Journal of Autism and Developmental Disorders

, Volume 46, Issue 4, pp 1477–1489 | Cite as

Brief Report: Reduced Temporal-Central EEG Alpha Coherence During Joint Attention Perception in Adolescents with Autism Spectrum Disorder

  • Mark Jaime
  • Camilla M. McMahon
  • Bridget C. Davidson
  • Lisa C. Newell
  • Peter C. Mundy
  • Heather A. Henderson
Brief Report


Although prior studies have demonstrated reduced resting state EEG coherence in adults with autism spectrum disorder (ASD), no studies have explored the nature of EEG coherence during joint attention. We examined the EEG coherence of the joint attention network in adolescents with and without ASD during congruent and incongruent joint attention perception and an eyes-open resting condition. Across conditions, adolescents with ASD showed reduced right hemisphere temporal–central alpha coherence compared to typically developing adolescents. Greater right temporal–central alpha coherence during joint attention was positively associated with social cognitive performance in typical development but not in ASD. These results suggest that, in addition to a resting state, EEG coherence during joint attention perception is reduced in ASD.


EEG coherence Joint attention Brain connectivity Cortical connectivity Joint attention network connectivity Neurocognitive features of joint attention in ASD Adolescents with ASD Adolescent autistic brain 



We would like to acknowledge and thank Justin H. G. Williams for providing us with the video stimulus used in this study, Mark E. Pflieger of Source Signal Imaging for consultation on analyses, and the National Institutes of Health (Grant R01 NIMH 071273; Mundy and Henderson co-PIs) for their support. A version of this study was presented at the International Meeting for Autism Research in 2010.


This study was funded by NIMH Grant RO1 MH071273.

Authors Contribution

MJ was responsible for the final design the study, led the execution of the study, performed the statistical and EEG analyses, and drafted the manuscript; CM participated in the coordination of the study and helped to draft the manuscript; BD participated in the coordination of the study and helped to draft the manuscript; LN participated in the initial design of the study and helped to draft the manuscript; PM conceived the study, participated in the initial design of the study, and helped to draft the manuscript; HH participated in the interpretation of the data and helped to draft the manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

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 and assent was obtained from all individual participants included in the study.


  1. Adolphs, R. (2009). The social brain: The neural basis of social knowledge. Annual Reviews of Psychology, 60, 693–716.CrossRefGoogle Scholar
  2. Assaf, M., Jagannathan, K., Calhoun, V. D., Miller, L., Stevens, M. C., Sahl, R., et al. (2010). Abnormal functional connectivity of default mode sub-networks in autism spectrum disorder patients. NeuroImage, 53, 247–256.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Baron-Cohen, S., Ring, H. A., Wheelwright, S., Bullmore, E. T., Brammer, M. J., Simmons, A., & Willimans, S. C. R. (1999). Social intelligence in the normal and autistic brain: An fMRI study. European Journal of Neuroscience, 11, 1891–1898.CrossRefPubMedGoogle Scholar
  4. Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., & Plumb, I. (2001). The “Reading the Mind in the Eyes” test revised version: A study with normal adults, and adults with Asperger Syndrome or high functioning autism. Journal of Child Psychology and Psychiatry, 42, 241–251.CrossRefPubMedGoogle Scholar
  5. Belmonte, M. K., Allen, G., Beckel-Mitchener, A., Boulanger, L. M., Carper, R. A., & Webb, S. J. (2004). Autism and abnormal development of brain connectivity. Journal of Neuroscience, 24, 9228–9231.CrossRefPubMedGoogle Scholar
  6. Berument, S., Rutter, M., Lord, C., Pickles, A., & Bailey, A. (1999). Autism screening questionnaire: Diagnostic validity. British Journal of Psychiatry, 175, 444–451.CrossRefPubMedGoogle Scholar
  7. Boddaert, N., Chabane, N., Gervais, H., Good, C. D., Bourgeois, M., Plumet, M.-H., et al. (2004). Superior temporal sulcus anatomical abnormalities in childhood autism: A voxel-based morphometry MRI study. NeuroImage, 23, 364–369.CrossRefPubMedGoogle Scholar
  8. Bonnelle, V., Leech, R., Kinnunen, K. M., Ham, T. E., Beckmann, C. F., Boissezon, De, et al. (2011). Default mode network connectivity predicts sustained attention deficits after traumatic brain injury. Journal of Cognitive Neuroscience, 31, 13442–13451.Google Scholar
  9. Castelli, F., Happé, F., Frith, U., & Frith, C. (2000). Movement and mind: A functional imaging study of perception and interpretation of complex intentional movement patterns. Neuroimage, 12, 314–325.CrossRefPubMedGoogle Scholar
  10. Cherkassky, V. L., Kana, R. K., Keller, T. A., & Just, M. A. (2006). Functional connectivity in a baseline resting-state network in autism. Brain Imaging, 17, 1687–1690.Google Scholar
  11. Coben, R., Clarke, A. R., Hudspeth, W., & Barry, R. J. (2008). EEG power and coherence in autistic spectrum disorder. Clinical Neurophysiology, 119, 1002–1009.CrossRefPubMedGoogle Scholar
  12. Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3, 201–215.CrossRefPubMedGoogle Scholar
  13. Courchesne, E., & Pierce, K. (2005a). Brain overgrowth in autism during a critical time in development: Implications for frontal pyramidal neuron and interneuron development and connectivity. International Journal of Developmental Neuroscience, 23, 153–173.CrossRefPubMedGoogle Scholar
  14. Courchesne, E., & Pierce, K. (2005b). Why the frontal cortex in autism might be talking only to itself: Local over-connectivity but long-distance disconnection. Current Opinion in Neurobiology, 15, 225–230.CrossRefPubMedGoogle Scholar
  15. Croft, R. J., & Barry, R. J. (2000). Removal of ocular artifact from the EEG: A review. Clinical Neurophysiology, 30, 5–19.CrossRefPubMedGoogle Scholar
  16. Dalton, K., Nacewicz, T., 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, 519–526.PubMedPubMedCentralGoogle Scholar
  17. Darmala, S. R., Keller, T. A., Kana, R. K., Cherkassky, V. L., Williams, D. L., Minshew, N. J., & Just, M. A. (2010). Cortical underconnectivity coupled with preserved visuospatial cognition in autism: Evidence from an fMRI study of an embedded figures task. Autism Research, 3, 273–279.CrossRefGoogle Scholar
  18. Ehrsson, H. H., Holmes, N. P., & Passingham, R. E. (2005). Touching a rubber hand: feeling of body ownership is associated with activity in multisensory brain areas. Journal of Neuroscience, 25, 10564–10573.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., & Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences, 102, 9673–9678.CrossRefGoogle Scholar
  20. Gallagher, H. L., & Frith, C. D. (2003). Functional imaging of ‘theory of mind’. Trends in Cognitive Sciences, 7, 77–83.CrossRefPubMedGoogle Scholar
  21. Grelotti, D., Klin, A. J., Gauthier, I. J., Skudlarski, P., Cohen, D., Gore, J. C., et al. (2005). fMRI activation of the fusiform gyrus and amygdale to cartoon characters but not to faces in a boy with autism. Neuropsychologia, 43, 373–385.CrossRefPubMedGoogle Scholar
  22. Haist, F., Adamo, M., Westerfield, M., Courchesne, E., & Townsend, J. (2005). The functional neuroanatomy of spatial attention in autism spectrum disorder. Developmental Neuropsychology, 27, 425–458.CrossRefPubMedGoogle Scholar
  23. Hoffman, E. A., & Haxby, J. V. (2000). Distinct representations of eye gaze and identity in the distributed human neural system for face perception. Nature Neuroscience, 3, 80–84.CrossRefPubMedGoogle Scholar
  24. Homan, R. W., Herman, J., & Purdy, P. (1987). Cerebral location of international 10–20 system electrode placement. Electroencephalography and Clinical Neuropsychology, 66, 376–382.CrossRefGoogle Scholar
  25. Jasper, H. H. (1958). The ten-twenty electrode system of the international federation. Electroencephalography and Clinical Neurophysiology, 10, 371–375.Google Scholar
  26. Jones, T., Bandettini, P. A., Kenworthy, L., Case, L. K., Milleville, S. C., Martin, A., & Birn, R. M. (2010). Sources of group differences in functional connectivity: An investigation applied to autism spectrum disorder. NeuroImage, 49, 401–414.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Just, M. A., Cherkassky, V. L., Keller, T., & Minshew, N. J. (2004). Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain, 127, 1811–1821.CrossRefPubMedGoogle Scholar
  28. Just, M. A., Cherkassky, V. L., Keller, T., Rajesh, K. K., & Minshew, N. J. (2007). Functional and anatomical cortical underconnectivity in autism: Evidence from an FMRI study of an executive function task and corpus callosum morphometry. Cerebral Cortex, 17, 951–961.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kana, R. K., Keller, T. A., Cherskassky, V. L., Minshew, N. J., & Just, M. A. (2006). Sentence comprehension in autism: Thinking in pictures with decreased functional connectivity. Brain, 129, 2484–2493.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kana, R. K., Uddin, L. Q., Kenet, T., Chugani, D., & Müller, R.-A. (2014). Brain connectivity in autism. Frontiers in Human Neuroscience, 8, 349.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kitzbichler, M. G., Khan, S., Ganesan, S., Vangel, M. G., Herbert, M. R., Hamalainen, M. S., & Kenet, T. (in press). Altered development and multifaceted band-specific abnormalities of resting state networks in autism. Biological Psychiatry.Google Scholar
  32. Koshino, H., Carpenter, P. A., Minshew, N. J., Cherkassky, V. L., Keller, T. A., & Just, M. A. (2005). Functional connectivity in an fMRI working memory task in high functioning autism. Neuroimage, 24, 810–821.CrossRefPubMedGoogle Scholar
  33. Koshino, H., Kana, R. K., Keller, T. A., Cherkassky, V. L., Minshew, N. J., & Just, M. A. (2008). fMRI investigation of working memory for faces in autism: Visual coding and underconnectivity with frontal areas. Cerebral Cortex, 18, 289–300.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kylliainen, A., & Hietanen, J. K. (2004). Attention orienting by another’s gaze direction in children with autism. Journal of Child Psychology and Psychiatry, 45, 435–444.CrossRefPubMedGoogle Scholar
  35. Lazarev, V. V., Pontes, A., Mitrofanov, A. A., & deAzevedo, L. C. (2013). Reduced interhemispheric connectivity in childhood autism detected by electroencephalographic photic driving coherence. Journal of Autism and Developmental Disorders,. doi: 10.1007/s10803-013-1959-8.Google Scholar
  36. Levitt, J. G., Blanton, R. E., Smalley, S., Thompson, P. M., Guthrie, D., McCracken, J. T., et al. (2003). Cortical sulcal maps in autism. Cerebral Cortex, 13, 728–735.CrossRefPubMedGoogle Scholar
  37. Lewis, J. D., & Elman, J. L. (2008). Growth-related neural reorganization and the autism phenotype: A test of the hypothesis that altered brain growth leads to altered connectivity. Developmental Science, 11, 135–155.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lombardo, M. V., Chakrabarti, B., Bullmore, E. T., Sadek, S., Pasco, G., et al. (2010). Atypical neural self-representation in autism. Brain, 133, 611–624.CrossRefPubMedGoogle Scholar
  39. Lord, C., Lambrecht, L., Cook, E., Leventhal, B., DiLavore, P., et al. (2000). The Autism diagnostic observation schedule—generic: A standard measure of social communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30, 205–223.CrossRefPubMedGoogle Scholar
  40. Lynch, C. J., Uddin, L. Q., Supekar, K., Khouzam, A., Phillips, J., & Menon, V. (2013). Default mode network in childhood autism: Posteromedial cortex heterogeneity and relationship with social deficits. Biological Psychiatry, 74, 212–219.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Mathewson, K. J., Jetha, M. K., Drmic, I. E., Bryson, S. E., Goldberg, J. O., & Schmidt, L. A. (2012). Regional EEG alpha power, coherence, and behavioral symptomatology in autism spectrum disorder. Clinical Neurophysiology, 123, 1798–1809.CrossRefPubMedGoogle Scholar
  42. Minshew, N. J., & Keller, T. A. (2010). The nature of brain dysfunction in autism: Functional brain imaging studies. Current Opinion in Neurology, 23(2), 124.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Mulholland, T. (1969). (1969). The concept of attention and the electroencephalographic alpha rhythm. In C. R. Evans & T. B. Mulholland (Eds.), Attention in Neurophysiology (pp. 100–127). London: Butterworths.Google Scholar
  44. Mundy, P. (2003). 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, 793–809.CrossRefPubMedGoogle Scholar
  45. Mundy, P. (in press). The human nature of Autism, joint attention and social cognition. New York: Guildford Publications.Google Scholar
  46. Mundy, P., Gwaltney, M., & Henderson, H. (2010). Self-referenced processing, neurodevelopment and joint attention in autism. Autism, 14, 408–429.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Mundy, P., & Jarrold, W. (2010). Infant joint attention, neural networks and social cognition. Neural Networks, 23, 985–997.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Mundy, P., & Newell, L. (2007). Attention, joint attention, and social cognition. Current Directions in Psychological Science, 16, 269–274.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Mundy, P., Sullivan, L., & Mastergeorge, A. M. (2009). A parallel and distributed-processing model of joint attention, social cognition and autism. Autism Research, 2, 2–21.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Murias, M., Webb, S. J., Greenson, J., & Dawson, G. (2007). Resting state cortical connectivity reflected in EEG coherence in individuals with autism. Biological Psychiatry, 62, 270–273.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Noonan, S. K., Haist, F., & Müller, R.-A. (2009). Aberrant functional connectivity in autism: Evidence from low-frequency BOLD signal fluctuations. Brain Research, 1262, 48–63.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Nunez, P. L., & Srinivasan, R. (2006). Electric fields of the brain: The neurophysics of EEG. New York, NY: Oxford University Press.CrossRefGoogle Scholar
  53. Ogawa, T., Sugiyama, A., Ishiwa, S., Suzuki, M., Ishihara, T., & Sato, K. (1982). Ontogenetic development of EEG-asymmertry in early infantile autism. Brain & Development, 4, 439–449.CrossRefGoogle Scholar
  54. Pelphrey, K. A., Morris, J. P., & McCarthy, G. (2005). Neural basis of eye gaze processing in autism. Brain, 128, 1038–1048.CrossRefPubMedGoogle Scholar
  55. Pelphrey, K. A., Singerman, J. D., Allison, T., & McCarthy, G. (2003). Brain activation evoked by perception of gaze shifts: The influence of context. Neuropsychologia, 41, 156–170.CrossRefPubMedGoogle Scholar
  56. Posner, M. I., & Peterson, S. E. (1990). The attention system of the human brain. Annual Review of Neuroscience, 13, 25–42.CrossRefPubMedGoogle Scholar
  57. Pruett, J., LaMacchia, A., Hoertel, S., Squire, E., McVey, K., Todd, R. D., et al. (2011). Social and non-social cueing of visuospatial attention in autism and typical development. Journal of Autism and Developmental Disorders, 41, 715–731.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Quartz, S. R. (1999). The constructivist brain. Trends in Cognitive Science, 3, 48–57.CrossRefGoogle Scholar
  59. Radovanovic, S., Korotkov, A., Ljubisavljevic, M., Lyskov, E., Thunberg, J., Kataeva, G., et al. (2002). Comparison of brain activity during different types of proprioceptive inputs: A positron emission tomography study. Experimental Brain Research, 143, 276–285.CrossRefPubMedGoogle Scholar
  60. Ray, W. J., & Cole, H. W. (1985). EEG alpha activity reflects attentional demands, and beta activity reflects emotional and cognitive processes. Science, 228, 750–752.CrossRefPubMedGoogle Scholar
  61. Redcay, E., Dodell-Feder, D., Mavros, P. L., Kleiner, M., Pearrow, M. J., Triantafyllou, C., et al. (2013). Atypical brain activation patterns during a face-to-face joint attention game in adults with Autism Spectrum Disorder. Human Brain Mapping, 34, 2511–2523.CrossRefPubMedGoogle Scholar
  62. Saxe, R. (2006). Uniquely human social cognition. Current Opinion in Neurobiology, 2, 235–239.CrossRefGoogle Scholar
  63. 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, 445–458.CrossRefPubMedGoogle Scholar
  64. Shih, P., Shen, M., Ottl, B., Keehn, B., Gaffrey, M. S., & Muller, R. A. (2010). Atypical network connectivity for imitation in autism spectrum disorder. Neuropsychologia, 48, 2931–2939.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Swanson, M. R., Serlin, G. C., & Siller, M. (2013). Broad autism phenotype in typically developing children predicts performance on an eye-tracking measure of joint attention. Journal of Autism and Developmental Disorders, 43, 707–718.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 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, 325–334.CrossRefPubMedPubMedCentralGoogle Scholar
  67. Thatcher, R., Krause, P., & Hrybyk, M. (1986). Cortico-cortical associations and EEG coherence: A two-compartmental model. Electroencephalography and Clinical Neurophysiology, 64, 123–143.CrossRefPubMedGoogle Scholar
  68. Uddin, L. Q., Supekar, K., Lynch, C. J., Khouzam, A., Phillips, J., et al. (2013a). Salience network-based classification and prediction of symptom severity in children with autism. JAMA Psychiatry, 70, 869–879.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Uddin, L. Q., Supekar, K., & Menon, V. (2013b). Reconceptualizing functional brain connectivity in autism from a developmental perspective. Frontiers in Human Neuroscience, 7, 458.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Villalobos, M. E., Mizuno, A., Dahl, B. C., Kemmotsu, N., & Muller, R. A. (2005). Reduced functional connectivity between V1 and inferior frontal cortex associated with visuomotor performance in autism. NeuroImage, 25, 916–925.CrossRefPubMedPubMedCentralGoogle Scholar
  71. Wicker, B., Fonlupt, P., Hubert, B., Tardif, C., Gepner, B., & Deruelle, C. (2008). Abnormal cerebral effective connectivity during explicit emotional processing in adults with autism spectrum disorder. Social Cognitive and Affective Neuroscience, 3, 135–143.CrossRefPubMedPubMedCentralGoogle Scholar
  72. Williams, J. H. G., Waiter, G. D., Perra, O., Perrett, D. I., & Whiten, A. (2005). An fMRI study of joint attention experience. NeuroImage, 25, 133–140.CrossRefPubMedGoogle Scholar
  73. Williams, P., Weiss, L., & Rolfhus, E. (2003). Wechsler intelligence scale for children–IV, technical report 1, theoretical model & test blueprint. San Antonio, TX: The Psychological Corporation.Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Mark Jaime
    • 1
    • 7
  • Camilla M. McMahon
    • 2
    • 7
  • Bridget C. Davidson
    • 3
    • 7
  • Lisa C. Newell
    • 4
    • 7
  • Peter C. Mundy
    • 5
    • 7
  • Heather A. Henderson
    • 6
    • 7
  1. 1.Division of ScienceIndiana University-Purdue University ColumbusColumbusUSA
  2. 2.Psychology DepartmentHamilton CollegeClintonUSA
  3. 3.Department of PsychologyUniversity of Texas – AustinAustinUSA
  4. 4.Department of PsychologyIndiana University of PennsylvaniaIndianaUSA
  5. 5.MIND InstituteUniversity of California – DavisSacramentoUSA
  6. 6.Department of PsychologyUniversity of WaterlooWaterlooCanada
  7. 7.Department of PsychologyUniversity of MiamiCoral GablesUSA

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