Neural basis of attention orienting abnormalities in children with autism

1601

Abstract

Detection of new events occurring outside the focus of attention is fundamental to adaptive functioning and is most critical when attention is focused elsewhere. The unattended novel sensory events may demand further analysis according to their task relevance and may appear important for survival. Behavioral and physiological findings reviewed in this article imply that brains of many people with autism spectrum disorders (ASD) are, to a certain extent, impenetrable to such unattended but potentially salient changes in the immediate sensory environment. Here we reviewed neurophysiological studies investigating neural processing of salient (rare, novel or deviant) auditory stimuli in ASD. We put forward a hypothesis that atypical processing of deviance and novelty in a proportion of individuals with ASD may be grounded in the failure of nicotinic cholinergic arousal pathways to engage cortical mechanisms involved in detection of changes in the environment and appraisal of their novelty, if these changes occur beyond the currently attended sensory stream. Further studies linking neurophysiological findings with attention behavior and those searching for their neurochemical and genetic bases will help to understand causes of attention problems and sensory modulation difficulties in children with ASD and may prove helpful to direct early intervention

General Information

Journal rubric: Clinical Psychology

Article type: scientific article

DOI: https://doi.org/10.17759/exppsy.2015080302

For citation: Stroganova T.A., Orekhova E.V., Galuta I.A. Neural basis of attention orienting abnormalities in children with autism. Eksperimental'naâ psihologiâ = Experimental Psychology (Russia), 2015. Vol. 8, no. 3, pp. 7–23. DOI: 10.17759/exppsy.2015080302. (In Russ., аbstr. in Engl.)

References

  1. Stroganova T.A., Orekhova E.V., Galuta I.A. Monotropizm vnimaniya u detey s autizmom [Monotropism of attention in children with autism], Eksperimentalnaya psikhologiya [Experimental Psychology (Russia)], 2014, vol. 7, no. 4, pp. 66–82 (In Russian; abstract in English).
  2. Ames C., Fletcher-Watson S. A review of methods in the study of attention in autism. Developmental Review, 2010, vol. 30, no. 1, pp. 52–73.
  3. Anand R., Amici S.A., Ponath G., Robson J.I., Nasir M., McKay S.B. Nicotinic acetylcholine receptor alterations in autism spectrum disorders – biomarkers and therapeutic targets. In Eapen V. (ed.), Autism - A Neurodevelopmental Journey from Genes to Behaviour, InTech, 2011, pp. 123–146.
  4. Andersson S., Posserud M.B., Lundervold A.J. Early and late auditory event-related potentials in cognitively high functioning male adolescents with autism spectrum disorder. Research in Autism Spectrum Disorders, 2013, vol. 7, no. 7, pp. 815–823.
  5. Bryson S.E., Wainwright-Sharp J.A., Smith I.M. Autism: A developmental spatial neglect syndrome? In James T.E. (ed.), Advances in Psychology. North-Holland, 1990, pp. 405–427.
  6. Buckley A.W., Rodriguez A.J., Jennison K., Buckley J., Thurm A., Sato S., Swedo S. Rapid eye movement sleep percentage in children with autism compared with children with developmental delay and typical development. Archives of Pediatrics and Adolescent Medicine, 2010, vol. 164, no. 11, pp. 1032–1037. doi: 10.1001/archpediatrics.2010.202.
  7. Casey B.J., Gordon C.T., Mannheim G.B., Rumsey J.M. Dysfunctional attention in autistic savants. Journal of Clinical and Experimental Neuropsychology, 1993, vol. 15, no. 6, pp. 933–946. doi: 10.1080/01688639308402609
  8. Chang W.P., Arfken C.L., Sangal M.P., Boutros N.N. Probing the relative contribution of the first and second responses to sensory gating indices: a meta-analysis. Psychophysiology, 2011, vol. 48, no. 7, pp. 980– 992. doi: 10.1111/j.1469-8986.2010.01168.x
  9. Corbetta M., Shulman G.L. Spatial neglect and attention networks. Annual Review of Neuroscience,
  10. 2011, vol. 34, pp. 569–599. doi: 10.1146/annurev-neuro-061010–113731
  11. Dunn M.A., Gomes H., Gravel J. Mismatch negativity in children with autism and typical development.
  12. Journal of Autism and Developmental Disorders, 2008, vol. 38, no. 1, pp. 52–71. doi: 10.1007/s10803-007-0359-3
  13. Gomot M., Blanc R., Clery H., Roux S., Barthelemy C., Bruneau N. Candidate electrophysiological endophenotypes of hyper-reactivity to change in autism. Journal of Autism and Developmental Disorders, 2011, vol. 41, no. 6, pp. 705–714. doi: 10.1007/s10803-010-1091-y
  14. Greenwood P.M., Parasuraman R., Espeseth T. A cognitive phenotype for a polymorphism in the nicoti- nic receptor gene CHRNA4. Neuroscience & Biobehavioral Reviews, 2012, vol. 36, no. 4, pp. 1331–1341. doi: 10.1016/j.neubiorev.2012.02.010
  15. Impey D., Chique-Alfonzo M., Shah D., Fisher D.J., Knott V.J. Effects of nicotine on visuospatial attentional orienting in non-smokers. Pharmacology Biochemistry and Behavior, 2013, vol. 106, pp. 1–7. doi: 10.1016/j.pbb.2013.02.015
  16. Karvat G., Kimchi T. Acetylcholine elevation relieves cognitive rigidity and social deficiency in a mouse model of autism. Neuropsychopharmacology, 2014, vol. 39, no. 4, pp. 831–840. doi: 10.1038/npp.2013.274
  17. Kawakubo Y., Kasai K., Okazaki S., Hosokawa-Kakurai M., Watanabe K., Kuwabara H., Ishijima M., Yamasue H., Iwanami A., Kato N., Maekawa H. Electrophysiological abnormalities of spatial attention in adults with autism during the gap overlap task. Clinical Neurophysiology, 2007, vol. 118, no. 7, pp. 1464– 1471. doi: 10.1016/j.clinph.2007.04.015
  18. Kemner C., Verbaten M.N., Cuperus J.M., Camfferman G., van Engeland H. Auditory event-related brain potentials in autistic children and three different control groups. Biological Psychiatry, 1995, vol. 38, no. 3, pp. 150–165. doi: 10.1016/0006-3223(94)00247-z
  19. Kuhl P.K., Coffey-Corina S., Padden D., Dawson G. Links between social and linguistic processing of speech in preschool children with autism: behavioral and electrophysiological measures. Developmental Science, 2005, vol. 8, no. 1, pp. F1–F12. doi: 10.1111/j.1467-7687.2004.00384.x
  20. Kujala T., Kuuluvainen S., Saalasti S., Jansson-Verkasalo E., von Wendt L., Lepisto T. Speech-feature discrimination in children with Asperger syndrome as determined with the multi-feature mismatch negativity paradigm. Clinical Neurophysiology, 2010, vol. 121, no. 9, pp. 1410–1419. doi: 10.1016/j.clinph.2010.03.017
  21. Lemonnier E., Grandgeorge M., Jacobzone-Leveque C., Bessaguet C., Peudenier S., Misery L. Red der- mographism in autism spectrum disorders: A clinical sign of cholinergic dysfunction? Research in Autism Spectrum Disorders, 2013, vol. 7, no. 5, pp. 601–605.
  22. Lepisto T., Nieminen-von Wendt T., von Wendt L., Naatanen R., Kujala T. Auditory cortical change detection in adults with Asperger syndrome. Neuroscience Letters, 2007, vol. 414, no. 2, pp. 136–140. doi:
  23. 10.1016/j.neulet.2006.12.009
  24. Lindell A.K., Hudry K. Atypicalities in cortical structure, handedness, and functional lateralization for language in autism spectrum disorders. Neuropsychology Review, 2013, vol. 23, no. 3, pp. 257–270. doi: 10.1007/s11065-013-9234-5
  25. Martin-Ruiz C.M., Lee M., Perry R.H., Baumann M., Court J.A., Perry E.K. Molecular analysis of nicotinic receptor expression in autism. Molecular Brain Research, 2004, vol. 123, no. 1–2, pp. 81–90. doi: 10.1016/j.molbrainres.2004.01.003
  26. May P.J., Tiitinen H. Mismatch negativity (MMN), the deviance-elicited auditory deflection, explained.
  27. Psychophysiology, 2010, vol. 47, no. 1, pp. 66–122. doi: 10.1111/j.1469-8986.2009.00856.x
  28. Mesulam M.M. Cholinergic pathways and the ascending reticular activating system of the human brain.
  29. Annals of the New York Academy of Sciences, 1995, vol. 757, pp. 169–179.
  30. Naatanen R., Paavilainen P., Rinne T., Alho K. The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clinical Neurophysiology, 2007, vol. 118, no. 12, pp. 2544–2590. doi: 10.1016/j.clinph.2007.04.026
  31. Orekhova E.V., Stroganova T.A., Prokofyev A.O., Nygren G., Gillberg C., Elam M. Sensory gating in young children with autism: relation to age, IQ, and EEG gamma oscillations. Neuroscience Letters, 2008, vol. 434, no. 2, pp. 218–223. doi: 10.1016/j.neulet.2008.01.066
  32. Orekhova E.V., Tsetlin M.M., Butorina A.V., Novikova S.I., Gratchev V.V., Sokolov P.A., Elam M., Stroganova T.A. Auditory cortex responses to clicks and sensory modulation difficulties in children with autism spectrum disorders (ASD). PLoS One, 2012, vol. 7, no. 6, pp. e39906. doi: 10.1371/journal. pone.0039906
  33. Ponton C., Eggermont J.J., Khosla D., Kwong B., Don M. Maturation of human central auditory system activity: separating auditory evoked potentials by dipole source modeling. Clinical Neurophysiology, 2002, vol. 113, no. 3, pp. 407–420.
  34. Sarter M., Hasselmo M.E., Bruno J.P., Givens B. Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain Research Reviews, 2005, vol. 48, no. 1, pp. 98–111. doi: 10.1016/j.brainresrev.2004.08.006
  35. Skinner R.D., Homma Y., Garcia-Rill E. Arousal mechanisms related to posture and locomotion:
  36. Ascending modulation. Progress in Brain Research, 2004, vol. 143, pp. 291–298. doi: 10.1016/s0079- 6123(03)43028-8
  37. Stroganova T.A., Kozunov V.V., Posikera I.N., Galuta I.A., Gratchev V.V., Orekhova E.V. Abnormal pre- attentive arousal in young children with autism spectrum disorder contributes to their atypical auditory behavior: an ERP study. PLoS One, 2013, vol. 8, no. 7, pp. e69100. doi: 10.1371/journal.pone.0069100
  38. Tarkka I.M., Luukkainen-Markkula R., Pitkanen K., Hamalainen H. Alterations in visual and audi- tory processing in hemispatial neglect: an evoked potential follow-up study. International Journal of Psychophysiology, 2011, vol. 79, no. 2, pp. 272–279. doi: 10.1016/j.ijpsycho.2010.11.002
  39. Thiel C.M., Fink G.R. Visual and auditory alertness: modality-specific and supramodal neural mechanisms and their modulation by nicotine. Journal of Neurophysiology, 2007, vol. 97, no. 4, pp. 2758– 2768. doi: 10.1152/jn.00017.2007
  40. Tsetlin M.M., Pushina N.P., Galuta I.A., Stroganova T.A. Spatial asymmetry of frontal tasks performance in young boys with autism. International Journal of Psychophysiology, 2008, vol. 69, pp. 267–267. doi: 10.1016/j.ijpsycho.2008.05.211
  41. Vossel S., Kukolja J., Thimm M., Thiel C.M., Fink G.R. The effect of nicotine on visuospatial attention in chronic spatial neglect depends upon lesion location. Journal of Psychopharmacology, 2010, vol. 24, no. 9, pp. 1357–1365. doi: 10.1177/0269881109105397
  42. Whitehouse A.J., Bishop D.V. Do children with autism ‘switch off’ to speech sounds? An investigation using event-related potentials. Developmental Science, 2008, vol. 11, no. 4, pp. 516–524. doi: 10.1111/j.1467– 7687.2008.00697.x
  43. Witte E.A., Davidson M.C., Marrocco R.T. Effects of altering brain cholinergic activity on covert orienting of attention: comparison of monkey and human performance. Psychopharmacology (Berl), 1997, vol. 132, no. 4, pp. 324–334.
  44. Yvert B., Crouzeix A., Bertrand O., Seither-Preisler A., Pantev C. Multiple supratemporal sources of magnetic and electric auditory evoked middle latency components in humans. Cerebral Cortex, 2001, vol. 11, no. 5, pp. 411–423.

Information About the Authors

Tatyana A. Stroganova, Doctor of Biology, Senior Researcher, Centre of Neurocognitive Research (MEG Centre), Moscow State University of Psychology and Education, Moscow, Russia, ORCID: https://orcid.org/0000-0003-3750-9890, e-mail: stroganova56@mail.ru

Elena V. Orekhova, PhD in Psychology, Senior Researcher, Centre of Neurocognitive Research (MEG Centre), Moscow State University of Psychology and Education, Moscow, Russia, ORCID: https://orcid.org/0000-0003-0950-1613, e-mail: orekhova.elena.v@gmail.com

Ilya A. Galuta, Laboratory for Interdisciplinary Autism Research, Moscow State University of Psychology and Education, Moscow, Russia, e-mail: iliagaluta@gmail.com

Metrics

Views

Total: 3052
Previous month: 13
Current month: 14

Downloads

Total: 1601
Previous month: 6
Current month: 5