Low-Frequency Repetitive Transcranial Magnetic Stimulation (rTMS) Affects Event-Related Potential Measures of Novelty Processing in Autism

Abstract

In our previous study on individuals with autism spectrum disorder (ASD) (Sokhadze et al., Appl Psychophysiol Biofeedback 34:37–51, 2009a) we reported abnormalities in the attention-orienting frontal event-related potentials (ERP) and the sustained-attention centro-parietal ERPs in a visual oddball experiment. These results suggest that individuals with autism over-process information needed for the successful differentiation of target and novel stimuli. In the present study we examine the effects of low-frequency, repetitive Transcranial Magnetic Stimulation (rTMS) on novelty processing as well as behavior and social functioning in 13 individuals with ASD. Our hypothesis was that low-frequency rTMS application to dorsolateral prefrontal cortex (DLFPC) would result in an alteration of the cortical excitatory/inhibitory balance through the activation of inhibitory GABAergic double bouquet interneurons. We expected to find post-TMS differences in amplitude and latency of early and late ERP components. The results of our current study validate the use of low-frequency rTMS as a modulatory tool that altered the disrupted ratio of cortical excitation to inhibition in autism. After rTMS the parieto-occipital P50 amplitude decreased to novel distracters but not to targets; also the amplitude and latency to targets increased for the frontal P50 while decreasing to non-target stimuli. Low-frequency rTMS minimized early cortical responses to irrelevant stimuli and increased responses to relevant stimuli. Improved selectivity in early cortical responses lead to better stimulus differentiation at later-stage responses as was made evident by our P3b and P3a component findings. These results indicate a significant change in early, middle-latency and late ERP components at the frontal, centro-parietal, and parieto-occipital regions of interest in response to target and distracter stimuli as a result of rTMS treatment. Overall, our preliminary results show that rTMS may prove to be an important research tool or treatment modality in addressing the stimulus hypersensitivity characteristic of autism spectrum disorders.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Aman, M. G. (2004). Management of hyperactivity and other acting-out problems in patients with autism spectrum disorder. Seminars in Pediatric Neurology, 11(3), 225–228.

    Article  PubMed  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  5. 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.

    Article  PubMed  Google Scholar 

  6. 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 

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

    Article  PubMed  Google Scholar 

  8. 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 

  9. 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.

    Article  PubMed  Google Scholar 

  10. Bodfish, J. W., Symons, F. J., & Lewis, M. H. (1999). Repetitive Behavior Scale. Western Carolina Center Research Reports.

  11. 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.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  13. Boutros, N. N., Korzyukov, O., Jansen, B., Feingold, A., & Bell, M. (2004). Sensory gating deficits during the mid-latency phase of information processing in medicated schizophrenia patients. Psychiatry Research, 126, 203–215.

    Article  PubMed  Google Scholar 

  14. Bruneau, N., Roux, S., Adrien, J. L., & Bathelemy, C. (1999). Auditory associative cortex dysfunction in children with autism: Evidence from late auditory evoked potentials (N 1 wave- T Complex). Clinical Neurophysiology, 110, 1927–1934.

    Article  PubMed  Google Scholar 

  15. Burack, J. A. (1994). Selective attention deficits in persons with autism: Preliminary evidence for inefficient attentional lens. Journal of Abnormal Psychology, 103, 515–543.

    Article  Google Scholar 

  16. 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 

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

    Article  PubMed  Google Scholar 

  18. 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.

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  20. 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 Child Neurology, 17, 515–521.

    Article  Google Scholar 

  21. 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 

  22. 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, 287–303.

    Article  PubMed  Google Scholar 

  23. Chandana, S. R., Behen, M. E., Juhász, C., Muzik, O., Rothermel, R., Mangner, T. J., et al. (2005). Significance of abnormalities in developmental trajectory and asymmetry of cortical serotonin synthesis in autism. International Journal of Developmental Neuroscience, 23, 171–182.

    Article  PubMed  Google Scholar 

  24. Childs, J. A., & Blair, J. L. (1997). Valproic acid treatment of epilepsy in autistic twins. Journal Neuroscience Nursing, 29, 244–248.

    Google Scholar 

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

    Article  Google Scholar 

  26. 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.

    Article  PubMed  Google Scholar 

  27. Constantino, J. N., & Gruber, C. P. (2005). The Social Responsiveness Scale (SRS) manual. Los Angeles, CA: Western Psychological Services.

    Google Scholar 

  28. 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.

    Article  PubMed  Google Scholar 

  29. Courchesne, E., & Pierce, K. (2005). Brain overgrowth in autism during a critical time in development: Implications for frontal pyramidal neuron and interneuron development and connectivity. International Journal Developmental Neuroscience, 23, 153–170.

    Article  Google Scholar 

  30. 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, 406–415.

    PubMed  Google Scholar 

  31. 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.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  34. DeFelipe, J., Hendry, S. H. C., Hashikawa, T., Molinari, M., & Jones, E. G. (1990). A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons.

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  37. Ferree, T. C., Luu, P., Russell, G. S., & Tucker, D. M. (2001). Scalp electrode impedance, infection risk, and EEG data quality. Clinical Neurophysiology, 112, 444–536.

    Article  Google Scholar 

  38. 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.

    Article  PubMed  Google Scholar 

  39. Fletcher, E. M., Kussmaul, C. L., & Mangun, G. R. (1996). Estimation of interpolation errors in scalp topographic mapping. Electroctoencephalography and Clinical Neuraphysiology, 98, 422–434.

    Article  Google Scholar 

  40. Garvey, M. A., & Mall, V. (2008). Transcranial magnetic stimulation in children. Clinical Neurophysiology, 119, 973–984.

    Article  PubMed  Google Scholar 

  41. George, M. S., & Belmaker, R. H. (2007). Transcranial magnetic stimulation in clinical psychiatry. Arlington, VA: American Psychiatry Publishing Inc.

    Google Scholar 

  42. George, M. S., Nahas, J., Kozol, F. A., Li, X., Yamanaka, K., Mishory, A., et al. (2003). Mechanisms and the current state of transcranial magnetic stimulation. CNS Spectrums, 8(7), 496–514.

    PubMed  Google Scholar 

  43. George, M. S., Nahas, Z., Molloy, M., Speer, A. M., Oliver, N. C., Li, X.-B., et al. (2000). A controlled trial of daily prefrontal cortex TMS for treating depression. Biological Psychiatry, 48, 962–970.

    Article  PubMed  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.

    Article  PubMed  Google Scholar 

  45. 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 

  46. 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.

    Article  PubMed  Google Scholar 

  47. 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 

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

    Article  PubMed  Google Scholar 

  49. 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.

    Article  PubMed  Google Scholar 

  50. Hollander, E., Dolgoff-Kaspar, R., Cartwright, C., Rawitt, R., & Novotny, S. (2001). An open trial of divalproex sodium in autism spectrum disorders. Journal of Clinical Psychiatry, 62, 530–534.

    PubMed  Google Scholar 

  51. Hruby, T., & Marsalek, P. (2003). Event-related potentials—The P3 wave. Acta Neurobiologiae Experimentalis (Wars), 63, 55–63.

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  53. 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.

    Article  PubMed  Google Scholar 

  54. 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.

    Article  PubMed  Google Scholar 

  55. 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.

    Article  PubMed  Google Scholar 

  56. Kisley, M. A., & Cornwell, Z. M. (2006). Gamma and beta neural activity evoked during a sensory gating paradigm: Effects of auditory, somatosensory and cross-modal stimulation. Clinical Neurophysiology, 11, 2549–2563.

    Article  Google Scholar 

  57. Kisley, M. A., Noecker, T. L., & Guinther, P. M. (2004). Comparison of sensory gating to mismatch negativity and self-reported perceptual phenomena in healthy adults. Psychophysiology, 41, 604–612.

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  59. 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.

    Article  PubMed  Google Scholar 

  60. 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.

    Article  PubMed  Google Scholar 

  61. Luu, P., Tucker, D. M. L., Englander, R., Lockfeld, A., Lutsep, H., & Oken, B. (2001). Localizing acute stroke-related EEC changes: Assessing the effects of spatial undersampling. Journal of Clinical Neurophysiology, 18, 302–317.

    Article  PubMed  Google Scholar 

  62. Mathalon, D. H., Fedor, M., Faustman, W. O., Gray, M., Askari, N., & Ford, J. M. (2002). Response-monitoring dysfunction in schizophrenia: An event-related brain potential study. Journal of Abnormal Psychology, 111, 22–41.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  64. Mountcastle, V. B. (2003). Introduction: Computation in cortical columns. Cerebral Cortex, 13, 2–4.

    Article  PubMed  Google Scholar 

  65. Nahas, Z., DeBrux, C., Chandler, V., Lorberbaum, J. P., Speer, A. M., et al. (2000). Lack of significant changes on magnetic resonance scans before and after 2 weeks of daily left prefrontal repetitive transcranial magnetic stimulation for depression. The Journal of ECT, 16(4), 380–390.

    Article  PubMed  Google Scholar 

  66. 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.

    Article  PubMed  Google Scholar 

  67. Ogawa, A., Ukai, S., Shinosaki, K., Yamamoto, M., Kawaguchi, S., Ishii, R., et al. (2004). Slow repetitive transcranial magnetic stimulation increases somatosensory high-frequency oscillations in humans. Neuroscience Letters, 358, 193–196.

    Article  PubMed  Google Scholar 

  68. Pascual-Leone, A., Walsh, V., & Rothwell, J. (2000). Transcranial magnetic stimulation in cognitive neuroscience—Virtual lesion, chronometry, and functional connectivity. Current Opinions in Neurobiology, 10, 232–237.

    Article  Google Scholar 

  69. Perrin, E., Pernier, J., Bertrand, O., Giard, M., & Echallier, J. F. (1987). Mapping of scalp potentials by surface spline interpolation. Electroencephalography and Clinical Neurophysiology, 66, 75–81.

    Article  PubMed  Google Scholar 

  70. Picton, T. W. (1992). The P300 wave of the human event-related potential. Journal Clinical Neurophysiology, 9, 456–479.

    Google Scholar 

  71. Plioplys, A. V. (1994). Autism: Electroencephalogram abnormalities and clinical improvement with valproic acid. Archives of Pediatrics and Adolescent Medicine, 148, 220–222.

    PubMed  Google Scholar 

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

    Google Scholar 

  73. 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.

    Article  PubMed  Google Scholar 

  74. Quintana, H. (2005). Transcranial magnetic stimulation in persons younger than the age of 18. The Journal of ECT, 21, 88–95.

    Article  PubMed  Google Scholar 

  75. Roid, G. H. (2003). Stanford-Binet Intelligence Scales, fifth edition, technical manual. Itasca, IL: Riverside Publishing.

    Google Scholar 

  76. 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 

  77. 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 

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

    Article  Google Scholar 

  79. Seldon, H. L. (1981a). Structure of human auditory cortex, I: Cytoarchitectonics and dendritic distributions. Brain Research, 229, 277–294.

    Article  PubMed  Google Scholar 

  80. Seldon, H. L. (1981b). Structure of human auditory cortex, II: Axon distributions and morphological correlates of speech perception. Brain Research, 229, 295–310.

    Article  PubMed  Google Scholar 

  81. Seri, S., Cerquiglini, A., Pisani, F., & Curatolo, P. (1999). Autism in tuberous sclerosis: Evoked potential evidence for a deficit in auditory sensory processing. Clinical Neurophysiology, 110, 1825–1830.

    Article  PubMed  Google Scholar 

  82. Sokhadze, E., Baruth, J., Tasman, A., Sears, L., Mathai, G., El-Baz, A., et al. (2009a). Event-related potential study of novelty processing abnormalities in autism. Applied Psychophysiology and Biofeedback, 34, 37–51.

    Article  PubMed  Google Scholar 

  83. Sokhadze, E. M., Singh, S., El-Baz, A., Baruth, J., Mathai, G., Sears, L., et al. (2009b). Effect of a low-frequency repetitive transcranial magnetic stimulation (rTMS) on induced gamma frequency oscillations and event-related potentials during processing of illusory figures in autism spectrum disorders. Journal of Autism and Developmental Disorders, 39, 619–634.

    Article  PubMed  Google Scholar 

  84. Srinivasan, R., Tucker, D. M., & Murias, M. (1998). Estimating the spatial Nyquist of the human EEC. Behavior Research Methods, Instruments, and Computers, 30, 8–19.

    Google Scholar 

  85. 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.

    Article  PubMed  Google Scholar 

  86. Uvebrant, P., & Bauzienè, R. (1994). Intractable epilepsy in children: The efficacy of lamotrigine treatment, including non-seizure-related benefits. Neuropediatrics, 25, 284–289.

    Article  PubMed  Google Scholar 

  87. 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 and Developmental Disorders, 21(4), 449–470.

    Article  PubMed  Google Scholar 

  88. Volkmar, F. R., & Nelson, D. S. (1995). Seizure disorders in autism. Journal of American Academy of Child Adolescent Psychiatry, 29, 127–129.

    Article  Google Scholar 

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

    Google Scholar 

  90. Wassermann, E. M., Grafman, J., Berry, C., Hollnagel, C., Wild, K., Clark, K., et al. (1996). Use and safety of a new repetitive transcranial magnetic stimulator. Electroencephalography Clinical Neurophysiology, 101, 412–417.

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  92. Wechsler, D. (2003). Wechsler Intelligence Scale for children (4th ed.). San Antonio, TX: Harcourt Assessment Inc.

    Google Scholar 

  93. Wechsler, D. (2004). Wechsler Abbreviated Scale for intelligence. San Antonio, TX: Harcourt Assessment Inc.

    Google Scholar 

  94. Welchew, D. E., Ashwin, C., Berkouk, K., Salvador, R., Suckling, J., Baron-Cohen, S., et al. (2005). Functional disconnectivity of the medial temporal lobe in Asperger’s syndrome. Biological Psychiatry, 57, 991–998.

    Article  PubMed  Google Scholar 

  95. 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. Vol. 3: Attention (pp. 333–387). Tullamore, Ireland: Academic Press.

    Google Scholar 

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

    Google Scholar 

Download references

Acknowledgments

The project was partially supported by R01 Eureka grant from the National Institutes of Health to Manuel Casanova.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Estate Sokhadze.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sokhadze, E., Baruth, J., Tasman, A. et al. Low-Frequency Repetitive Transcranial Magnetic Stimulation (rTMS) Affects Event-Related Potential Measures of Novelty Processing in Autism. Appl Psychophysiol Biofeedback 35, 147–161 (2010). https://doi.org/10.1007/s10484-009-9121-2

Download citation

Keywords

  • Event-related potentials
  • Autism
  • Novelty
  • Transcranial Magnetic Stimulation
  • Cortical excitation/inhibition balance
  • Minicolumns