the National Institutes of Mental Health MH084961, and from Children’s National Medical Center Grant HD040677-07.

Author information

Authors and Affiliations

  1. Department of Psychiatry, Washington University in St. Louis, 4444 Forest Park Parkway, Suite 2100, St Louis, MO, 63108, USA

    Eric R. Murphy

  2. Department of Psychology, University of California, Berkley, Berkley, USA

    Megan Norr

  3. Children’s Research Institute, Children’s National Medical Center, Washington, USA

    John F. Strang, Lauren Kenworthy, William D. Gaillard & Chandan J. Vaidya

  4. Department of Psychology, 306 White-Gravenor Hall, Georgetown University, 37th and O Street, NW, Washington, DC, 20057, USA

    Chandan J. Vaidya

Authors
  1. Eric R. Murphy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Megan Norr
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John F. Strang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lauren Kenworthy
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. William D. Gaillard
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chandan J. Vaidya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eric R. Murphy.

Ethics declarations

Conflict of Interest

Eric R. Murphy, Megan Norr, John F. Strang, Lauren Kenworthy, William D. Gaillard, Chandan J. Vaidya declares that they 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.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 622 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Murphy, E.R., Norr, M., Strang, J.F. et al. Neural Basis of Visual Attentional Orienting in Childhood Autism Spectrum Disorders. J Autism Dev Disord 47, 58–67 (2017). https://doi.org/10.1007/s10803-016-2928-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-016-2928-9

Keywords

Search

Navigation