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

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Abstract

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.

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References

  • Adolphs, R. (2009). The social brain: The neural basis of social knowledge. Annual Reviews of Psychology, 60, 693–716.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Berument, S., Rutter, M., Lord, C., Pickles, A., & Bailey, A. (1999). Autism screening questionnaire: Diagnostic validity. British Journal of Psychiatry, 175, 444–451.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Coben, R., Clarke, A. R., Hudspeth, W., & Barry, R. J. (2008). EEG power and coherence in autistic spectrum disorder. Clinical Neurophysiology, 119, 1002–1009.

    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, 201–215.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Croft, R. J., & Barry, R. J. (2000). Removal of ocular artifact from the EEG: A review. Clinical Neurophysiology, 30, 5–19.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Gallagher, H. L., & Frith, C. D. (2003). Functional imaging of ‘theory of mind’. Trends in Cognitive Sciences, 7, 77–83.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Homan, R. W., Herman, J., & Purdy, P. (1987). Cerebral location of international 10–20 system electrode placement. Electroencephalography and Clinical Neuropsychology, 66, 376–382.

    Article  Google Scholar 

  • Jasper, H. H. (1958). The ten-twenty electrode system of the international federation. Electroencephalography and Clinical Neurophysiology, 10, 371–375.

    Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kana, R. K., Uddin, L. Q., Kenet, T., Chugani, D., & Müller, R.-A. (2014). Brain connectivity in autism. Frontiers in Human Neuroscience, 8, 349.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  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, 435–444.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • Mundy, P. (in press). The human nature of Autism, joint attention and social cognition. New York: Guildford Publications.

  • Mundy, P., Gwaltney, M., & Henderson, H. (2010). Self-referenced processing, neurodevelopment and joint attention in autism. Autism, 14, 408–429.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mundy, P., & Jarrold, W. (2010). Infant joint attention, neural networks and social cognition. Neural Networks, 23, 985–997.

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nunez, P. L., & Srinivasan, R. (2006). Electric fields of the brain: The neurophysics of EEG. New York, NY: Oxford University Press.

    Book  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Pelphrey, K. A., Morris, J. P., & McCarthy, G. (2005). Neural basis of eye gaze processing in autism. Brain, 128, 1038–1048.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Quartz, S. R. (1999). The constructivist brain. Trends in Cognitive Science, 3, 48–57.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Saxe, R. (2006). Uniquely human social cognition. Current Opinion in Neurobiology, 2, 235–239.

    Article  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, 445–458.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  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, 325–334.

    Article  PubMed  PubMed Central  Google Scholar 

  • Thatcher, R., Krause, P., & Hrybyk, M. (1986). Cortico-cortical associations and EEG coherence: A two-compartmental model. Electroencephalography and Clinical Neurophysiology, 64, 123–143.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Uddin, L. Q., Supekar, K., & Menon, V. (2013b). Reconceptualizing functional brain connectivity in autism from a developmental perspective. Frontiers in Human Neuroscience, 7, 458.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

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Acknowledgments

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.

Funding

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.

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Authors and Affiliations

  1. Division of Science, Indiana University-Purdue University Columbus, 4601 Central Avenue, Columbus, IN, 47203, USA

    Mark Jaime

  2. Psychology Department, Hamilton College, 198 College Hill Road, Clinton, NY, 13323, USA

    Camilla M. McMahon

  3. Department of Psychology, University of Texas – Austin, 1 University Station – A8000, Austin, TX, 78712, USA

    Bridget C. Davidson

  4. Department of Psychology, Indiana University of Pennsylvania, 1020 Oakland Avenue, Indiana, PA, 15705, USA

    Lisa C. Newell

  5. MIND Institute, University of California – Davis, 2825 50th Street, Sacramento, CA, 95817, USA

    Peter C. Mundy

  6. Department of Psychology, University of Waterloo, 200 University Ave. W., Waterloo, ON, N2L 3G1, Canada

    Heather A. Henderson

  7. Department of Psychology, University of Miami, Coral Gables, FL, USA

    Mark Jaime, Camilla M. McMahon, Bridget C. Davidson, Lisa C. Newell, Peter C. Mundy & Heather A. Henderson

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  1. Mark Jaime
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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.

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Jaime, M., McMahon, C.M., Davidson, B.C. et al. Brief Report: Reduced Temporal-Central EEG Alpha Coherence During Joint Attention Perception in Adolescents with Autism Spectrum Disorder. J Autism Dev Disord 46, 1477–1489 (2016). https://doi.org/10.1007/s10803-015-2667-3

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