Applied Psychophysiology and Biofeedback

, Volume 41, Issue 1, pp 47–60 | Cite as

Heart Rate Variability and Skin Conductance During Repetitive TMS Course in Children with Autism

  • Yao Wang
  • Marie K. Hensley
  • Allan Tasman
  • Lonnie Sears
  • Manuel F. Casanova
  • Estate M. Sokhadze
Article

Abstract

Autism spectrum disorder (ASD) is a developmental disorder marked by difficulty in social interactions and communication. ASD also often present symptoms of autonomic nervous system (ANS) functioning abnormalities. In individuals with autism the sympathetic branch of the ANS presents an over-activation on a background of the parasympathetic activity deficits, creating an autonomic imbalance, evidenced by a faster heart rate with little variation and increased tonic electrodermal activity. The objective of this study was to explore the effect of 12 sessions of 0.5 Hz repetitive transcranial magnetic stimulation (rTMS) over dorsolateral prefrontal cortex (DLPFC) on autonomic activity in children with ASD. Electrocardiogram and skin conductance level (SCL) were recorded and analyzed during each session of rTMS. The measures of interest were time domain (i.e., R–R intervals, standard deviation of cardiac intervals, NN50-cardio-intervals >50 ms different from preceding interval) and frequency domain heart rate variability (HRV) indices [i.e., power of high frequency (HF) and low frequency (LF) components of HRV spectrum, LF/HF ratio]. Based on our prior pilot studies it was proposed that the course of 12 weekly inhibitory low-frequency rTMS bilaterally applied to the DLPFC will improve autonomic balance probably through improved frontal inhibition of the ANS activity, and will be manifested in an increased length of cardiointervals and their variability, and in higher frequency-domain HRV in a form of increased HF power, decreased LF power, resulting in decreased LF/HF ratio, and in decreased SCL. Our post-12 TMS results showed significant increases in cardiac intervals variability measures and decrease of tonic SCL indicative of increased cardiac vagal control and reduced sympathetic arousal. Behavioral evaluations showed decreased irritability, hyperactivity, stereotype behavior and compulsive behavior ratings that correlated with several autonomic variables.

Keywords

Autism spectrum disorder Autonomic activity Transcranial magnetic stimulation (TMS) Heart rate Heart rate variability Skin conductance level 

References

  1. Althaus, M., Mulder, L. J., Mulder, G., Aarnoudse, C., & Minderaa, R. (1999). Cardiac adaptivity to attention-demanding tasks in children with a pervasive developmental disorder not otherwise specified (PDD-NOS). Biological Psychiatry, 46(6), 799–809.CrossRefPubMedGoogle Scholar
  2. Althaus, M., Van Roon, A. M., Mulder, L. J., Mulder, G., Aarnoudse, C., & Minderaa, R. (2004). Autonomic response patterns observed during the performance of an attention-demanding task in two groups of children with autistic-type difficulties in social adjustment. Psychophysiology, 41(6), 893–904.CrossRefPubMedGoogle Scholar
  3. 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.CrossRefPubMedGoogle Scholar
  4. Aman, M. G., & Singh, N. N. (1994). Aberrant behavior checklist-community. Supplementary manual. East Aurora, NY: Slosson Educational.Google Scholar
  5. Amat, J., Baratta, M. V., Paul, E., Bland, S. T., Watkins, L., & Maier, L. F. (2005). Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nature Neuroscience, 8(3), 365–371.CrossRefPubMedGoogle Scholar
  6. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., text revision). Washington, DC: American Psychiatric Association.Google Scholar
  7. Angus, Z. (1970). Autonomic and cognitive functions in childhood psychosis. Bulletin of British Psychological Society, 23, 228–229.Google Scholar
  8. Barry, R. J., & James, A. L. (1988). Coding of stimulus parameters in autistic, retarded, and normal children: Evidence for a two-factor theory of autism. International Journal of Psychophysiology, 6(2), 139–149.CrossRefPubMedGoogle Scholar
  9. Baruth, J. M., Casanova, M. F., El-Baz, A., Horrell, T., Mathai, G., & Sears, L. (2010). Low-frequency repetitive transcranial magnetic stimulation (rTMS) modulates evoked-gamma frequency oscillations in autism spectrum disorder (ASD). Journal of Neurotherapy, 14(3), 179–194.PubMedCentralCrossRefPubMedGoogle Scholar
  10. Baruth, J., Williams, E., Sokhadze, E., El-Baz, A., Sears, L., & Casanova, M. F. (2011). Repetitive transcranial stimulation (rTMS) improves electroencephalographic and behavioral outcome measures in autism spectrum disorders (ASD). Autism Science Digest, 1(1), 52–57.Google Scholar
  11. Benarroch, E. E. (1997). The central autonomic network. In P. A. Low (Ed.), Clinical autonomic disorders (2nd ed., pp. 17–23). Philadelphia: Lippincott-Raven.Google Scholar
  12. Ben-Shachar, D., Belmaker, R. H., Grisaru, N., & Klein, E. (1997). Transcranial magnetic stimulation induces in brain monoamines. Journal of Neural Transmission, 104(2–3), 191–197.CrossRefPubMedGoogle Scholar
  13. Berntson, G. G., Bigger, J. T., Eckberg, D. L., Grossman, P., Kaufmann, P. G., Malik, M., et al. (1997). Heart rate variability: Origins, methods and interpretive caveates. Psychophysiology, 34(6), 623–648.CrossRefPubMedGoogle Scholar
  14. Bodfish, J. W., Symons, F. J., & Lewis, J. (1999). Repetitive behavior scale. Western Carolina Center research reports. Morgantown, NC: Western Carolina Center.Google Scholar
  15. 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(3), 237–243.CrossRefPubMedGoogle Scholar
  16. Boucsein, W. (2012). Electrodermal activity (2nd ed.). New York: Springer.CrossRefGoogle Scholar
  17. Casanova, M. F. (2006). Neuropathological and genetic findings in autism: The significance of a putative minicolumnopathy. Neuroscientist, 12(5), 435–441.CrossRefPubMedGoogle Scholar
  18. Casanova, M. F., Baruth, J., El-Baz, A., Tasman, A., Sears, L., & Sokhadze, E. (2012). Repetitive transcranial magnetic stimulation (rTMS) modulates event-related potential (ERP) indices of attention in autism. Translational Neuroscience, 3(2), 170–180.PubMedCentralCrossRefPubMedGoogle Scholar
  19. Casanova, M. F., Buxhoeveden, D. P., & Brown, C. (2002). Clinical and macroscopic correlates of minicolumnar pathology in autism. Journal of Child Neurology, 17(9), 692–695.CrossRefPubMedGoogle Scholar
  20. Casanova, M. F., Hensley, M. K., Sokhadze, E., El-Baz, A., Wang, Y., & Sears, L. (2014). Effects of rTMS on autonomic functions in autism spectrum disorder. Frontiers in Behavioral Neurosciences, 8(851), 1–11. doi:10.389/fnsys.2014.00134.Google Scholar
  21. Casanova, M. F., Sokhadze, E., Opris, I., Wang, Y., & Li, X. (2015). Autism spectrum disorders: Linking neuropathological findings to treatment with transcranial magnetic stimulation. Acta Pediatrica, 104(4), 346–355.CrossRefGoogle Scholar
  22. Casanova, M. F., van Kooten, I. A., Switala, A. E., van Engeland, H., Heinsen, H., Steinbusch, H. W., et al. (2006). Abnormalities of cortical minicolumnar organization in the prefrontal lobes of autistic patients. Clinical Neuroscience Research, 6, 127–133.CrossRefGoogle Scholar
  23. Chang, M. C., Parham, L. D., Blanche, E. I., Schell, A., Chou, C. P., Dawson, M., & Clark, F. (2012). Autonomic and behavioral responses of children with autism to auditory stimuli. American Journal of Occupational Therapy, 66(5), 67–76.CrossRefGoogle Scholar
  24. Cohen, N., Benjamin, J., Geva, A. B., Matar, M. A., Kaplan, Z., & Kotler, M. (2000). Autonomic dysregulation in panic disorder and in post-traumatic stress disorder: Application of power spectrum analysis of heart rate variability at rest and in response to recollection of trauma or panic attack. Psychiatry Research, 96(1), 1–13.CrossRefPubMedGoogle Scholar
  25. Corona, R., Dissanayake, C., Arbelle, S., Wellington, P., & Sigman, M. (1998). Is affect aversive to young children with autism? Behavioral and cardiac responses to experimenter distress. Child Development, 69(6), 1494–1502.CrossRefPubMedGoogle Scholar
  26. Czeh, B., Welt, T., Fischer, A. K., Erhardt, A., Schmitt, W., Muler, M. B., et al. (2002). Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: Effects on stress hormone levels and adult hippocampal neurogenesis. Biological Psychiatry, 52(11), 1057–1065.CrossRefPubMedGoogle Scholar
  27. Damasio, A. R. (1994). Descartes error: Emotion, reason, and the human brain. New York: Avon Books.Google Scholar
  28. Davidson, R. J. (2000). The functional neuroanatomy of affective style. In R. D. Lane & L. Nadel (Eds.), Cognitive neuroscience of emotion (pp. 106–128). New York: Oxford University Press.Google Scholar
  29. De Bruin, E. L., Ferdinand, R. F., Meester, S., de Nijs, P. F., & Verheij, F. (2007). High rates of psychiatric co-morbidity in PDD-NOS. Journal of Autism and Developmental Disorders, 37(5), 877–886.CrossRefPubMedGoogle Scholar
  30. Dombroski, B., Kaplan, M., Kotsamanidis-Burg, B., Edelson, S. M., Hensley, M. K., Sokhadze, E. M., et al. (2013). Effects of ambient prism lenses and visual-motor training on heart rate variability and behavioral outcomes in autism. In K. Siri & T. Lyons (Eds.), Cutting-edge therapies for autism (3rd ed., pp. 138–150). New York, NY: Skyhorse Publishing.Google Scholar
  31. Filippi, M. M., Oliveri, M., Vernieri, F., Pasqualetti, P., & Rossini, P. M. (2000). Are autonomic signals influencing cortico-spinal motor excitability? A study with transcranial magnetic stimulation. Brain Research, 881(2), 159–164.CrossRefPubMedGoogle Scholar
  32. Fitzgerald, P. B., Hoy, K., Gunewardene, R., Slack, C., Ibrahim, S., Bailey, M., et al. (2011). A randomized trial of unilateral and bilateral prefrontal cortex transcranial magnetic stimulation in treatment-resistant major depression. Psychological Medicine, 41(6), 1187–1196.CrossRefPubMedGoogle Scholar
  33. Friedman, B. H. (2007). An autonomic flexibility–neurovisceral integration model of anxiety and cardiac vagal tone. Biological Psychology, 74(2), 185–199.CrossRefPubMedGoogle Scholar
  34. Friedman, B. H., & Thayer, J. F. (1998). Anxiety and autonomic flexibility: A cardiovascular approach. Biological Psychology, 49(3), 303–323.CrossRefPubMedGoogle Scholar
  35. George, M. S., Lisanby, S. H., & Sackeim, H. A. (1999). Transcranial magnetic stimulation: Applications in neuropsychiatry. Archives of General Psychiatry, 56(4), 300–311.CrossRefPubMedGoogle Scholar
  36. Hedges, D. W., Salyer, D. L., Higginbotham, B. J., Lund, T. D., Hellewell, J. L., Ferguson, D., et al. (2002). Transcranial magnetic stimulation (TMS) effects on testosterone, prolactin, and corticosterone in adult male rats. Biological Psychiatry, 51(5), 417–421.CrossRefPubMedGoogle Scholar
  37. Hensley, M., El-Baz, A., Casanova, M. F., & Sokhadze, E. (2013). Heart rate variability and cardiac autonomic measures changes during rTMS course in autism. Applied Psychophysiology and Biofeedback, 38(3), 238.Google Scholar
  38. Hensley, M., El-Baz, A., Sokhadze, G., Sears, L., Casanova, M. F., & Sokhadze, E. M. (2012). TMS effects on cardiac autonomic control in children with autism. Psychophysiology, 49, S40.Google Scholar
  39. Hirstein, W., Iversen, P., & Ramachandran, V. S. (2001). Autonomic responses of autistic children to people and objects. Proceedings of the Royal Society of London B, Biological Sciences, 268(1479), 1883–1888.CrossRefGoogle Scholar
  40. Holsboer, F. (2000). The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology, 23(5), 477–501.CrossRefPubMedGoogle Scholar
  41. Hutt, C., Forrest, S. J., & Richer, J. (1975). Cardiac arrhythmia and behavior in autistic children. Acta Psychiatrica Scandinavica, 51(5), 361–372.CrossRefPubMedGoogle Scholar
  42. Jenkins, J., Shajahan, P. M., Lappin, J. M., & Ebmeier, K. P. (2002). Right and left prefrontal transcranial magnetic stimulation at 1 Hz does not affect mood in healthy volunteers. BMC Psychiatry, 2, 1–5.PubMedCentralCrossRefPubMedGoogle Scholar
  43. Julu, P. O., Kerr, A. M., Apartipoulos, F., Al-Rawas, S., Engerstrom, I. W., Jamal, G. A., & Hansen, S. (2001). Characterisation of breathing and associated central autonomic dysfunction in the Rett disorder. Archives of Disease in Childhood, 85(1), 29–37.PubMedCentralCrossRefPubMedGoogle Scholar
  44. Keck, M. E., Engelmann, M., Muller, M. B., Henniger, M. S., Hermann, B., Rupprecht, R., et al. (2000). Repetitive transcranial magnetic stimulation induces active coping strategies and attenuates the neuroendocrine stress response in rats. Journal of Psychiatric Research, 34(4–5), 265–276.CrossRefPubMedGoogle Scholar
  45. Khedr, E. M., Rothwell, J. C., Ahmed, M. A., & El-Atar, A. (2008). Effect of daily repetitive transcranial magnetic stimulation for treatment of tinnitus: Comparison of different stimulus frequencies. Journal of Neurology, Neurosurgery and Psychiatry, 79(2), 212–215.CrossRefPubMedGoogle Scholar
  46. Kleiger, R. E., Stein, P. K., & Bigger, J. T. (2005). Heart rate Variability: Measurement and clinical utility. Annals of Noninvasive Electrocardiology, 10(1), 88–101.CrossRefPubMedGoogle Scholar
  47. Klusek, J., Roberts, J., & Losh, M. (2015). Cardiac autonomic regulation in autism and Fragile X syndrome: A review. Psychological Bulletin, 141(1), 141–175.PubMedCentralCrossRefPubMedGoogle Scholar
  48. Kobayashi, M., & Pascual-Leone, A. (2003). Transcaranial magnetic stimulation in neurology. Lancet Neurology, 2(3), 145–156.CrossRefPubMedGoogle Scholar
  49. Kushki, A., Drumm, E., Pla Mobarak, M., Tanel, N., Dupuis, A., Chau, T., et al. (2013). Investigating the autonomic nervous system response to anxiety in children with autism spectrum disorders. PLoS One, 8(4), e59730. doi:10.1371/journal.pone.0059730.PubMedCentralCrossRefPubMedGoogle Scholar
  50. Lam, K. S., & Aman, M. G. (2007). The repetitive behavior scale revised: Independent validation in individuals with autism spectrum disorders. Journal of Autism and Developmental Disorders, 37(5), 855–866.CrossRefPubMedGoogle Scholar
  51. Lane, R. D. (2008). Neural substrates of implicit and explicit emotional processes: A unifying framework for psychosomatic medicine. Psychosomatic Medicine, 70, 213–230.CrossRefGoogle Scholar
  52. Lane, R. D., McRae, K., Reiman, E. M., Ahern, G. L., & Thayer, J. F. (2007). Neural correlates of vagal tone during emotion. Psychosomatic Medicine, 69, A-8.Google Scholar
  53. Le Couteur, A., Lord, C., & Rutter, M. (2003). The autism diagnostic interview-revised (ADI-R). Los Angeles, CA: Western Psychological Services.Google Scholar
  54. Levy, M. N. (1990). Autonomic interactions in cardiac control. Annals of the New York Academy of Sciences, 601, 209–221.CrossRefPubMedGoogle Scholar
  55. Loveland, K. A., Bachevalier, J., Pearson, D. A., & Lane, D. M. (2008). Fronto-limbic functioning in children and adolescents with and without autism. Neuropsychologia, 46(1), 49–62.PubMedCentralCrossRefPubMedGoogle Scholar
  56. Lydon, S., Healy, O., Reed, P., Mulhern, T., Hughes, B. M., & Goodwin, M. S. (2014). A systematic review of physiological reactivity to stimuli in autism. Developmental Neurorehabilitation. doi:10.3109/17518423.2014.971975.Google Scholar
  57. Malliani, A., Pagani, M., & Lombardi, F. (1994). Physiology and clinical implications of variability of cardiovascular parameters with focus on heart rate and blood pressure. The American Journal of Cardiology, 73(10), 3C–9C.CrossRefPubMedGoogle Scholar
  58. Mayberg, H. S. (2003). Modulating dysfunctional limbic-cortical circuits in depression: Towards development of brain-based algorithms for diagnosis and optimized treatment. British Medical Bulletin, 65, 193–207.CrossRefPubMedGoogle Scholar
  59. McPheeters, M. L., Davis, A., Nayarre, J. R., & Scott, T. A. (2011). Family report of ASD concomitant with depression or anxiety among US children. Journal of Autism and Developmental Disorders, 41(5), 646–653.CrossRefPubMedGoogle Scholar
  60. Mezzacappa, E., Kindlon, D., Saul, J. P., & Earls, F. (1998). Executive and motivational control of performance task behavior, and autonomic heart-rate regulation in children: Physiological validation of two-factor solution inhibitory control. Journal of Child Psychology and Psychiatry and Allied Disciplines, 39(4), 525–531.CrossRefGoogle Scholar
  61. Ming, X., Bain, J. M., Smith, D., Brimacombe, M., Gold von-Simson, G., & Axelrod, F. B. (2011). Assessing autonomic dysfunction symptoms in children: A pilot study. Journal of Child Neurology, 26(4), 420–427.CrossRefPubMedGoogle Scholar
  62. Ming, X., Julu, P. O., Brimacombe, M., Connor, S., & Daniels, M. L. (2005). Reduced cardiac parasympathetic activity in children with autism. Brain and Development, 27(7), 509–516.CrossRefPubMedGoogle Scholar
  63. Movius, H. L., & Allen, J. J. (2005). Cardiac vagal tone, defensiveness, and motivational style. Biological Psychology, 68(2), 147–162.CrossRefPubMedGoogle Scholar
  64. Pagani, M., Lombardi, F., Guzzetti, S., Rimoldi, O., Furlan, R., Pizzinelli, P., et al. (1986). lllPower spectral analysis of heart rate and arterial pressure variabilities as a marker of sympatho-vagal interaction in man and conscious dog. Circulation Research, 59(2), 178–193.CrossRefPubMedGoogle Scholar
  65. Palkovitz, R. J., & Wiesenfeld, A. R. (1980). Differential autonomic responses of autistic and normal children. Journal of Autism and Developmental Disorders, 10(3), 347–360.CrossRefPubMedGoogle Scholar
  66. Pascual-Leone, A., Walsh, V., & Rothwell, J. (2000). Transcranial magnetic stimulation in cognitive neuroscience—Virtual lesion, chronometry, and functional connectivity. Current Opinion in Neurobiology, 10(2), 232–237.CrossRefPubMedGoogle Scholar
  67. Patriquin, M. A., Lorenzi, J., & Scarpa, A. (2013a). Relationship between respiratory sinus arrhythmia, heart period, and caregiver-reported language and cognitive delays in children with autism spectrum disorders. Applied Psychophysiology and Biofeedback, 38(3), 203–207.CrossRefPubMedGoogle Scholar
  68. Patriquin, M. A., Scarpa, A., Friedman, B. H., & Porges, S. W. (2013b). Respiratory sinus arrhythmia: A marker for positive social functioning and receptive language skills in children with autism spectrum disorders. Developmental Psychobiology, 55(2), 101–112.CrossRefPubMedGoogle Scholar
  69. Porges, S. W. (2001). The polyvagal theory: Phylogenetic substrates of a social nervous system. International Journal of Psychophysiology, 42(2), 123–146.CrossRefPubMedGoogle Scholar
  70. Porges, S. W. (2003). The polyvagal theory: Phylogenetic contributions to social behavior. Physiology & Behavior, 79(3), 503–513.CrossRefGoogle Scholar
  71. Ridding, M. C., & Rothwell, J. C. (2007). Is there a future for therapeutic use of transcranial magnetic stimulation? Nature Review Neuroscience, 8(7), 559–567.CrossRefGoogle Scholar
  72. Rubenstein, J. L., & Merzenich, M. M. (2003). Model of autism: Increased ratio of excitation/inhibition in key neural systems. Genes, Brain, and Behavior, 2(5), 255–267.CrossRefPubMedGoogle Scholar
  73. Saha, S., Batten, T. F., & Henderson, Z. (2000). A GABAergic projection from the central nucleus of the amygdala to the nucleus of the solitary tract: A combined anterograde tracing and electron microscopic immunohistochemical study. Neuroscience, 99(4), 613–626.CrossRefPubMedGoogle Scholar
  74. Schaaf, R. C., Benevides, T. W., Leiby, B. E., & Sendecki, J. A. (2015). Autonomic dysregulation during sensory stimulation in children with autism spectrum disorder. Journal Autism and Developmental Disorders, 45(2), 461–472.CrossRefGoogle Scholar
  75. Seminowicz, D. A., Mayberg, H. S., McIntosh, A. R., Goldapple, K., Kennedy, S., Segal, Z., & Rafi-Tari, S. (2004). Limbic-frontal circuitry in major depression: A path modeling metanalysis. Neuroimage, 22(1), 409–418.CrossRefPubMedGoogle Scholar
  76. Shahrestani, S., Stewart, E. M., Quintana, D. S., Hickie, I. B., & Guastella, A. J. (2014). Heart variability during social interactions in children with and without psychopathology: A meta-analysis. Journal of Child Psychology and Psychiatry and Allied Disciplines, 55(9), 981–989.CrossRefGoogle Scholar
  77. Shekhar, A., Sajdyk, T. J., Gehlert, D. R., & Rainnie, D. G. (2003). The amygdala, panic disorder, and cardiovascular responses. Annals of the New York Academy of Sciences, 985, 308–325.CrossRefPubMedGoogle Scholar
  78. Smeekens, I., Didden, R., & Verhoeven, E. W. (2015). Exploring the relationship of autonomic and endocrine activity with social functioning in adults with autism spectrum disorders. Journal Autism and Developmental Disorders, 45(2), 495–505.CrossRefGoogle Scholar
  79. Sohn, J.-H., Sokhadze, E., & Watanuki, S. (2001). Electrodermal and cardiovascular manifestations of emotions in children. Journal of Physiological Anthropology and Applied Human Science, 20(2), 55–64.CrossRefPubMedGoogle Scholar
  80. Sokhadze, E. M., Baruth, J. M., Sears, L., Sokhadze, G. E., El-Baz, A. S., & Casanova, M. F. (2012). Prefrontal neuromodulation using rTMS improves error monitoring and correction functions in autism. Applied Psychophysiology and Biofeedback, 37(2), 91–102.CrossRefPubMedGoogle Scholar
  81. Sokhadze, E., Baruth, J., Tasman, A., Mansoor, M., Ramaswamy, R., Sears, L., et al. (2010). Low-frequency repetitive transcranial magnetic stimulation (rTMS) affects event-related potential measures of novelty processing in autism. Applied Psychophysiology and Biofeedback, 35(1), 147–161.PubMedCentralCrossRefPubMedGoogle Scholar
  82. Sokhadze, E. M., El-Baz, A., Baruth, J., Mathai, G., Sears, L., & Casanova, M. F. (2009). Effects of a low-frequency repetitive transcranial magnetic stimulation (rTMS) on gamma frequency oscillations and event-related potentials during processing of illusory figures in autism. Journal of Autism and Developmental Disorders, 39(4), 619–634.CrossRefPubMedGoogle Scholar
  83. Sokhadze, E., El-Baz, A., Sears, L., Opris, I., & Casanova, M. F. (2014). Neuromodulation based on rTMS improves electrocortical functional measures of information processing and behavioral responses in autism. Frontiers in System Neurosciences, 8, 134. doi:10.3389/fnsys.2014.00134.Google Scholar
  84. Thayer, J. F. (2015). A neurovisceral integration perspective. In The 46th annual meeting of the Association for Applied Psychophysiology and Biofeedback, Austin, TX, March 14. Google Scholar
  85. Thayer, J. F., & Friedman, B. H. (2002). Stop that! Inhibition, sensitization, and their neurovisceral concomitants. Scandinavian Journal of Psychology, 43(2), 123–130.CrossRefPubMedGoogle Scholar
  86. Thayer, J. F., & Lane, R. D. (2000). A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective Disorders, 61(3), 201–216.CrossRefPubMedGoogle Scholar
  87. Thayer, J. F., & Lane, R. D. (2005). The importance of inhibition in dynamical systems models of emotion and neurobiology. Brain and Behavioral Sciences, 28(2), 218–219.CrossRefGoogle Scholar
  88. Thayer, J. F., & Lane, R. D. (2009). Claude Bernard and the heart–brain connection: Further elaboration of a model of neurovisceral integration. Neuroscience and Biobehavioral Reviews, 33(2), 81–88.CrossRefPubMedGoogle Scholar
  89. Toichi, M., & Kamio, Y. (2003). Paradoxical autonomic response to mental tasks in autism. Journal of Autism and Developmental Disorders, 33(4), 417–426.CrossRefPubMedGoogle Scholar
  90. Udupa, K., Sathyaprabha, T. N., Thirthalli, J., Kishore, K. R., Raju, T. R., & Gangadhar, B. N. (2007). Modulation of cardiac autonomic functions in patients with major depression treated with repetitive transcranial magnetic stimulation. Journal of Affective Disorders, 104(1–3), 231–236.CrossRefPubMedGoogle Scholar
  91. Uijtdehaage, S. H., & Thayer, J. F. (2000). Accentuated antagonism in the control of human heart rate. Clinical Autonomic Research, 10(3), 107–110.CrossRefPubMedGoogle Scholar
  92. van Engeland, H. (1984). The electrodermal orienting response to auditive stimuli in autistic children, normal children, mentally retarded children, and child psychiatric patients. Journal of Autism and Developmental Disorders, 14(3), 261–279.CrossRefPubMedGoogle Scholar
  93. Wechsler, D. (2004). Wechsler intelligence scale for children-fourth edition integrated (WISC-IV Integrated). San Antonio, TX: Harcourt.Google Scholar
  94. Yoshida, T., Yoshino, A., Kobayashi, Y., Inoue, M., Kamakura, K., & Nomura, S. (2001). Effects of slow repetitive transcranial magnetic stimulation on heart rate variability according to power spectrum analysis. Journal of the Neurological Sciences, 184(1), 77–80.CrossRefPubMedGoogle Scholar
  95. Zahn, T. P., Rumsey, J. M., & Van Kammen, D. P. (1987). Autonomic nervous system activity in autistic, schizophrenic, and normal men: Effects of stimulus significance. Journal of Abnormal Psychology, 96(2), 135–144.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Yao Wang
    • 1
    • 2
  • Marie K. Hensley
    • 1
  • Allan Tasman
    • 1
  • Lonnie Sears
    • 1
  • Manuel F. Casanova
    • 1
  • Estate M. Sokhadze
    • 1
  1. 1.University of LouisvilleLouisvilleUSA
  2. 2.State Key Laboratory of Cognitive Neuroscience and LearningBeijing Normal UniversityBeijingPeople’s Republic of China

Personalised recommendations