Skip to main content
Log in

Brief Report: When Large Becomes Slow: Zooming-Out Visual Attention Is Associated to Orienting Deficits in Autism

  • Brief Report
  • Published:
Journal of Autism and Developmental Disorders Aims and scope Submit manuscript

Abstract

Previous studies independently demonstrated impairments in rapid orienting/disengagement and zooming-out of spatial attention in autism spectrum disorder (ASD). These attentional mechanisms, however, are not completely independent. Aiming at a more complete picture of spatial attention deficits in ASD, we examined the relationship between orienting and zooming in participants with ASD and typically developing peers. We modified a classical spatial cuing task, presenting two small or large cues in the two visual hemifields and subsequently cueing attention to one of them. Our results demonstrate a sluggish orienting mechanism in ASD only when a large attentional focus is deployed. Moreover, only the sluggish orienting mechanism in the large cues condition predicts the severity in the social-interaction symptomatology in individuals with ASD.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

References

  • American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (DSM-IV) (4th ed.). American Psychiatric Publishing, Inc.

  • Ames, C., & Fletcher-Watson, S. (2010). A review of methods in the study of attention in autism. Developmental Review, 30(1), 52–73.

    Article  Google Scholar 

  • Bediou, B., Adams, D. M., Mayer, R. E., Tipton, E., Green, C. S., & Bavelier, D. (2018). Meta-analysis of action video game impact on perceptual, attentional, and cognitive skills. Psychological Bulletin, 144(1), 77–110.

    Article  PubMed  Google Scholar 

  • Benso, F., Turatto, M., Mascetti, G. G., & Umiltà, C. (1998). The time course of attentional focusing. European Journal of Cognitive Psychology, 10, 373–388.

  • Bertone, A., Mottron, L., Jelenic, P., & Faubert, J. (2005). Enhanced and diminished visuo-spatial information processing in autism depends on stimulus complexity. Brain, 128(10), 2430–2441.

    Article  PubMed  Google Scholar 

  • Carrasco, M. (2011). Visual attention: The past 25 years. Vision Research, 51(13), 1484–1525. https://doi.org/10.1016/j.visres.2011.04.012.

    Article  PubMed  PubMed Central  Google Scholar 

  • Castiello, U., & Umiltà, C. (1992). Splitting focal attention. Journal of Experimental Psychology: Human Perception and Performance, 18(3), 837–848.

    PubMed  Google Scholar 

  • Castiello, U., & Umiltà, C. (1990). Size of the attentional focus and efficiency of processing. Acta Psychologica, 73(3), 195–209.

    Article  PubMed  Google Scholar 

  • Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3(3), 215–229.

    Article  Google Scholar 

  • Courchesne, E., Townsend, J., Akshoomoff, N. A., Saitoh, O., Yeung-Courchesne, R., Lincoln, A. J., … Lau, L. (1994). Impairment in shifting attention in autistic and cerebellar patients. Behavioral Neuroscience, 108(5), 848.

    Article  PubMed  Google Scholar 

  • Dakin, S., & Frith, U. (2005). Vagaries of visual perception in autism. Neuron, 48(3), 497–507.

    Article  PubMed  Google Scholar 

  • Elsabbagh, M., Fernandes, J., Jane Webb, S., Dawson, G., Charman, T., & Johnson, M.H. & British Autism Study of Infant Siblings Team. (2013). Disengagement of visual attention in infancy is associated with emerging autism in toddlerhood. Biological Psychiatry, 74(3), 189–194. https://doi.org/10.1016/j.biopsych.2012.11.030.

    Article  PubMed  PubMed Central  Google Scholar 

  • Eriksen, C. W., & St James, J. D. (1986). Visual attention within and around the field of focal attention: A zoom lens model. Perception and Psychophysics, 40(4), 225–240.

    Article  PubMed  Google Scholar 

  • Facoetti, A., Trussardi, A. N., Ruffino, M., Lorusso, M. L., Cattaneo, C., Galli, R., … Zorzi, M. (2010). Multisensory spatial attention deficits are predictive of phonological decoding skills in developmental dyslexia. Journal of Cognitive Neuroscience, 22(5), 1011–1025.

    Article  PubMed  Google Scholar 

  • Franceschini, S., Bertoni, S., Gianesini, T., Gori, S., & Facoetti, A. (2017a). A different vision of dyslexia: Local precedence on global perception. Scientific Reports, 7(1), 17462.

    Article  PubMed  PubMed Central  Google Scholar 

  • Franceschini, S., Gori, S., Ruffino, M., Viola, S., Molteni, M., & Facoetti, A. (2013). Action video games make dyslexic children read better. Current Biology, 23(6), 462–466. https://doi.org/10.1016/j.cub.2013.01.044.

    Article  PubMed  Google Scholar 

  • Franceschini, S., Trevisan, P., Ronconi, L., Bertoni, S., Colmar, S., Double, K., … Gori, S. (2017b). Action video games improve reading abilities and visual-to-auditory attentional shifting in english-speaking children with dyslexia. Scientific Reports. https://doi.org/10.1038/s41598-017-05826-8.

    Google Scholar 

  • Frith, U., & Happé, F. (1994). Autism: Beyond “theory of mind”. Cognition, 50(1), 115–132.

    Article  PubMed  Google Scholar 

  • Fu, S., Caggiano, D. M., Greenwood, P. M., & Parasuraman, R. (2005). Event-related potentials reveal dissociable mechanisms for orienting and focusing visuospatial attention. Cognitive Brain Research, 23(2–3), 341–353.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gliga, T., Bedford, R., Charman, T., & Johnson, M. H. & BASIS Team. (2015). Enhanced visual search in infancy predicts emerging autism symptoms. Current Biology, 25(13), 1727–1730. https://doi.org/10.1016/j.cub.2015.05.011.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gori, S., Seitz, A. R., Ronconi, L., Franceschini, S., & Facoetti, A. (2016). Multiple causal links between magnocellular—dorsal pathway deficit and developmental dyslexia. Cerebral Cortex, 26(11), 4356–4369.

    Article  PubMed  Google Scholar 

  • Green, C. S., Pouget, A., & Bavelier, D. (2010). Improved probabilistic inference as a general learning mechanism with action video games. Current Biology, 20(17), 1573–1579. https://doi.org/10.1016/j.cub.2010.07.040.

    Article  PubMed  PubMed Central  Google Scholar 

  • Keehn, B., Muller, R. A., & Townsend, J. (2013). Atypical attentional networks and the emergence of autism. Neuroscience and Biobehavioral Reviews, 37(2), 164–183. https://doi.org/10.1016/j.neubiorev.2012.11.014.

    Article  PubMed  Google Scholar 

  • Klein, R. M. (2000). Inhibition of return. Trends in Cognitive Sciences, 4(4), 138–147.

    Article  PubMed  Google Scholar 

  • Landry, R., & Bryson, S. E. (2004). Impaired disengagement of attention in young children with autism. Journal of Child Psychology and Psychiatry, 45(6), 1115–1122.

    Article  PubMed  Google Scholar 

  • Lord, C., Rutter, M., DiLavore, P., & Risi, S. (2002). Autism diagnostic observation schedule. Los Angeles: ADOS Western Psychological Services.

    Google Scholar 

  • Mann, T. A., & Walker, P. (2003). Autism and a deficit in broadening the spread of visual attention. Journal of Child Psychology and Psychiatry, 44(2), 274–284.

    Article  PubMed  Google Scholar 

  • McMains, S. A., & Somers, D. C. (2004). Multiple spotlights of attentional selection in human visual cortex. Neuron, 42(4), 677–686.

    Article  PubMed  Google Scholar 

  • McMains, S. A., & Somers, D. C. (2005). Processing efficiency of divided spatial attention mechanisms in human visual cortex. The Journal of Neuroscience, 25(41), 9444–9448.

    Article  PubMed  Google Scholar 

  • Mottron, L., Dawson, M., Soulieres, I., Hubert, B., & Burack, J. (2006). Enhanced perceptual functioning in autism: An update, and eight principles of autistic perception. Journal of Autism and Developmental Disorders, 36(1), 27–43.

    Article  PubMed  Google Scholar 

  • Müller, M. M., Malinowski, P., Gruber, T., & Hillyard, S. A. (2003b). Sustained division of the attentional spotlight. Nature, 424(6946), 309–312.

    Article  PubMed  Google Scholar 

  • Müller, N. G., Bartelt, O. A., Donner, T. H., Villringer, A., & Brandt, S. A. (2003a). A physiological correlate of the “zoom lens” of visual attention. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 23(9), 3561–3565.

    Article  Google Scholar 

  • Mundy, P. (2003). Annotation: The neural basis of social impairments in autism: The role of the dorsal medial-frontal cortex and anterior cingulate system. Journal of Child Psychology and Psychiatry, 44(6), 793–809.

    Article  PubMed  Google Scholar 

  • Mundy, P., & Newell, L. (2007). Attention, joint attention, and social cognition. Current Directions in Psychological Science, 16(5), 269–274.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pellicano, E., & Burr, D. (2012). When the world becomes ‘too real’: A Bayesian explanation of autistic perception. Trends in cognitive sciences, 16(10), 504–510.

    Article  PubMed  Google Scholar 

  • Posner, M. I. (1980). Orienting of attention. Quarterly Journal of Experimental Psychology, 32(1), 3–25.

    Article  PubMed  Google Scholar 

  • Posner, M. I., & Cohen, Y. (1984). Components of visual orienting. Attention and Performance X: Control of Language Processes, 32, 531–556.

    Google Scholar 

  • Posner, M. I., & Petersen, S. E. (1990). The attention system of the human brain. Annual Review of Neuroscience, 13(1), 25–42.

    Article  PubMed  Google Scholar 

  • Robertson, C. E., Kravitz, D. J., Freyberg, J., Baron-Cohen, S., & Baker, C. I. (2013). Tunnel vision: Sharper gradient of spatial attention in autism. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 33(16), 6776–6781. https://doi.org/10.1523/JNEUROSCI.5120-12.

    Article  Google Scholar 

  • Ronconi, L., Basso, D., Gori, S., & Facoetti, A. (2014a). TMS on right frontal eye fields induces an inflexible focus of attention. Cerebral Cortex, 24(2), 396–402. https://doi.org/10.1093/cercor/bhs319.

    Article  PubMed  Google Scholar 

  • Ronconi, L., Facoetti, A., Bulf, H., Franchin, L., Bettoni, R., & Valenza, E. (2014b). Paternal autistic traits are predictive of infants visual attention. Journal of Autism and Developmental Disorders, 44(7), 1556–1564. https://doi.org/10.1007/s10803-013-2018-1.

    Article  PubMed  Google Scholar 

  • Ronconi, L., Franchin, L., Valenza, E., Gori, S., & Facoetti, A. (2016). The attentional ‘zoom-lens’ in 8-month-old infants. Developmental Science, 19(1), 145–154. https://doi.org/10.1111/desc.12288.

    Article  PubMed  Google Scholar 

  • Ronconi, L., Gori, S., Ruffino, M., Franceschini, S., Urbani, B., Molteni, M., & Facoetti, A. (2012). Decreased coherent motion discrimination in autism spectrum disorder: The role of attentional zoom-out deficit. PloS ONE, 7(11), e49019.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ronconi, L., Gori, S., Ruffino, M., Molteni, M., & Facoetti, A. (2013). Zoom-out attentional impairment in children with autism spectrum disorder. Cortex, 49(4), 1025–1033. https://doi.org/10.1016/j.cortex.2012.03.005.

    Article  PubMed  Google Scholar 

  • Ronconi, L., Molteni, M., & Casartelli, L. (2016). Building blocks of others’ understanding: A perspective shift in investigating social-communicative deficit in autism. Frontiers in Human Neuroscience, 10, 144.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rutter, M., Bailey, A., Lord, C., & Berument, S. (2003). Social communication questionnaire. Los Angeles: Western Psychological Services.

    Google Scholar 

  • Sacrey, L. R., Armstrong, V. L., Bryson, S. E., & Zwaigenbaum, L. (2014). Impairments to visual disengagement in autism spectrum disorder: A review of experimental studies from infancy to adulthood. Neuroscience and Biobehavioral Reviews, 47, 559–577.

    Article  PubMed  Google Scholar 

  • Simmons, D. R., Robertson, A. E., McKay, L. S., Toal, E., McAleer, P., & Pollick, F. E. (2009). Vision in autism spectrum disorders. Vision Research, 49(22), 2705–2739.

    Article  PubMed  Google Scholar 

  • Townsend, J., Courchesne, E., & Egaas, B. (1996). Slowed orienting of covert visual-spatial attention in autism: Specific deficits associated with cerebellar and parietal abnormality. Development and Psychopathology, 8(03), 563–584.

    Article  Google Scholar 

  • Turatto, M., Benso, F., Facoetti, A., Galfano, G., Mascetti, G. G., & Umiltà, C. (2000). Automatic and voluntary focusing of attention. Perception, and Psychophysics, 62(5), 935–952.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Wainwright-Sharp, J. A., & Bryson, S. E. (1993). Visual orienting deficits in high-functioning people with autism. Journal of Autism and Developmental Disorders, 23(1), 1–13.

    Article  PubMed  Google Scholar 

  • Wass, S., Porayska-Pomsta, K., & Johnson, M. H. (2011). Training attentional control in infancy. Current Biology, 21(18), 1543–1547.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wechsler, D. (1991). WISC-III: Wechsler intelligence scale for children. San Antonio, TX: Psychological Corporation.

    Google Scholar 

Download references

Acknowledgments

The contributions of staff members from the Scientific Institute “E. Medea” (Bosisio Parini) and of Dr. Gialuigi Visentini from “Associazione La Nostra Famiglia” (Padova) as well as of participants with ASD and their families are gratefully acknowledged. This work was supported by grants from the University of Padua (“Junior Post-Doc Researcher 2014–2016” to A.F. and L.R., “Senior Post Doc Researcher 2014–2016” to S.G., “Progetti di Eccellenza CARIPARO 2012–2014 rep. no. 1873/2012” to L.R., S.G., and A.F.).

Author Contributions

LR, SG and AF designed the study. LR and MD collected the data. LR and AF analyzed the data. MM provided supervision for clinical characterization of the participants. LR wrote the manuscript with support and critical revisions from all the co-authors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luca Ronconi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ronconi, L., Devita, M., Molteni, M. et al. Brief Report: When Large Becomes Slow: Zooming-Out Visual Attention Is Associated to Orienting Deficits in Autism. J Autism Dev Disord 48, 2577–2584 (2018). https://doi.org/10.1007/s10803-018-3506-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-018-3506-0

Keywords

Navigation