Skip to main content
SpringerLink
Log in

Social and Non-Social Cueing of Visuospatial Attention in Autism and Typical Development

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

Abstract

Three experiments explored attention to eye gaze, which is incompletely understood in typical development and is hypothesized to be disrupted in autism. Experiment 1 (n = 26 typical adults) involved covert orienting to box, arrow, and gaze cues at two probabilities and cue-target times to test whether reorienting for gaze is endogenous, exogenous, or unique; experiment 2 (total n = 80: male and female children and adults) studied age and sex effects on gaze cueing. Gaze cueing appears endogenous and may strengthen in typical development. Experiment 3 tested exogenous, endogenous, and gaze-based orienting in 25 typical and 27 Autistic Spectrum Disorder (ASD) children. ASD children made more saccades, slowing their reaction times; however, exogenous and endogenous orienting, including gaze cueing, appear intact in 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
Fig. 4
Fig. 5

Similar content being viewed by others

Notes

  1. In an interaction the dependent variable changes different amounts for a given change of one independent variable, depending on the levels of another independent variable. For example, here, the effect of validity on RT is different at the two different SOAs.

  2. We originally questioned reports of reflexive arrow cueing (Tipples, 2002); we purposely implemented a large target eccentricity to central stimulus size ratio to bias against finding this result; but our own data have convinced us about the robust nature of reflexive arrow cueing.

  3. We used a photo in experiment 2 because early piloting for experiment 3 raised concerns that typical children might not show a gaze cueing effect for cartoon cues. After collection of more data, we decided to keep the cartoon for experiment 3. It is our belief that the nature of the cue (photo or cartoon) matters little for the issues at hand. A small number of typical children were tested with both the photo and cartoon, and they showed robust gaze cueing effects for both stimuli. A larger study would be needed to assess for any quantitative differences across these two types of gaze cues.

  4. Explanation of dfs: acceptable EOG quality on 74/80 subjects, followed by DF-correction for unequal variances across groups.

References

  • Achenbach, T. (2001). CBLC/6-18 profile for boys—syndrome scales. ASEBA.

  • Achenbach, T. (2003). Adult behavior checklist for ages 18–59. ASEBA.

  • Akiyama, T., Kato, M., et al. (2006a). A deficit in discriminating gaze direction in a case with right superior temporal gyrus lesion. Neuropsychologia, 44(2), 161–170.

    Article  PubMed  Google Scholar 

  • Akiyama, T., Kato, M., et al. (2006b). Gaze but not arrows: A dissociative impairment after right superior temporal gyrus damage. Neuropsychologia, 44(10), 1804–1810.

    Article  PubMed  Google Scholar 

  • Allen, G., & Courchesne, E. (2001). Attention function and dysfunction in autism. Frontiers in Bioscience, 6, D105–D119.

    Article  PubMed  Google Scholar 

  • American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed. Text Revision). Washington, DC: American Psychiatric Association.

  • Baron-Cohen, S., Cox, A., Baird, G., Swettenham, J., Nightingale, N., Morgan, K., et al. (1996). Psychological markers in the detection of autism in infancy in a large population. British Journal of Psychiatry, 168(2), 158–163.

    Article  PubMed  Google Scholar 

  • Bayliss, A. P., di Pellegrino, G., & Tipper, S. P. (2005). Sex differences in eye gaze and symbolic cueing of attention. Quarterly Journal of Experimental Psychology A, 58(4), 631–650.

    Google Scholar 

  • Bayliss, A. P., & Tipper, S. P. (2005). Gaze and arrow cueing of attention reveals individual differences along the autism spectrum as a function of target context. British Journal of Psychology, 96(Pt 1), 95–114.

    Article  PubMed  Google Scholar 

  • Brignani, D., Guzzon, D., Marzi, C. A., & Miniussi, C. (2009). Attentional orienting induced by arrows and eye-gaze compared with an endogenous cue. Neuropsychologia, 47(2), 370–381.

    Article  PubMed  Google Scholar 

  • Brodeur, D. A., & Enns, J. T. (1997). Covert visual orienting across the lifespan. Canadian Journal of Experimental Psychology, 51(1), 20–35.

    PubMed  Google Scholar 

  • Casey, B. J., Gordon, C. T., Mannheim, G. B., & Rumsey, J. M. (1993). Dysfunctional attention in autistic savants. Journal of Clinical Experimental Neuropsychology, 15(6), 933–946.

    Article  Google Scholar 

  • Chawarska, K., Klin, A., & Volkmar, F. (2003). Automatic attention cueing through eye movement in 2-year-old children with autism. Child Development, 74(4), 1108–1122.

    Article  PubMed  Google Scholar 

  • Chawarska, K., Volkmar, F., et al. (2010). Limited attentional bias for faces in toddlers with autism spectrum disorders. Archives of General Psychiatry, 67(2), 178–185.

    Article  PubMed  Google Scholar 

  • Collie, A., Maruff, P., Yucel, M., Danckert, J., & Currie, J. (2000). Spatiotemporal distribution of facilitation and inhibition of return arising from the reflexive orienting of covert attention. Journal of Experimental Psychology: Human Perception and Performance, 26(6), 1733–1745.

    Article  PubMed  Google Scholar 

  • Constantino, J. N. (2002). The social responsiveness scale. Los Angeles: Western Psychological Services.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Cornish, K. M., Manly, T., Savage, R., Swanson, J., Morisano, D., Butler, N., et al. (2005). Association of the dopamine transporter (DAT1) 10/10-repeat genotype with ADHD symptoms and response inhibition in a general population sample. Molecular Psychiatry, 10(7), 686–698.

    Article  PubMed  Google Scholar 

  • Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., et al. (2005). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8(4), 519–526.

    PubMed  Google Scholar 

  • Driver, J., Davis, G., Ricciardelli, P., Kidd, P., Maxwell, E., & Baron-Cohen, S. (1999). Gaze perception triggers reflexive visuospatial orienting. Visual Cognition, 6(5), 509–540.

    Article  Google Scholar 

  • Emery, N. J. (2000). The eyes have it: The neuroethology, function and evolution of social gaze. Neuroscience and Biobehavioral Reviews, 24(6), 581–604.

    Article  PubMed  Google Scholar 

  • Faust, M. E., Balota, D. A., Ferraro, F. R., & Spieler, D. H. (1999). Individual differences in information-processing rate and amount: Implications for group differences in response latency. Psychological Bulletin, 125(6), 777–799.

    Article  PubMed  Google Scholar 

  • Fombonne, E. (2005). Epidemiology of autistic disorder and other pervasive developmental disorders. Journal of Clinical Psychiatry, 66(suppl 10), 3–8.

    PubMed  Google Scholar 

  • Friesen, C. K., & Kingstone, A. (1998). The eyes have it! Reflexive orienting is triggered by nonpredictive gaze. Psychonomic Bulletin & Review, 5(3), 490–495.

    Article  Google Scholar 

  • Friesen, C. K., & Kingstone, A. (2003). Abrupt onsets and gaze direction cues trigger independent reflexive attentional effects. Cognition, 87(1), B1–B10.

    Article  PubMed  Google Scholar 

  • Frischen, A., Bayliss, A. P., & Tipper, S. P. (2007). Gaze cueing of attention: visual attention, social cognition, and individual differences. Psychological Bulletin, 133(4), 694–724.

    Article  PubMed  Google Scholar 

  • Goldberg, M. C., Landa, R., Lasker, A., Cooper, L., & Zee, D. S. (2000). Evidence of normal cerebellar control of the vestibulo-ocular reflex (VOR) in children with high-functioning autism. Journal of Autism and Developmental Disorders, 30(6), 519–524.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Goldberg, M. C., Mostow, A. J., et al. (2007). Evidence for impairments in using static line drawings of eye gaze cues to orient visual-spatial attention in children with high functioning autism. Journal of Autism and Developmental Disorders, 38(8), 1405–1413.

    Article  PubMed  Google Scholar 

  • Greene, D. J., Mooshagian, E., et al. (2009). The neural correlates of social attention: Automatic orienting to social and nonsocial cues. Psychological Research, 73(4), 499–511.

    Article  PubMed  Google Scholar 

  • Hadjikhani, N., Joseph, R. M., Snyder, J., Chabris, C. F., Clark, J., Steele, S., et al. (2004). Activation of the fusiform gyrus when individuals with autism spectrum disorder view faces. Neuroimage, 22(3), 1141–1150.

    Article  PubMed  Google Scholar 

  • Hietanen, J. K., Nummenmaa, L., et al. (2006). Automatic attention orienting by social and symbolic cues activates different neural networks: An fMRI study. Neuroimage, 33(1), 406–413.

    Article  PubMed  Google Scholar 

  • Howlin, P., Magiati, I., & Charman, T. (2009). Systematic review of early intensive behavioral interventions for children with autism. American Journal of Intellectual and Developmental Disabilities, 114(1), 23–41.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Itier, R. J., & Batty, M. (2009). Neural bases of eye and gaze processing: The core of social cognition. Neuroscience and Biobehavioral Reviews, 33(6), 843–863.

    Article  PubMed  Google Scholar 

  • Kertesz, A., Nicholson, I., et al. (1985). Motor impersistence: A right-hemisphere syndrome. Neurology, 35(5), 662–666.

    PubMed  Google Scholar 

  • Kingstone, A., Friesen, C. K., & Gazzaniga, M. S. (2000). Reflexive joint attention depends on lateralized cortical connections. Psychological Science, 11(2), 159–166.

    Article  PubMed  Google Scholar 

  • Kingstone, A., Tipper, C., Ristic, J., & Ngan, E. (2004). The eyes have it! An fMRI investigation. Brain and Cognition, 55(2), 269–271.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Kogan, M. D., Blumberg, S. J., Schieve, L. A., Boyle, C. A., Perrin, J. M., Ghandour, R. M., et al. (2009). Prevalence of parent-reported diagnosis of autism spectrum disorder among children in the US, 2007. Pediatrics, 124(4), 1395–1403.

    Article  PubMed  Google Scholar 

  • Kylliainen, A., & Hietanen, J. K. (2004). Attention orienting by another’s gaze direction in children with autism. Journal of Child Psychology and Psychiatry, 45(3), 435–444.

    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 

  • Langton, S. R. H., & Bruce, V. (1999). Reflexive visual orienting in response to the social attention of others. Visual Cognition, 6(5), 541–567.

    Article  Google Scholar 

  • Loe, I. M., Feldman, H. M., Yasui, E., & Luna, B. (2009). Oculomotor performance identifies underlying cognitive deficits in attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 48(4), 431–440.

    Article  PubMed  Google Scholar 

  • Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Jr., Leventhal, B. L., DiLavore, P. C., et al. (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., & Le 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • MacPherson, A. C., Klein, R. M., & Moore, C. (2003). Inhibition of return in children and adolescents. Journal of Experimental Child Psychology, 85(4), 337–351.

    Article  PubMed  Google Scholar 

  • Mahone, E. M., Powell, S. K., et al. (2006). Motor persistence and inhibition in autism and ADHD. Journal of the International Neuropsychological Society, 12(5), 622–631.

    Article  PubMed  Google Scholar 

  • Maruff, P., Yucel, M., Danckert, J., Stuart, G., & Currie, J. (1999). Facilitation and inhibition arising from the exogenous orienting of covert attention depends on the temporal properties of spatial cues and targets. Neuropsychologia, 37(6), 731–744.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Morales, M., Mundy, P., Delgado, C. E. F., Yale, M., Messinger, D., Neal, R., et al. (2000). Responding to joint attention across the 6- through 24-month age period and early language acquisition. Journal of Applied Developmental Psychology, 21(4), 283–298.

    Article  Google Scholar 

  • Mosconi, M. W., Mack, P. B., et al. (2005). Taking an “intentional stance” on eye-gaze shifts: A functional neuroimaging study of social perception in children. Neuroimage, 27(1), 247–252.

    Article  PubMed  Google Scholar 

  • Nation, K., & Penny, S. (2008). Sensitivity to eye gaze in autism: Is it normal? Is it automatic? Is it social? Developmental Psychopathology, 20(1), 79–97.

    Article  Google Scholar 

  • Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9(1), 97–113.

    Article  PubMed  Google Scholar 

  • Pelphrey, K. A., Morris, J. P., et al. (2005). Neural basis of eye gaze processing deficits in autism. Brain, 128(Pt 5), 1038–1048.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Posner, M. I., Rafal, R. D., Choate, L. S., & Vaughan, J. (1985). Inhibition of return: Neural basis and function. Cognitive Neuropsychology, 2(3), 211–228.

    Article  Google Scholar 

  • Reichow, B., & Wolery, M. (2009). Comprehensive synthesis of early intensive behavioral interventions for young children with autism based on the UCLA young autism project model. Journal of Autism and Developmental Disorders, 39(1), 23–41.

    Article  PubMed  Google Scholar 

  • Ristic, J., Friesen, C. K., & Kingstone, A. (2002). Are eyes special? It depends on how you look at it. Psychonomic Bulletin Review, 9(3), 507–513.

    Article  PubMed  Google Scholar 

  • Ristic, J., Mottron, L., Friesen, C. K., Iarocci, G., Burack, J. A., & Kingstone, A. (2005). Eyes are special but not for everyone: The case of autism. Brain Research: Cognitive Brain Research, 24(3), 715–718.

    Article  PubMed  Google Scholar 

  • Rutherford, M. D., & Krysko, K. M. (2008). Eye direction, not movement direction, predicts attention shifts in those with autism spectrum disorders. Journal of Autism and Developmental Disorders, 38(10), 1958–1965.

    Article  PubMed  Google Scholar 

  • Senju, A., Tojo, Y., Dairoku, H., & Hasegawa, T. (2004). Reflexive orienting in response to eye gaze and arrow in children with and without autism. Journal of Child Psychology and Psychiatry, 45(3), 445–458.

    Article  PubMed  Google Scholar 

  • Swettenham, J., Condie, S., Campbell, R., Milne, E., & Coleman, M. (2003). Does the perception of moving eyes trigger reflexive visual orienting in autism? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358(1430), 325–334.

    Article  PubMed  Google Scholar 

  • Tipper, C. M., Handy, T. C., et al. (2008). Brain responses to biological relevance. Journal of Cognitive Neuroscience, 20(5), 879–891.

    Article  PubMed  Google Scholar 

  • Tipples, J. (2002). Eye gaze is not unique: Automatic orienting in response to uninformative arrows. Psychonomic Bulletin Review, 9(2), 314–318.

    Article  PubMed  Google Scholar 

  • Townsend, J., Harris, N. S., & Courchesne, E. (1996). Visual attention abnormalities in autism: Delayed orienting to location. Journal of the International Neuropsychological Society, 2(6), 541–550.

    Article  PubMed  Google Scholar 

  • Vecera, S. P., & Rizzo, M. (2003). Spatial attention: Normal processes and their breakdown. Neurologic Clinics, 21(3), 575–607.

    Article  PubMed  Google Scholar 

  • Vecera, S. P., & Rizzo, M. (2004). What are you looking at? Impaired ‘social attention’ following frontal-lobe damage. Neuropsychologia, 42(12), 1657–1665.

    Article  PubMed  Google Scholar 

  • Vecera, S. P., & Rizzo, M. (2006). Eye gaze does not produce reflexive shifts of attention: Evidence from frontal-lobe damage. Neuropsychologia, 44(1), 150–159.

    Article  PubMed  Google Scholar 

  • Vlamings, P. H., Stauder, J. E., van Son, I. A., & Mottron, L. (2005). Atypical visual orienting to gaze- and arrow-cues in adults with high functioning autism. Journal of Autism and Developmental Disorders, 35(3), 267–277.

    Article  PubMed  Google Scholar 

  • Vuilleumier, P. (2002). Perceived gaze direction in faces and spatial attention: A study in patients with parietal damage and unilateral neglect. Neuropsychologia, 40(7), 1013–1026.

    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 

  • Wechsler, D. (2003). Wechsler intelligence scale for children (4th ed.). San Antonio, TX: The Psychological Corporation.

    Google Scholar 

Download references

Acknowledgments

We thank all of the families who generously participated in this study. We thank Maggie M. Gross for study coordination and clinical assessments, Ansley Stanfill for technical support, Fran Miezin for computer engineering, and Patricia LaVesser for clinical assessments. Subjects were recruited with the assistance of the Interactive Autism Network (IAN) Research Database at the Kennedy Krieger Institute and Johns Hopkins Medicine—Baltimore, sponsored by the Autism Speaks Foundation. We thank the Washington University School of Medicine Volunteers for Health (VFH) program; Autism Speaks; Missouri Families for Effective Autism Treatment (MO-FEAT); the Illinois Center for Autism; and other local research laboratories, clinics, schools, and community doctors’ offices for their help in advertising the studies. Research funding included: R21 MH079958, K12 EY16336, T32 DA07261 (John Pruett); The Blanch F. Ittleson Endowment Fund (Richard Todd); McDonnell Center for Higher Brain Function grant “Cueing visual-spatial attention with biologically-relevant versus non-biological stimuli in children and adults with and without autism” (Steve Petersen).

Conflict of Interest Statement

Drs. Pruett and Petersen report no biomedical financial interest or potential conflicts of interest. Dr. Todd is deceased but had no biomedical financial interest or potential conflicts of interest. Dr. Constantino receives royalties on the Social Responsiveness Scale, which is published and distributed by Western Psychological Services. Ms. LaMacchia, Ms. Hoertel, Ms. Squire, and Ms. McVey report no biomedical financial interest or potential conflicts of interest.

Author information

Authors and Affiliations

  1. Department of Psychiatry (Child Division), Washington University School of Medicine, Box 8134, 660 S. Euclid Avenue, St. Louis, MO, 63110, USA

    John R. Pruett Jr, Angela LaMacchia, Sarah Hoertel & Emma Squire

  2. Department of Neurology, Washington University School of Medicine, St. Louis, MO, USA

    Kelly McVey

  3. Departments of Psychiatry (Child Division) and Genetics, Washington University School of Medicine, Box 8134, 660 S. Euclid Avenue, St. Louis, MO, 63110, USA

    Richard D. Todd

  4. Departments of Psychiatry (Child Division) and Pediatrics, Washington University School of Medicine, St. Louis, MO, USA

    John N. Constantino

  5. Departments of Neurology, Radiology, and Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, MO, USA

    Steven E. Petersen

  6. Departments of Psychology and Biomedical Engineering, Washington University, St. Louis, MO, USA

    Steven E. Petersen

Authors
  1. John R. Pruett Jr
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angela LaMacchia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sarah Hoertel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emma Squire
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kelly McVey
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Richard D. Todd
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. John N. Constantino
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Steven E. Petersen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John R. Pruett Jr.

Additional information

Richard D. Todd is now deceased.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 375 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pruett, J.R., LaMacchia, A., Hoertel, S. et al. Social and Non-Social Cueing of Visuospatial Attention in Autism and Typical Development. J Autism Dev Disord 41, 715–731 (2011). https://doi.org/10.1007/s10803-010-1090-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-010-1090-z

Keywords

Search

Navigation