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Auditory Attentional Disengagement in Children with Autism Spectrum Disorder

  • Brandon KeehnEmail author
  • Girija Kadlaskar
  • Rebecca McNally Keehn
  • Alexander L. Francis
Original Paper

Abstract

Despite early differences in orienting to sounds, no study to date has investigated whether children with ASD demonstrate impairments in attentional disengagement in the auditory modality. Twenty-one 9–15-year-old children with ASD and 20 age- and IQ-matched TD children were presented with an auditory gap–overlap paradigm. Evidence of impaired disengagement in ASD was mixed. Differences in saccadic reaction time for overlap and gap conditions did not differ between groups. However, children with ASD did show increased no-shift trials in the overlap condition, as well as reduced disengagement efficiency compared to their TD peers. These results provide further support for disengagement impairments in ASD, and suggest that these deficits include disengaging from and shifting to unimodal auditory information.

Keywords

Autism spectrum disorder Attention Auditory Disengagement Eye movements EOG 

Notes

Author Contributions

BK conceived of and designed the study. ALF participated in the design of the study. BK, GK, and RMK acquired the data. BK performed the statistical analyses and drafted the manuscript. GK, RMK, and ALF helped revise the manuscript. All authors read and approved the final version of the manuscript.

Compliance with Ethical Standards

Conflict of interest

All authors report 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 assent and consent was obtained from all individual participants included in the study.

References

  1. Anderson, C. J., & Colombo, J. (2009). Larger tonic pupil size in young children with autism spectrum disorder. Developmental Psychobiology, 51(2), 207–211.Google Scholar
  2. Anderson, C. J., Colombo, J., & Unruh, K. E. (2013). Pupil and salivary indicators of autonomic dysfunction in autism spectrum disorder. Developmental Psychobiology, 55(5), 465–482.Google Scholar
  3. Baranek, G. T. (1999). Autism during infancy: A retrospective video analysis of sensory-motor and social behaviors at 9–12 months of age. Journal of Autism and Developmental Disorders, 29(3), 213–224.Google Scholar
  4. Colombo, J. (2002). Infant attention grows up: The emergence of a developmental cognitive neuroscience perspective. Current Directions in Psychological Science, 11(6), 196–200.Google Scholar
  5. Colombo, J., Richman, W. A., Shaddy, D. J., Greenhoot, A. F., & Maikranz, J. M. (2001). Heart rate-defined phases of attention, look duration, and infant performance in the paired-comparison paradigm. Child Development, 72(6), 1605–1616.Google Scholar
  6. Connolly, J. D., Goodale, M. A., Goltz, H. C., & Munoz, D. P. (2005). fMRI activation in the human frontal eye field is correlated with saccadic reaction time. Journal of Neurophysiology, 94(1), 605–611.Google Scholar
  7. Constantino, J. M., & Gruber, C. P. (2012). Social Responsiveness Scale—second edition (SRS-2). Torrance: Western Psychological Services.Google Scholar
  8. 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.Google Scholar
  9. Curtis, C. E., & Connolly, J. D. (2008). Saccade preparation signals in the human frontal and parietal cortices. Journal of Neurophysiology, 99(1), 133–145.Google Scholar
  10. 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.Google Scholar
  11. Dawson, G., Toth, K., Abbott, R., Osterling, J., Munson, J., Estes, A., et al. (2004). Early social attention impairments in autism: Social orienting, joint attention, and attention to distress. Developmental Psychology, 40(2), 271–283.Google Scholar
  12. Dorris, M. C., & Munoz, D. P. (1995). A neural correlate for the gap effect on saccadic reaction times in monkey. Journal of Neurophysiology, 73(6), 2558–2562.Google Scholar
  13. Elison, J. T., Paterson, S. J., Wolff, J. J., Reznick, J. S., Sasson, N. J., Gu, H., et al. (2013). White matter microstructure and atypical visual orienting in 7-month-olds at risk for autism. American Journal of Psychiatry, 170(8), 899–908.Google Scholar
  14. Elsabbagh, M., Fernandes, J., Jane Webb, S., Dawson, G., Charman, T., & Johnson, M. H. (2013). Disengagement of visual attention in infancy is associated with emerging autism in toddlerhood. Biological Psychiatry, 74(3), 189–194.Google Scholar
  15. Fendrich, R., Hughes, H. C., & Reuter-Lorenz, P. A. (1991). Fixation-point offsets reduce the latency of saccades to acoustic targets. Perception and Psychophysics, 50(4), 383–387.Google Scholar
  16. Fischer, J., Koldewyn, K., Jiang, Y. V., & Kanwisher, N. (2014). Unimpaired attentional disengagement and social orienting in children with autism. Clinical Psychological Science, 2(2), 214–223.Google Scholar
  17. Fischer, J., Smith, H., Martinez-Pedraza, F., Carter, A. S., Kanwisher, N., & Kaldy, Z. (2016). Unimpaired attentional disengagement in toddlers with autism spectrum disorder. Developmental Science, 19(6), 1095–1103.Google Scholar
  18. Frens, M. A., Van Opstal, A. J., & Van der Willigen, R. F. (1995). Spatial and temporal factors determine auditory-visual interactions in human saccadic eye movements. Perception and Psychophysics, 57(6), 802–816.Google Scholar
  19. 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.Google Scholar
  20. Jeste, S. S., & Nelson, C. A., 3rd. (2009). Event related potentials in the understanding of autism spectrum disorders: An analytical review. Journal of Autism and Developmental Disorders, 39(3), 495–510.Google Scholar
  21. Jin, Z., & Reeves, A. (2009). Attentional release in the saccadic gap effect. Vision Research, 49(16), 2045–2055.Google Scholar
  22. Joshi, S., Li, Y., Kalwani, R. M., & Gold, J. I. (2016). Relationships between pupil diameter and neuronal activity in the locus coeruleus, colliculi, and cingulate cortex. Neuron, 89(1), 221–234.Google Scholar
  23. Kadlaskar, G., Seidl, A., Tager-Flusberg, H., Nelson, C., & Keehn, B. (2019). Atypical response to caregiver touch in infants at high-risk for autism spectrum disorder. Journal of Autism and Developmental Disorders.  https://doi.org/10.1007/s10803-019-04021-0.Google Scholar
  24. Keehn, B., Muller, R. A., & Townsend, J. (2013). Atypical attentional networks and the emergence of autism. Neuroscience and Biobehavioral Reviews, 37(2), 164–183.Google Scholar
  25. Keehn, B., Nair, A., Lincoln, A. J., Townsend, J., & Muller, R. A. (2016). Under-reactive but easily distracted: An fMRI investigation of attentional capture in autism spectrum disorder. Dev Cogn Neurosci, 17, 46–56.Google Scholar
  26. Keehn, B., Westerfield, M., Müller, R. A., & Townsend, J. (2017). Autism, attention, and alpha oscillations: An electrophysiological study of attentional capture. Biological Psychiatry, 2(6), 528–536.Google Scholar
  27. Kingstone, A., & Klein, R. M. (1993). Visual offsets facilitate saccadic latency: Does predisengagement of visuospatial attention mediate this gap effect? Journal of Experimental Psychology, 19(6), 1251–1265.Google Scholar
  28. Kleberg, J. L., Thorup, E., & Falck-Ytter, T. (2017). Reduced visual disengagement but intact phasic alerting in young children with autism. Autism Research, 10(3), 539–545.Google Scholar
  29. Landry, O., & Parker, A. (2013). A meta-analysis of visual orienting in autism. Frontiers in Human Neuroscience, 7, 833.Google Scholar
  30. 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.Google Scholar
  31. Lord, C., Rutter, M., DiLavore, P. C., Risi, S., Gotham, K., & Bishop, S. (2012). Autism diagnostic obervation schedule (2nd ed.). Torrance: Western Psychological Services.Google Scholar
  32. 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.Google Scholar
  33. Nadig, A. S., Ozonoff, S., Young, G. S., Rozga, A., Sigman, M., & Rogers, S. J. (2007). A prospective study of response to name in infants at risk for autism. Archives of Pediatrics and Adolescent Medicine, 161(4), 378–383.Google Scholar
  34. Nieuwenhuis, S., Aston-Jones, G., & Cohen, J. D. (2005). Decision making, the P3, and the locus coeruleus-norepinephrine system. Psychological Bulletin, 131(4), 510–532.Google Scholar
  35. O’Connor, K. (2012). Auditory processing in autism spectrum disorder: A review. Neuroscience and Biobehavioral Reviews, 36(2), 836–854.Google Scholar
  36. Orekhova, E. V., & Stroganova, T. A. (2014). Arousal and attention re-orienting in autism spectrum disorders: Evidence from auditory event-related potentials. Frontiers in Human Neuroscience, 8, 34.Google Scholar
  37. Osterling, J., & Dawson, G. (1994). Early recognition of children with autism: a study of first birthday home videotapes. Journal of Autism and Developmental Disorders, 24(3), 247–257.Google Scholar
  38. Osterling, J., Dawson, G., & Munson, J. A. (2002). Early recognition of 1-year-old infants with autism spectrum disorder versus mental retardation. Development and Psychopathology, 14(2), 239–251.Google Scholar
  39. Posner, M. I., Walker, J. A., Friedrich, F. J., & Rafal, R. D. (1984). Effects of parietal injury on covert orienting of attention. Journal of Neuroscience, 4(7), 1863–1874.Google Scholar
  40. Robic, S., Sonie, S., Fonlupt, P., Henaff, M. A., Touil, N., Coricelli, G., et al. (2015). Decision-making in a changing world: A study in autism spectrum disorders. Journal of Autism and Developmental Disorders, 45(6), 1603–1613.Google Scholar
  41. Ronconi, L., Devita, M., Molteni, M., Gori, S., & Facoetti, A. (2018). Brief report: When large becomes slow: Zooming-out visual attention is associated to orienting deficits in autism. Journal of Autism and Developmental Disorders, 48(7), 2577–2584.Google Scholar
  42. 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.Google Scholar
  43. Rothbart, M. K., Posner, M. I., & Rosicky, J. (1994). Orienting in normal and pathological development. Development and Psychopathology, 6(4), 635–652.Google Scholar
  44. Rutter, M., Bailey, A., & Lord, C. (2003). Social Communication Questionnaire (SCQ). Los Angeles: Western Psychological Services.Google Scholar
  45. Sabatos-DeVito, M., Schipul, S. E., Bulluck, J. C., Belger, A., & Baranek, G. T. (2016). Eye tracking reveals impaired attentional disengagement associated with sensory response patterns in children with autism. Journal of Autism and Developmental Disorders, 46(4), 1319–1333.Google Scholar
  46. Sacrey, L. A., 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.Google Scholar
  47. Sacrey, L. A., Bryson, S. E., & Zwaigenbaum, L. (2013). Prospective examination of visual attention during play in infants at high-risk for autism spectrum disorder: A longitudinal study from 6 to 36 months of age. Behavioural Brain Research, 256, 441–450.Google Scholar
  48. Salley, B., Sheinkopf, S. J., Neal-Beevers, A. R., Tenenbaum, E. J., Miller-Loncar, C. L., Tronick, E., et al. (2016). Infants’ early visual attention and social engagement as developmental precursors to joint attention. Developmental Psychology, 52(11), 1721–1731.Google Scholar
  49. Saslow, M. G. (1967). Effects of components of displacement-step stimuli upon latency for saccadic eye movement. Journal of the Optical Society of America, 57(8), 1024–1029.Google Scholar
  50. Schmitt, L. M., Cook, E. H., Sweeney, J. A., & Mosconi, M. W. (2014). Saccadic eye movement abnormalities in autism spectrum disorder indicate dysfunctions in cerebellum and brainstem. Molecular Autism, 5(1), 47.Google Scholar
  51. Shafiq, R., Stuart, G. W., Sandbach, J., Maruff, P., & Currie, J. (1998). The gap effect and express saccades in the auditory modality. Experimental Brain Research, 118(2), 221–229.Google Scholar
  52. Stroganova, T. A., Kozunov, V. V., Posikera, I. N., Galuta, I. A., Gratchev, V. V., & Orekhova, E. V. (2013). Abnormal pre-attentive arousal in young children with autism spectrum disorder contributes to their atypical auditory behavior: An ERP study. PLoS ONE, 8(7), e69100.Google Scholar
  53. Sturm, W., & Willmes, K. (2001). On the functional neuroanatomy of intrinsic and phasic alertness. Neuroimage, 14(1 Pt 2), S76–84.Google Scholar
  54. Taylor, T. L., Kingstone, A., & Klein, R. M. (1998). The disapperance of foveal and nonfoveal stimuli: Decomposing the gap effect. Canadian Journal of Experimental Psychology, 52(4), 192–199.Google Scholar
  55. Taylor, T. L., Klein, R. M., & Munoz, D. P. (1999). Saccadic performance as a function of the presence and disappearance of auditory and visual fixation stimuli. Journal of Cognitive Neuroscience, 11(2), 206–213.Google Scholar
  56. Van de Cruys, S., Evers, K., Van der Hallen, R., Van Eylen, L., Boets, B., de-Wit, L., et al. (2014). Precise minds in uncertain worlds: Predictive coding in autism. Psychological Review, 121(4), 649–675.Google Scholar
  57. van der Geest, J. N., Kemner, C., Camfferman, G., Verbaten, M. N., & van Engeland, H. (2001). Eye movements, visual attention, and autism: a saccadic reaction time study using the gap and overlap paradigm. Biological Psychiatry, 50(8), 614–619.Google Scholar
  58. Wechsler, D. (2011). Wechsler’s Abbreviated Scale of Intelligence—second edition (WASI-II). San Antonio: NCS Pearson.Google Scholar
  59. Werner, E., Dawson, G., Osterling, J., & Dinno, N. (2000). Brief report: Recognition of autism spectrum disorder before one year of age: A retrospective study based on home videotapes. Journal of Autism and Developmental Disorders, 30(2), 157–162.Google Scholar
  60. Wilson, C. E., & Saldana, D. (2018). No evidence of atypical attentional disengagement in autism: A study across the spectrum. Autism, 23(3), 677–688.Google Scholar
  61. Yu, A. J., & Dayan, P. (2005). Uncertainty, neuromodulation, and attention. Neuron, 46(4), 681–692.Google Scholar
  62. Zalla, T., Seassau, M., Cazalis, F., Gras, D., & Leboyer, M. (2018). Saccadic eye movements in adults with high-functioning autism spectrum disorder. Autism, 22(2), 195–204.Google Scholar
  63. Zambarbieri, D. (2002). The latency of saccades toward auditory targets in humans. Progress in Brain Research, 140, 51–59.Google Scholar
  64. Zwaigenbaum, L., Bryson, S., Rogers, T., Roberts, W., Brian, J., & Szatmari, P. (2005). Behavioral manifestations of autism in the first year of life. International Journal of Developmental Neuroscience, 23(2–3), 143–152.Google Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Speech, Language, and Hearing SciencesPurdue UniversityWest LafayetteUSA
  2. 2.Department of Psychological SciencesPurdue UniversityWest LafayetteUSA
  3. 3.Department of PediatricsIndiana University School of MedicineIndianapolisUSA

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