Effects of Low Frequency Repetitive Transcranial Magnetic Stimulation (rTMS) on Gamma Frequency Oscillations and Event-Related Potentials During Processing of Illusory Figures in Autism

Abstract

Previous studies by our group suggest that the neuropathology of autism is characterized by a disturbance of cortical modularity. In this model a decrease in the peripheral neuropil space of affected minicolumns provides for an inhibitory deficit and a readjustment in their signal to noise bias during information processing. In this study we proposed using low frequency transcranial magnetic stimulation (rTMS) as a way increasing the surround inhibition of minicolumns in autism. Thirteen patients (ADOS and ADI-R diagnized) and equal number of controls participated in the study. Repetitive TMS was delivered at 0.5 Hz, 2 times per week for 3 weeks. Outcome measures based on event-related potentials (ERP), induced gamma activity, and behavioral measures showed significant post-TMS improvement. The results suggest that rTMS offers a potential therapeutic intervention for autism.

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References

  1. Alonso, P., Pujol, J., Cardoner, N., Benlloch, L., Deus, J., Menchón, J. M., et al. (2001). Right prefrontal repetitive transcranial magnetic stimulation in obsessive-compulsive disorder: A double-blind, placebo-controlled study. American Journal of Psychiatry, 158, 1143–1145.

    PubMed  Article  Google Scholar 

  2. Aman, M. G. (2004). Management of hyperactivity and other acting-out problems in patients with autism spectrum disorder. Seminars in Pediatric Neurology, 11, 225–228.

    PubMed  Article  Google Scholar 

  3. Aman, M. G., & Singh, N. N. (1994). Aberrant behavior checklist—Community. Supplementary manual. East Aurora, NY: Slosson Educational Publications.

    Google Scholar 

  4. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (DSM-IV TR) (4th ed.). Washington, DC: American Psychiatric Association. (text revised).

    Google Scholar 

  5. Barker, A. T. (1999). The history and basic principles of magnetic nerve stimulation. Electroencephalography and Clinical Neurophysiology. Supplement, 51, 3–21.

    PubMed  Google Scholar 

  6. Belmonte, M. K. (2000). Abnormal attention in autism shown by steady-state visual evoked potentials. Autism, 4, 269–285.

    Article  Google Scholar 

  7. Belmonte, M. K., Allen, G., Beckel-Mitchener, A., Boulanger, L., Carper, R., & Webb, S. J. (2004a). Autism and abnormal development of brain connectivity. Journal of Neuroscience, 24, 9228–9231.

    PubMed  Article  Google Scholar 

  8. Belmonte, M. K., Cook, E. H., Anderson, G. M., Rubenstein, J. L. R., Greenhough, W. T., Beckel-Mitchener, A., et al. (2004b). Autism as a disorder of neural information processing: Directions for research and targets for therapy. Molecular Psychiatry, 9, 646–663.

    PubMed  Google Scholar 

  9. Belmonte, M. K., & Yurgelun-Todd, D. A. (2003a). Functional anatomy of impaired selective attention and compensatory processing in autism. Brain Research. Cognitive Brain Research, 17, 651–664.

    PubMed  Article  Google Scholar 

  10. Belmonte, M. K., & Yurgelun-Todd, D. A. (2003b). Anatomic dissociation of selective and suppressive processes in visual attention. NeuroImage, 19, 180–189.

    PubMed  Google Scholar 

  11. Bertone, A., Mottron, L., Jelenic, P., & Faubert, J. (2005). Enhanced and diminished visuo-spatial information processing in autism depend on stimulus complexity. Brain, 128, 2430–2441.

    PubMed  Article  Google Scholar 

  12. Bodfish, J. W., Symons, F. J., & Lewis, M. H. (1999). Repetitive behavior scale. Morganton, NC: Western Carolina Center Research Reports.

  13. Bodfish, J. W., Symons, F. S., Parker, D. E., & Lewis, M. H. (2000). Varieties of repetitive behavior in autism: Comparisons to mental retardation. Journal of Autism and Developmental Disorders, 30, 237–243.

    PubMed  Article  Google Scholar 

  14. Bomba, M. D., & Pang, E. W. (2004). Cortical auditory evoked potentials in autism: A review. International Journal of Psychophysiology, 53, 161–169.

    PubMed  Article  Google Scholar 

  15. Bottger, D., Herrmann, C., & von Ramon, D. Y. (2002). Amplitude differences of evoked alpha and gamma oscillations in two different age groups. International Journal of Psychophysiology, 45, 245–251.

    PubMed  Article  Google Scholar 

  16. Brock, J., Brown, C. C., Boucher, J., & Rippon, G. (2002). The temporal binding deficit hypothesis of autism. Development and Psychopathology, 14, 209–224.

    PubMed  Article  Google Scholar 

  17. Brown, C. (2005). EEG in autism: Is there just too much going on in there? In F. Manuel & M. F. Casanova (Eds.), Recent developments in autism research (pp. 109–126). New York: Nova Science Publishers.

    Google Scholar 

  18. Brown, C., Gruber, T., Boucher, J., Rippon, G., & Brock, J. (2005). Gamma abnormalities during perception of illusory figures in autism. Cortex, 41, 364–376.

    PubMed  Article  Google Scholar 

  19. Buxhoeveden, D. P., & Casanova, M. F. (2002). The minicolumn and evolution of the brain. Brain, Behavior and Evolution, 60(3), 125–151.

    PubMed  Article  Google Scholar 

  20. Casanova, M. F. (2005). Minicolumnar pathology in autism. In M. F. Casanova (Ed.), Recent developments in autism research (pp. 133–144). New York: Nova Biomedical Books.

    Google Scholar 

  21. Casanova, M. F. (2006). Neuropathological and genetic findings in autism: The significance of a putative minicolumnopathy. The Neuroscientist, 12(5), 435–441.

    PubMed  Article  Google Scholar 

  22. Casanova, M. F., Buxhoeveden, D., & Gomez, J. (2003). Disruption in the inhibitory architecture of the cell minicolumn: Implications for autism. The Neuroscientist, 9, 496–507.

    PubMed  Article  Google Scholar 

  23. Casanova, M. F., Buxhoeveden, D. P., Switala, A. E., & Roy, E. (2002a). Minicolumnar pathology in autism. Neurology, 58, 428–432.

    PubMed  Google Scholar 

  24. Casanova, M. F., Buxhoeveden, D. P., Switala, A. E., & Roy, E. (2002b). Neuronal density and architecture (gray level index) in the brains of autistic patients. Journal of Child Neurology, 17, 515–521.

    PubMed  Article  Google Scholar 

  25. Casanova, M. F., van Kooten, I., Switala, A. E., van England, H., Heinsen, H., Steinbuch, H. W. M., et al. (2006a). Abnormalities of cortical minicolumnar organization in the prefrontal lobes of autistic patients. Clinical Neuroscience Research, 6(3–4), 127–133.

    Article  Google Scholar 

  26. Casanova, M. F., van Kooten, I., van Engeland, H., Heinsen, H., Steinbursch, H. W. M., Hof, P. R., et al. (2006b). Minicolumnar abnormalities in autism II. Neuronal size and number. Acta Neuropathologica, 112(3), 287–303.

    PubMed  Article  Google Scholar 

  27. Ciesielski, K. T., Courchesne, E., & Elmasian, R. (1990). Effects of focused selective attention tasks on event-related potentials in autistic and normal individuals. Electroencephalography and Clinical Neurophysiology, 75, 207–220.

    PubMed  Article  Google Scholar 

  28. Ciesielski, K. T., Knoght, J. E., Prince, R. J., Harris, R. J., & Handmaker, S. D. (1995). Event-related potentials in cross-modal divided attention in autism. Neuropsychologia, 33, 225–246.

    PubMed  Article  Google Scholar 

  29. Constantino, J. N., & Gruber, C. P. (2005). The social responsiveness scale (SRS) manual. Los Angeles, CA: Western Psychological Services.

    Google Scholar 

  30. Courchesne, E., Lincoln, A. J., Yeung-Courchesne, R., Elmasian, R., & Grillon, C. (1989). Pathophysiologic findings in nonretarded autism and receptive developmental disorder. Journal of Autism and Developmental Disorders, 19, 1–17.

    PubMed  Article  Google Scholar 

  31. Daskalakis, Z. J., Christensen, B. K., Fitzgerald, P. B., & Chen, R. (2002). Transcranial magnetic stimulation: A new investigational and treatment tool in psychiatry. Journal of Neuropsychiatry and Clinical Neurosciences, 14(4), 406–415.

    PubMed  Google Scholar 

  32. Dawson, G., Finley, C., Phillips, S., Galpert, L., & Lewy, A. (1988). Reduced P3 amplitude of the event-related brain potential: Its relationship to language ability in autism. Journal of Autism and Developmental Disorders, 18, 493–504.

    PubMed  Article  Google Scholar 

  33. DeFelipe, J. (1999). Chandelier cells and epilepsy. Brain, 122, 1807–1822.

    PubMed  Article  Google Scholar 

  34. DeFelipe, J. (2004). Cortical microanatomy and human brain disorders: Epilepsy. Cortex, 40(1), 232–233.

    PubMed  Article  Google Scholar 

  35. DeFelipe, J., Hendry, S. H. C., Hashikawa, T., Molinary, M., & Jones, E. G. (1990). A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons. Neuroscience, 37, 655–673.

    PubMed  Article  Google Scholar 

  36. Douglas, R. J., & Martin, K. A. C. (2004). Neuronal circuits of the neocortex. Annual Review of Neuroscience, 27, 419–451.

    PubMed  Article  Google Scholar 

  37. Engel, A. K., Konig, P., Kreiter, A. K., & Singer, W. (1991). Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex. Science, 252, 218–226.

    Article  Google Scholar 

  38. Favorov, O. V., & Kelly, D. G. (1994a). Minicolumnar organization within somatosensory cortical segregates, I: Development of afferent connections. Cerebral Cortex, 4, 408–427.

    PubMed  Article  Google Scholar 

  39. Favorov, O. V., & Kelly, D. G. (1994b). Minicolumnar organization within somatosensory cortical segregates, II: Emergent functional properties. Cerebral Cortex, 4, 428–442.

    PubMed  Article  Google Scholar 

  40. Felli, R., Fernandez, G., Klaver, P., Elger, C. E., & Fries, P. (2003). Is synchronized neuronal gamma activity relevant for selective attention? Brain Research Reviews, 42, 265–272.

    Article  Google Scholar 

  41. Ferri, R., Elia, M., Agarwal, N., Lanuzza, B., Musumeci, S. A., & Pennisi, G. (2003). The mismatch negativity and the P3a components of the auditory event-related potentials in autistic low-functioning subjects. Clinical Neurophysiology, 114, 1671–1680.

    PubMed  Article  Google Scholar 

  42. First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (2001). Structured clinical interview for DSM-IV-TR axis I disorders, non-patient edition (SCID—I/P). New York: New York State Psychiatric Institute.

    Google Scholar 

  43. Frith, U., & Happé, F. (1994). Autism: Beyond theory of mind. Cognition, 50, 115–132.

    PubMed  Article  Google Scholar 

  44. Gershon, A. A., Dannon, P. N., & Grunhaus, L. (2003). Transcranial magnetic stimulation in the treatment of depression. American Journal of Psychiatry, 160, 835–845.

    PubMed  Article  Google Scholar 

  45. Goodman, W. K., Price, L. H., Rasmussen, S. A., Mazure, C., Fleischmann, R. L., Hill, C. L., et al. (1989). The yale-brown obsessive compulsive scale, I: Development, use, and reliability. Archives of General Psychiatry, 46, 1006–1011.

    PubMed  Google Scholar 

  46. Goupillaud, P., Grossman, A., & Morlet, J. (1984). Cycle-octave and related transforms in seismic signal analysis. Geoexploration, 23, 85–102.

    Article  Google Scholar 

  47. Gray, C. M., & Singer, W. (1989). Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proceedings of the National Academy of Sciences of the USA, 86, 1698–1702.

    PubMed  Article  Google Scholar 

  48. Greenberg, B. D. (2007). Transcranial magnetic stimulation in anxiety disorders. In M. S. George & R. H. Belmaker (Eds.), Thanscranial magnetic stimulation in clinical psychiatry (pp. 165–178). Washington, DC: American Psychiatric Publishing Inc.

    Google Scholar 

  49. Greenberg, B. D., George, M. S., Martin, J. D., Benjamin, J., Schlaepfer, T. E., Altemus, M., et al. (1997). Effect of prefrontal repetitive transcranial magnetic stimulation in obsessive-compulsive disorder: A preliminary study. American Journal of Psychiatry, 154, 867–869.

    PubMed  Google Scholar 

  50. Griffith, E. M., Pennington, B. F., Wehner, E. A., & Rogers, S. J. (1999). Executive functions in young children with autism. Child Development, 70, 817–832.

    PubMed  Article  Google Scholar 

  51. Gruber, T., Muller, M. M., Keil, A., & Elbert, T. (1999). Selective visual-spatial attention alters induced gamma band responses in the human EEG. Clinical Neurophysiology, 110, 2074–2085.

    PubMed  Article  Google Scholar 

  52. Guy, W. (1976). Clinical global impressions. ECDEU assessment manual for psychopharmacology. Rockville, MD: National Institute of Mental Health.

    Google Scholar 

  53. Happe, F., & Frith, U. (2006). The weak coherence account: Detail-focused cognitive style in autism spectrum disorders. Journal of Autism and Developmental Disorders, 36(1), 5–25.

    PubMed  Article  Google Scholar 

  54. Helmich, R. C., Siebner, H. R., Bakker, M., Munchau, A., & Bloem, B. R. (2006). Repetitive transcranial magnetic stimulation to improve mood and motor function in Parkinson’s disease. Journal of Neurological Sciences, 248, 84–96.

    Article  Google Scholar 

  55. Herrmann, C. S., & Mecklinger, A. (2000). Magnetoencephalographic responses to illusory figures: Early evoked gamma is affected by processing of stimulus features. International Journal of Psychophysiology, 38, 265–281.

    PubMed  Article  Google Scholar 

  56. Herrmann, C. S., Mecklinger, A., & Pfeirffer, E. (1999). Gamma responses and ERPs in a visual classification task. Clinical Neurophysiology, 110(4), 636–642.

    PubMed  Article  Google Scholar 

  57. Herrmann, C. S., & Knight, R. T. (2001). Mechanisms of human attention: Event related potentials and oscillations. Neuroscience and Biobehavioral Reviews, 25, 465–476.

    PubMed  Article  Google Scholar 

  58. Herrmann, C. S., & Mecklinger, A. (2000). Magnetoencephalographic responses to illusory figures: Early evoked gamma is affected by processing of stimulus features. International Journal of Psychophysiology, 38, 265–281.

    PubMed  Article  Google Scholar 

  59. Hoffman, R. E., & Cavus, I. (2002). Slow transcranial magnetic stimulation, long-term depotentiation, and brain hyperexcitability disorders. American Journal of Psychiatry, 159, 1093–1102.

    PubMed  Article  Google Scholar 

  60. Holcomb, P. J., Ackerman, P. T., & Dykman, R. A. (1985). Cognitive event-related brain potentials in children with attention and reading deficits. Psychophysiology, 22, 656–667.

    PubMed  Article  Google Scholar 

  61. Holtzheimer, P. E., Russo, J., & Avery, D. H. (2001). A meta-analysis of repetitive transcranial magnetic stimulation in the treatment of depression. Psychopharmacology Bulletin, 35, 149–169.

    PubMed  Google Scholar 

  62. Kahana, M. J. (2006). The cognitive correlates of human brain oscillations. The Journal of Neuroscience, 26(6), 1669–1672.

    PubMed  Article  Google Scholar 

  63. Kanizsa, G. (1976). Subjective contours. Scientific American, 235, 48–52.

    Article  Google Scholar 

  64. Katayama, J., & Polich, J. (1998). Stimulus context determines P3a and P3b. Psychophysiology, 35, 23–33.

    PubMed  Article  Google Scholar 

  65. Keil, A., Muller, M. M., Ray, W. J., Gruber, T., & Elbert, T. (1999). Human gamma band activity and perception of a Gestalt. The Journal of Neuroscience, 19, 7152–7161.

    PubMed  Google Scholar 

  66. Kemner, C., van der Gaag, R. J., Verbaten, M., & van Engeland, H. (1999). ERP differences among subtypes of pervasive developmental disorders. Biological Psychiatry, 46, 781–789.

    PubMed  Article  Google Scholar 

  67. Kemner, C., Verbaten, M. N., Cuperus, J. M., Camfferman, G., & Van Engeland, H. (1994). Visual and somatosensory event-related brain potentials in autistic children and three different control groups. Electroencephalography and Clinical Neurophysiology, 92, 225–237.

    PubMed  Article  Google Scholar 

  68. Kemner, C., Verbaten, M. N., Cuperus, J. M., Camfferman, G., & Van Engeland, H. (1995). Auditory event-related potentials in autistic children and three different control groups. Biological Psychiatry, 38, 150–165.

    PubMed  Article  Google Scholar 

  69. Le Couteur, A., Lord, C., & Rutter, M. (2003). The autism diagnostic interview—Revised (ADI-R). Los Angeles, CA: Western Psychological Services.

    Google Scholar 

  70. Lincoln, A. J., Courchesne, E., Harms, L., & Allen, M. (1993). Contextual probability evaluation in autistic, receptive developmental disorder and control children: Event-related potential evidence. Journal of Autism and Developmental Disorders, 23, 37–58.

    PubMed  Article  Google Scholar 

  71. Lohmann, H., & Köppen, H. J. (1995). Postnatal development of pyramidal dendritic and axonal bundles in the visual cortex of the rat. Journal für Hirnforsch, 36(1), 101–111.

    Google Scholar 

  72. Loo, C., & Mitchell, P. (2005). A review of the efficacy of transcranial magnetic stimulation (TMS) treatment for depression, and current and future strategies to optimize efficacy. Journal of Affective Disorders, 88, 255–267.

    PubMed  Article  Google Scholar 

  73. Martin, J. L. R., Barbanoj, M. J., Pérez, V., & Sacristán, M. (2003). Transcranial magnetic stimulation for the treatment of obsessive-compulsive disorder. Cochrane Database of Systematic Reviews, 2003(2), Art No.: CD003387. doi:10.1002/14651858.CD003387.

  74. Morgan, B., Maybery, M., & Durkin, K. (2003). Weak central coherence, poor joint attention, and low verbal ability: Independent deficits in early autism. Developmental Psychology, 39(4), 646–656.

    PubMed  Article  Google Scholar 

  75. Mottron, L., Burack, J., Iarocci, G., Belleville, S., & Enns, J. T. (2003). Locally oriented perception with intact global processing among adolescents with high-functioning autism: Evidence from multiple paradigms. Journal of Child Psychology and Psychiatry, 44, 904–913.

    PubMed  Article  Google Scholar 

  76. Mountcastle, V. B. (1997). The columnar organization of the neocortex. Brain, 120, 701–722.

    PubMed  Article  Google Scholar 

  77. Muller, M. M., Gruber, T., & Keil, A. (2000). Modulation of induced gamma band activity in the human EEG by attention and visual information processing. International Journal of Psychophysiology, 38, 283–299.

    PubMed  Article  Google Scholar 

  78. Nakatani, C., Ito, J., Nikolaev, A. R., Gong, P., & Leeuwen, C. V. (2005). Phase synchronization analysis of EEG during attentional blink. Journal of Cognitive Neuroscience, 17(12), 1969–1979.

    PubMed  Article  Google Scholar 

  79. Oades, R. D., Walker, M. K., Geffen, L. B., & Stern, L. M. (1988). Event-related potentials in autistic and healthy children on an auditory choice reaction time task. International Journal of Psychophysiology, 6, 25–37.

    PubMed  Article  Google Scholar 

  80. Pavlova, M., Birbaumer, N., & Sokolov, A. (2006). Attentional modulation of cortical neuromagnetic gamma response to biological movement. Cerebral Cortex, 16, 321–327.

    PubMed  Article  Google Scholar 

  81. Plaisted, K., Saksida, L., Alcántara, J., & Weisblatt, E. (2003). Towards an understanding of the mechanisms of weak central coherence effects: Experiments in visual configural learning and auditory perception. Philosophical Transactions of the Royal Society of London B. Series B, Biological Sciences, 358, 375–386.

    Article  Google Scholar 

  82. Polich, J. (2003). Theoretical overview of P3a and P3b. In J. Polich (Ed.), Detection of change: Event-related potential and fMRI findings (pp. 83–98). Boston: Kluwer Academic Press.

    Google Scholar 

  83. Potts, G. F., Patel, S. H., & Azzam, P. N. (2004). Impact of instructed relevance on the visual ERP. International Journal of Psychophysiology, 52, 197–209.

    PubMed  Article  Google Scholar 

  84. Prasko, J., Pasková, B., Záleský, R., Novák, T., Kopecek, M., Bares, M., et al. (2006). The effect of repetitive transcranial magnetic stimulation (rTMS) on symptoms in obsessive compulsive disorder. A randomized, double blind, sham controlled study. Neuro Endocrinology Letters, 27, 327–332.

    PubMed  Google Scholar 

  85. Rippon, G., Brock, J., Brown, C., & Boucher, J. (2007). Disordered connectivity in the autistic brain: Challenges for the ‘new psychophysiology’. International Journal of Psychophysiology, 63, 164–172.

    PubMed  Article  Google Scholar 

  86. Rodriguez, E., George, N., Lachaux, J. P., Martinerie, J., Renault, B., & Varela, F. J. (1999). Perception’s shadow: Long distance synchronization of human brain activity. Nature, 397, 430–433.

    PubMed  Article  Google Scholar 

  87. Roid, G. H. (2003). Stanford–Binet intelligence scales. Technical manual (5th ed.). Itasca, IL: Riverside Publishing.

    Google Scholar 

  88. Rosenberg, P. B., Mehndiratta, R. B., Mehndiratta, Y. P., Wamer, A., Rosse, R. B., & Balish, M. (2002). Repetitive magnetic stimulation treatment of comorbid posttraumatic stress disorder and major depression. Journal of Neuropsychiatry and Clinical Neurosciences, 14, 270–276.

    PubMed  Google Scholar 

  89. Rossi, S., & Rossini, P. M. (2004). TMS in cognitive plasticity and the potential for rehabilitation. Trends in Cognitive Sciences, 86, 273–279.

    Article  Google Scholar 

  90. Rubenstein, J. L., & Merzenich, M. M. (2003). Model of autism: Increased ratio of excitation/inhibition in key neural systems. Genes, Brain, and Behavior, 2, 255–267.

    PubMed  Article  Google Scholar 

  91. Sachdev, P. S., Loo, C. K., Mitchell, P. B., McFarquhar, T. F., & Malhi, G. S. (2007). Repetitive transcranial magnetic stimulation for the treatment of obsessive compulsive disorder: A double-blind controlled investigation. Psychological Medicine, 37, 1645–1649.

    PubMed  Article  Google Scholar 

  92. Sachdev, P. S., McBride, R., Loo, C. K., Mitchell, P. B., Malhi, G. S., & Croker, V. M. (2001). Right versus left prefrontal transcranial magnetic stimulation for obsessive-compulsive disorder: A preliminary investigation. Journal of Clinical Psychiatry, 62, 981–984.

    PubMed  Google Scholar 

  93. Tallon-Baudry, C. (2003). Oscillatory synchrony and human visual cognition. Journal of Physiology, Paris, 97, 355–363.

    PubMed  Article  Google Scholar 

  94. Tallon-Baudry, C., Bertrand, O., Henaff, M.-A., Isnard, J., & Fischer, C. (2005). Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. Cerebral Cortex, 15, 654–662.

    PubMed  Article  Google Scholar 

  95. Tallon-Baudry, C., Bertrand, O., Peronnet, F., & Pernier, J. (1998). Induced gamma-band activity during the delay of a visual short-term memory task in humans. The Journal of Neuroscience, 18(11), 4244–4254.

    PubMed  Google Scholar 

  96. Townsend, J., Westerfield, M., Leaver, E., Makeig, S., Jung, T., et al. (2001). Event-related brain response abnormalities in autism: Evidence for impaired cerebello-frontal spatial attention networks. Brain Research. Cognitive Brain Research, 11, 127–145.

    PubMed  Article  Google Scholar 

  97. Varela, F., Lachaux, J., Rodriguez, E., & Martinerie, J. (2001). The brainweb: Phase synchronization and large-scale integration. Nature Reviews. Neuroscience, 2, 229–239.

    PubMed  Article  Google Scholar 

  98. Verbaten, M. N., Roelofs, J. W., van Engeland, H., Kenemans, J. K., & Slangen, J. L. (1991). Abnormal visual event-related potentials of autistic children. Journal of Autism Developmental Disorders, 21, 449–470.

    Article  Google Scholar 

  99. Von Stein, A., Rappelsberger, P., Sarnthein, J., & Petsche, H. (1999). Synchronization between temporal and parietal cortex during multimodal object processing in man. Cerebral Cortex, 9, 137–150.

    Article  Google Scholar 

  100. Walsh, V., & Pascual-Leone, A. (2003). Transcranial magnetic stimulation: A neurochronometrics of mind. Cambridge, MA: MIT Press.

    Google Scholar 

  101. Wassermann, E. M., & Lisanby, S. H. (2001). Therapeutic application of repetitive transcranial magnetic stimulation: A review. Clinical Neurophysiology, 112, 1367–1377.

    PubMed  Article  Google Scholar 

  102. Wechsler, D. (2003). Wechsler intelligence scale for children (4th ed.). San Antonio, TX: Harcourt Assessment, Inc.

    Google Scholar 

  103. Wijers, A. A., Mulder, G., Gunter, T. C., & Smid, H. G. O. M. (1996). Brain potential analysis of selective attention. In O. Neumann & A. F. Sanders (Eds.), Handbook of perception and action. Attention (Vol. 3, pp. 333–387). Tullamore, Ireland: Academic Press.

    Google Scholar 

  104. Yáñez, I. B., Muñoz, A., Contreras, J., Gonzalez, J., Rodriguez-Veiga, E., & DeFelipe, J. (2005). Double bouquet cell in the human cerebral cortex and a comparison with other mammals. Journal of Comparative Neurology, 486(4), 344–360.

    PubMed  Article  Google Scholar 

  105. Ziemann, U. (2004). TMS induced plasticity in human cortex. Reviews Neuroscience, 15(4), 253–266.

    Google Scholar 

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Sokhadze, E.M., El-Baz, A., Baruth, J. et al. Effects of Low Frequency Repetitive Transcranial Magnetic Stimulation (rTMS) on Gamma Frequency Oscillations and Event-Related Potentials During Processing of Illusory Figures in Autism. J Autism Dev Disord 39, 619–634 (2009). https://doi.org/10.1007/s10803-008-0662-7

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Keywords

  • Autism
  • Minicolumns
  • Event-related potentials
  • Electroencephalography
  • Gamma frequencies